Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

The Brain Resting-State Functional Connectivity Underlying Violence Proneness: Is It a Reliable Marker for Neurocriminology? A Systematic Review

The Brain Resting-State Functional Connectivity Underlying Violence Proneness: Is It a Reliable... behavioral sciences Review The Brain Resting-State Functional Connectivity Underlying Violence Proneness: Is It a Reliable Marker for Neurocriminology? A Systematic Review 1 , 1 2 2 Ángel Romero-Martínez * , Macarena González , Marisol Lila , Enrique Gracia , 3 3 3 Luis Martí-Bonmatí , Ángel Alberich-Bayarri , Rebeca Maldonado-Puig , 3 1 Amadeo Ten-Esteve and Luis Moya-Albiol Psychobiology Department, University of València, 46010 València, Spain; gonporma@alumni.uv.es (M.G.); Luis.Moya@uv.es (L.M.-A.) Department of Social Psychology, University of Valencia, 46010 València, Spain; Marisol.Lila@uv.es (M.L.); Enrique.Gracia@uv.es (E.G.) Biomedical Imaging Research Group (GIBI230), La Fe Health Research Institute, 46026 Valencia, Spain; marti_lui@gva.es (L.M.-B.); alberich_ang@gva.es (A.A.-B.); rebecagibi230@gmail.com (R.M.-P.); ten_ama@gva.es (A.T.-E.) * Correspondence: Angel.Romero@uv.es; Tel.: +3-496-386-4302; Fax: +3-496-386-4668 Received: 9 November 2018; Accepted: 11 January 2019; Published: 15 January 2019 Abstract: Introduction: There is growing scientific interest in understanding the biological mechanisms affecting and/or underlying violent behaviors in order to develop effective treatment and prevention programs. In recent years, neuroscientific research has tried to demonstrate whether the intrinsic activity within the brain at rest in the absence of any external stimulation (resting-state functional connectivity; RSFC) could be employed as a reliable marker for several cognitive abilities and personality traits that are important in behavior regulation, particularly, proneness to violence. Aims: This review aims to highlight the association between the RSFC among specific brain structures and the predisposition to experiencing anger and/or responding to stressful and distressing situations with anger in several populations. Methods: The scientific literature was reviewed following the PRISMA quality criteria for reviews, using the following digital databases: PubMed, PsycINFO, Psicodoc, and Dialnet. Results: The identification of 181 abstracts and retrieval of 34 full texts led to the inclusion of 17 papers. The results described in our study offer a better understanding of the brain networks that might explain the tendency to experience anger. The majority of the studies highlighted that diminished RSFC between the prefrontal cortex and the amygdala might make people prone to reactive violence, but that it is also necessary to contemplate additional cortical (i.e., insula, gyrus [angular, supramarginal, temporal, fusiform, superior, and middle frontal], anterior and posterior cingulated cortex) and subcortical brain structures (i.e., hippocampus, cerebellum, ventral striatum, and nucleus centralis superior) in order to explain a phenomenon as complex as violence. Moreover, we also described the neural pathways that might underlie proactive violence and feelings of revenge, highlighting the RSFC between the OFC, ventral striatal, angular gyrus, mid-occipital cortex, and cerebellum. Conclusions. The results from this synthesis and critical analysis of RSFC findings in several populations offer guidelines for future research and for developing a more accurate model of proneness to violence, in order to create effective treatment and prevention programs. Keywords: anger state; brain; inmates; mental illness; resting functional connectivity; violence Behav. Sci. 2019, 9, 11; doi:10.3390/bs9010011 www.mdpi.com/journal/behavsci Behav. Sci. 2019, 9, 11 2 of 19 1. Introduction There is growing scientific interest in understanding the biological mechanisms affecting and/or underlying violent behaviors, in order to develop effective treatment and prevention programs [1–3]. In this regard, the relatively recent appearance of the field of neurocriminology represents an important advance in our understanding of these problems by applying the neuroscientific perspective to their study. In fact, neurocriminology aims to establish the neurobiological basis for crime and violence. Specifically, this neuroscientific subdiscipline has incorporated several tools and/or procedures, such as neuroimaging techniques, genetic markers, and hormonal measurements, among others, to predict these antisocial behaviors [3]. Neuroimaging techniques are non-invasive, and make it possible to visualize brain structures and functional connectivity in brain networks, thanks to their good spatial and functional resolution. Indeed, functional magnetic resonance imaging (fMRI) has offered insight into the functional synchrony between brain structures, that is, how the activation of several brain structures is temporally coordinated [4,5]. These techniques have usually relied on showing changes in the activation of different brain networks by analysing the blood oxygen level-dependent (BOLD) presented in these brain regions, which is especially sensitive to the increase in blood flow in the cerebral capillaries of the activated neuronal regions [6,7]. Studies using fMRI to assess brain networks have demonstrated that altered functional connectivity across distant brain regions might make individuals prone to violence [8–15]. In fact, most of the research in this field has highlighted that the alteration in the cerebral connectivity between the key nodes involved in emotional and cognitive behavioral regulation might explain this proneness to violence. Particularly, the inhibitory malfunction of the frontal lobe (i.e., prefrontal structures, frontal gyrus . . . ) would lead to an overactivation of the limbic system (i.e., amygdala, hypothalamus, hippocampus . . . ), which under certain stimuli might facilitate impulsive and/or reactive violence. In this regard, it has been suggested that the activation of frontal structures facilitates self-regulation and control over emotion-related behaviors by attenuating limbic responses to emotional stimuli and/or the context [8–15]. By contrast, several authors demonstrated that individuals characterized by predatory and instrumental violence (proactive) might present normal prefrontal cortex (PFC) functioning, and an increase in dorsolateral PFC activation has even been described during emotion processing tasks in these individuals [16–19]. Furthermore, studies have indicated that the reduction in amygdala activation during emotion processing might be characteristic of instrumental violence [19]. In this case, unimpaired or even higher frontal activation is related to the ability to control impulses and/or emotional processing, but also to certain alterations in empathic abilities. Unfortunately, the majority of the previously mentioned studies analyzed the functional activation of these brain structures in response to certain tasks (i.e., exposure to a stimulus, emotional induction tasks . . . ), and so little is known about whether these brain structures and their connections in the absence of external stimulation might be employed as reliable markers of proneness to violence. In recent years, neuroscientific research has not only been interested in brain functioning during a task, but it has also focused on the intrinsic activity within the brain at rest without any external stimulation (resting-state functional connectivity; RSFC). In this direction, several studies have demonstrated the existence of resting intrinsic brain connectivity (networks) when an individual is awake and alert [20–22]. Synchronicity across a group of distant brain regions during resting periods has been called the default mode network (DMN; precuneus/posterior cingulate cortex, medial PFC and medial, lateral, and inferior parietal cortex). Although it has been suggested that the DMN is relatively deactivated during a demanding task [23–25], some authors have maintained that it might make an active contribution to cognitive processing [26,27], or even be important for cognitive abilities [28–30] or a correlate of certain personality traits [31,32]. With regard to the aforementioned, it should be mentioned that the activation of individual brain structures that encompass the DMN does not necessarily mean that the DMN is activated. In fact, it is necessary to consider how these brain structures establish and maintain networks with other brain structures outside the DMN during Behav. Sci. 2019, 9, 11 3 of 19 the resting state. Since evidence about whether the DMN or other brain networks might be important in violence proneness is less clear, it would be important to summarize the main results of this field of research. In light of the above, this review aims to highlight the association between the RSFC among specific brain structures and the predisposition to experiencing anger and/or responding to stressful and distressing situations with anger. Specifically, we will focus on the following concepts related to violence: reactive violence (characterized by impulsivity, emotional drive, and lack of self-control); proactive violence (characterized by planning, high awareness of the purpose of this conduct, and low emotionality); trait anger (frequency of experiencing feelings of anger); and anger expression (frequency of externally and/or internally manifesting angry feelings). The present study will first describe the main findings on the association between RSFC and self-reported anger in non-violent normative individuals and in others with mental disorders. Then, we will describe the association between RSFC and changes in anger levels after laboratory tasks in non-violent and violent populations. Next, with the main purpose of analyzing whether these connections could be employed as reliable markers of violence proneness, we will analyze the RSFC in highly violent populations (i.e., young offenders, inmates, and soldiers) in comparison with non-violent individuals. Finally, considering the existing data, we will discuss the implications for clinical practice and further research. 2. Methods Search Strategy A literature search on the existence of a relationship between brain RSFC and proneness to violence was carried out following the PRISMA quality criteria for reviews [33], using the following digital databases: PubMed, PsycINFO, Psicodoc, and Dialnet. The search terms were the following: Resting functional connectivity or resting fMRI or default mode network) and (violence or aggressive or anger). All of the papers that were selected for final inclusion met the following criteria: (a) they employed fMRI techniques to assess brain RSFC; (b) they were empirical studies; (c) they involved research with human subjects; and (d) they were written in English. Moreover, other criteria were not common to all of the papers, as they either: (a) examined anger through self-reports; (b) examined aggressive behavior through laboratory tasks; (c) examined RSFC in highly violent populations; (d) or assessed the relationship (i.e., correlational, regression analysis . . . ) between RSFC and aggressive behavior as a trait and/or response to a laboratory task. Articles mentioning RSFC or aggressive behavior separately, but without examining the relationship between the two, were excluded. Moreover, studies were excluded if they did not directly examine anger or anger expression (i.e., externalizing behaviors, but not aggressive, criminal records . . . ), or they did not explicitly mention that the participants were highly violent (PRISMA flow diagram; Figure 1). Article selection was entrusted to two researchers. In cases of disagreement, a third member of the team helped them reach a consensus. Behav. Sci. 2019, 9, 11 4 of 19 Figure 1. Flow chart of literature search with reasons for exclusion. 3. Results After a systematic scientific literature search, we identified 181 abstracts, of which 34 texts were fully read because they seemed to present all of the inclusion criteria. Ultimately, only 17 of these papers were included in the review (Figure 1). In all, 17 studies investigated the relationship between brain RSFC and several aspects of violence proneness (e.g., self-reported anger, changes in anger levels after a laboratory task-paradigm, or brain RSFC in a highly violent population). First, we will present the association between RSFC and self-reported anger in a non-violent normative population, followed by groups of non-violent patients with several mental disorders or brain damage (e.g., schizophrenia, bipolar disorder, attention deficit hyperactivity disorder (ADHD), and individuals with brain damage from traumatic brain injury). It should be noted that three studies mainly focused on the association between the RSFC and self-reported anger in carriers of specific alleles, and so we described the association by mentioning the specific allele subgroup. Third, we will describe whether brain RSFC predicts anger level changes after a laboratory method for inducing anger in a non-violent normative population, as well as in violent groups. Finally, we will describe the RSFC in different samples of highly violent populations (young offenders, inmates, and impulsive/violent soldiers). The main characteristics of the participants in each study are summarized in Table 1 (age, gender, education level, drug use, and handedness). Behav. Sci. 2019, 9, 11 5 of 19 Table 1. Main sociodemographic characteristics and details about the participants in each study and the assessment methods used. ADHD: attention deficit hyperactivity disorder, fMRI: functional magnetic resonance imaging, TBI: traumatic brain injury. Handedness Violent Behavior Methods of Authors Sample Characteristics Age Gender Education Drug Use (Right/Left) Assessment Analysis Park et al. Healthy young children (n = 79) 6.06  0.96 49% 51%  - - - Child Behavior Checklist Seed-based (2018) [34] Fulwiler et al. Spielberger State–Trait Anger Healthy males (n = 16) 34  14.42  - No current drug use Right-handed ROI (2012) [35] Expression Inventory-2 Abram et al. Psychiatry healthy sample Externalizing Spectrum 26 50% 50%  - No current drug use Right-handed ICA (2015) [36] (n = 244) Inventory, brief form Klasen et al. Buss–Perry Aggression Healthy young adults (n = 83) 23.8  3.6  - - Right-handed ROI (2018) [37] Questionnaire Buss–Perry Aggression Antisocial personality disorder Kolla et al. 36.2  8.7 Questionnaire subjects (n = 21)  - No current drug use - ROI (2018) [38] 34.2  7.7 Reactive–Proactive Controls (n = 19) Aggression Questionnaire Patients with schizophrenia or 36.7  10.5 88% 12% Buss Perry Aggression Hoptman et al. schizoaffective disorder (n = 25) 12.3  2.1 (years) Questionnaire CPZ equivalents - ROI (2010) [39] 15.5  3.0 (years) Life history of aggression Controls (n = 21) 40.4  10.8 76% 24% Number total of arrests Unmedicated female patients 26.7  6.4 Wagner et al. 12.1  1.6 (years) Buss–Perry Aggression with BPD (n = 33)  No current drug use . ROI (2018) [40] 11.8  1.5 (years) Questionnaire Controls (n = 33) 26.4  6.2 48h free of Hasler et al. ADHD (n = 30) 38.7  9.9 70% 30% Spielberger State–Trait Anger CO challenge - methylphenidate Right handed (2017) [41] Controls (n = 15) 32.2  5.5 26% 73% Expression Inventory-2 regressor before fMRI Veterans males with TBI (n = 24) Buss–Perry Aggression McGlade et al. 37.75  9.59  14.33  2.10 (years) Veterans females with TBI - - QuestionnaireDisplaced Seed-based (2015) [42] 40.0 11.15 15.06  2.51 (years) (n = 17) Aggression Questionnaire Retired athletes with a history of Goswami et al. 50  12 17  1.8 Personality Assessment multiple concussions (n = 19);  No current drug use - Seed-based (2016) [43] 46  10 16  1.9 Inventory (aggression scale) Controls (n = 17) Dailey et al. Adults with TBI (n = 17) 21.86  2.79 26% 73% Buss–Perry Aggression - - - ROI (2018) [44] Healthy controls (n = 17) 23.88  3.26 29% 71% Questionnaire Spielberger State–Trait Anger Gilam et al. > secondary Brain functional Soldiers (n = 60) 18.62  0.88  No current drug use Right-handed Expression Inventory (2017) [45] education parcellation Geneva Emotion Wheel Buades-Rotger Social Threat Aggression Healthy young women (n = 39) 23.22  3.2 - No current drug use Right-handed ROI et al. (2018) [46] Paradigm Behav. Sci. 2019, 9, 11 6 of 19 Table 1. Cont. Handedness Violent Behavior Methods of Authors Sample Characteristics Age Gender Education Drug Use (Right/Left) Assessment Analysis Siep et al. Violent offenders (n = 18) 35.17  7.12 Current alcohol use - - Seed-based (2018) [47] Non-offender controls (n = 18) 37.06  15.24 No current drug use Chen et al. Young violent offenders (n = 30) 16.06  0.7 16.06 7.76  2.2 - Right-handed - ROI (2015) [48] Controls (n = 29)  0.4 10.06  0.0 Violent inmates of maximum 36.8 12.0 Leutgeb et al. 11.3  1.7 (years) security prison (n = 31)  Non-medicated Right-handed - Seed-based (2016) [49] 11.6  1.0 (years) Controls (n = 30) 35.1  9.0 Impulsive and violent soldiers Varkevisser et al. 36.54  6.27 67,9% middle Interviews and criminal (n = 28)  - - ROI (2017) [50] 34.53  7.59 53,3% middle records Controls (n = 30) Behav. Sci. 2019, 9, 11 7 of 19 3.1. Normative Population (Self-Reported Aggression) One study investigated whether RSFC was associated with trait anger in normative children (both genders). Its authors concluded that low functional connectivity between the bilateral amygdala and ventromedial prefrontal cortex (vmPFC) was related to higher levels of trait aggression (assessed by the Child Behavior Checklist), but this relationship did not remain significant after controlling for family income and maternal education [34]. Another study with young adults added to the previous results by studying whether the amygdala also presented connections with other prefrontal cortex (PFC) structures that facilitate proneness to experiencing anger feelings. In fact, Fulwiler, King, and Zhang [35] studied whether the amygdala’s functional connectivity with other PFC structures predicted trait aggression in young men. These authors demonstrated that, in men, low RSFC between the amygdala (bilateral) and left orbitofrontal cortex (OFC) was associated with high trait anger (measured by the State-Trait Anger Expression Inventory 2, STAXI-2), especially for the right amygdala and left middle orbitofrontal cortex (mOFC). Conversely, the high functional connectivity between these brain structures was related to high anger control-out; in other words, the higher the association between these two brain structures, the greater the effort to control the expression of anger toward others (persons or objects) [35]. Finally, the interconnections between the amygdala and the PFC have not only been studied as facilitators of anger. Abram, Wisner, Grazioplene, Krueger, MacDonald, and DeYoung [36] conducted a study with a relatively larger sample of healthy young adults (of both genders). They assessed whether RSFC was associated with several facets of callous aggression (assessed by externalizing spectrum inventory), such as relational, physical, and destructive aggression. In this regard, they concluded that there was a positive association between the anterior insula, ventral striatum (VStr), and anterior cingulate cortex (ACC), connectivity and physical aggression. However, they also found a negative association between anterior insula and OFC connectivity and physical aggression and destructive aggression. 3.2. Self-Reported Aggression Mediated by Genetic Markers Two studies included genetic markers as mediators of the relationship between RSFC and trait aggression in a sample of young males. One of these studies concluded that Monoamine oxidase A-L (MAOA-L) carriers (in comparison with MAOA-H carriers) showed that a higher RSFC between the ventromedial prefrontal cortex (vmPFC) and the right angular gyrus (AG), posterior cingulate cortex (PCC), and dorsomedial prefrontal cortex, was related to higher aggression traits. Nevertheless, when the RSFC between the vmPFC and bilateral supramarginal gyrus was high, the aggressive traits were low [37]. The other study revealed that in participants with antisocial personality traits with the MAOA-L variant, high RSFC between the ventral striatal and angular gyrus was related to high proactive aggression [38]. 3.3. Mental Disorders (Self-Reported Aggression) In order to avoid biased results, it is important to consider whether and how these variables are related in a normative population and in people with mental disorders, in order to be able to generalize the conclusions to the entire population. For example, in schizophrenic patients, low functional connectivity (bilaterally) between the amygdala and the ventromedial prefrontal cortex (vmPFC) was related to a higher total score on the Buss–Perry Aggression Questionnaire (BPAQ), a life history of aggression, and the total number of arrests. However, the functional connectivity between the bilateral amygdala and the bilateral orbitofrontal cortex (OFC), supragenual cingulate, subgenual cingulate, or dorsolateral prefrontal cortex (DLPFC) regions was unrelated to the aforementioned aggressive behavior scales in schizophrenic patients. These results remained significant even after controlling for the patients’ diagnosis (schizophrenia and schizoaffective disorder), age, and neuroleptic medication dosage [39]. Behav. Sci. 2019, 9, 11 8 of 19 Nevertheless, not all of the studies considered the connections between the amygdala and the PFC. Specifically in bipolar disorder, the assessment of functional connectivity and the BPAQ total score in a group of women with borderline personality disorder demonstrated that low functional connectivity between the serotonergic nucleus centralis superior (NCS) and the frontopolar cortex (FPC) was associated with higher BPAQ total scores in unmedicated bipolar patients. However, the RSFC between these brain structures was unrelated to a control group [40]. In ADHD patients, a study demonstrated that higher connectivity between the right hippocampus, the parietal lobe (supramarginal and angular gyrus), and the frontal lobe (superior and middle frontal gyrus) in carriers of the AG or GG variant of rs8079626 within the BAIAP2 gene (brain-specific angiogenesis inhibitor) was related to higher anger expression-out (or an unmanageable tendency to manifest anger externally) in ADHD patients [41]. In patients with brain damage after traumatic brain injury (TBI), the reduction in the functional connectivity between the left orbitofrontal cortex (OFC) and the left angular region was related to higher scores on the BPAQ physical aggression subscale in male veterans with TBI. Moreover, high RSFC between the right OFC and the right cerebellum and right angular gyrus was related to high scores on the Displaced Aggression Questionnaire (DAQ) Revenge Planning scale in this group. Conversely, connectivity between the right OFC and the right mid occipital cortex was negatively correlated with the scores on the DAQ Revenge Planning scale. Finally, it should be noted that the frontal cortex (FC) of these brain regions was unrelated to BPAQ and/or DAQ scores in female veterans with TBI [42]. Although a study that analyzed the RSFC of a group of retired athletes with a history of multiple concussions failed to find a significant relationship between the RSFC of the bilateral anterior temporal lobe (ATL) and the bilateral medial orbitofrontal cortex (mOFC) and the PAI aggression subscale [43], a recent study demonstrated that in a group of adults with TBI, high RSFC between the right hippocampus and midcingulate cortex was associated with elevated BPAQ scores. However, in a control group, higher self-reported aggression was associated with low RSFC between the right hippocampus and midcingulate cortex, as well as between the right hippocampus and mPFC [44]. Finally, it should be noted that the majority of the studies that analyzed the associations between brain RSFC and violence-related concepts found significant results related to the BPAQ questionnaire [39,40,42,44], but they failed to find these associations on other self-reports such as the PAI. In this regard, a possible explanation for this difference would be that the BPAQ is a self-report to analyze violence-related concepts, unlike the PAI (e.g. total score consists of the average of approximately 29 items), which is a broader personality self-report with only a few questions about violence. 3.4. Laboratory Assessment of Aggression The assessment of anger expression under controlled laboratory conditions offers an interesting alternative to self-reports, although these methods also have some limitations, such as artificial conditions, social biases, the simplification of violence measurement, etc. However, they offer complementary information to self-report assessments of violence-related concepts. 3.4.1. Non-Violent Groups A group of men were submitted to a modified version of the Ultimatum Game, which was employed to induce anger. During this laboratory task, participants have to split a specific amount of money with another player by using negotiation strategies. However, the other player breaks the rules of the game and confronts his opponent directly and insults him/her. Participants experienced an increase in the right amygdala and right inferior frontal gyrus (IFG) functional connectivity after this laboratory task, which, in turn, was associated with higher trait anger scores. Moreover, it should also be noted that individuals with high pre-task functional connectivity in the right amygdala had low anger levels during the task [45]. Behav. Sci. 2019, 9, 11 9 of 19 Another study analyzed whether being exposed to a modified version of a reaction time task (Social Threat Aggression Paradigm) to promote anger induction would produce changes in the RSFC among different brain structures in a sample of healthy young women. On this task, participants had to punish an opponent if he/she (loser) presented longer reaction times than the participant (winner). The punishment consisted of an aversive tone whose intensity was manipulated by the winner. The authors concluded that although the resting functional connectivity (before the laboratory task) among the basolateral amygdala (BLA), the medial orbitofrontal cortex (mOFC), and the lateral orbitofrontal cortex (OFC) (bilaterally) was unrelated to the anger levels in the Social Threat Aggression Paradigm (a laboratory task), participants who presented higher increases in BLA–mOFC connectivity after the task showed a less aggressive response to this task [46]. Moreover, high baseline RSFC between the BLA and the left superior temporal gyrus (STG) was correlated with high aggression levels on the laboratory task. By contrast, high basal connectivity between the BLA and the superior parietal lobule (SPL) was associated with lower aggression [46]. 3.4.2. Violent Group Two groups of men (reactive violent offenders and non-violent offenders) participated in a laboratory task to promote different emotional states (they had to pay attention to several audiotaped angry, happy, and/or neutral stories). This is an adapted version of the Anger Articulated Thoughts during Simulated Situations (ATSS) paradigm for fMRI. Authors of the study concluded that before the emotional task, reactive violent offenders showed a heightened RSFC between the left medial PFC (mPFC) and the left amygdala, as well as a diminished pre-task RSFC between the left amygdala and the uncus/amygdala and posterior insula. After the emotion task, violent offenders showed a significant decrease in the RSFC between the left mPFC and the left amygdala, but non-offender controls experienced an increase in RSFC. Furthermore, an increase was found in the RSFC between the left amygdala and the right posterior insula and right superior temporal gyrus in violent offenders after the task, but the control group showed a decreased RSFC between the left amygdala and the right posterior insula and right superior temporal gyrus, as well as the left uncus/amygdala [47]. 4. Violent Populations Finally, in order to complete the previously mentioned results, it is important to analyze whether individuals with a proneness to expressing anger present alterations in the RSFC among the brain structures that have been identified as responsible (at least in part) for violence-related concepts. First, violent juvenile offenders showed significantly lower resting regional connectivity between the following brain structures and their adjacent structures: the right caudate, right medial prefrontal cortex, and left precuneus. However, significantly higher RSFC was also found between the right supramarginal gyrus and its adjacent brain structures, compared to the non-violent control group [48]. One study compared the RSFC of a group of violent inmates to that of a non-violent group, and they concluded that the violent offender group showed an increase in the RSFC between the left amygdala and the right cerebellar hemisphere. Furthermore, these violent offenders also presented an increase in the RSFC with the dorsolateral prefrontal cortex (DLPFC) (bilateral). Nonetheless, inmates showed a decrease in RSFC between the left/right cerebellar hemisphere and the left/right orbitofrontal cortex (OFC), as well as between the vermis and the left OFC [49]. Varkevisser, Gladwin, Heesink, van Honk, and Geuze [50] compared the RSFC of a group of aggressive and impulsive soldiers to a non-violent group. Although no significant group differences in functional connectivity were found between the orbitofrontal cortex and basolateral amygdala, significant patterns of connectivity were found in impulsive and aggressive soldiers. First, these authors concluded that the left dorsolateral prefrontal cortex presents a negative association with the (bilateral) basolateral amygdala. Nevertheless, they found a positive association between the left centromedial (CeM) amygdala and a region spanning the left fusiform gyrus and lingual gyrus, as well as between the left anterior cingulate cortex (ACC) and a region spanning the left cuneus, calcarine cortex, Behav. Sci. 2019, 9, 11 10 of 19 and superior occipital cortex. Furthermore, they also found a positive association between the right ACC and a region spanning the left cuneus, calcarine cortex, superior occipital cortex, and precuneus. Finally, they demonstrated a positive relationship between the left anterior insular cortex (AIC) and the right temporal pole. However, in the control group, the associations among these brain structures presented the opposite connectivity pattern. 5. Discussion The results described here offer a better understanding of RSFC that might explain proneness to violence, particularly the neural pathways that underlie key variables of violence, such as reactive and proactive violence, trait anger, and anger expression and/or control. It should be noted that only one study failed to find a significant association between the RSFC of the bilateral anterior temporal lobe and mOFC and the anger trait; the other 16 manuscripts did find a significant association between these variables. Even though several studies highlighted that the diminished RSFC between the PFC and the amygdala increased proneness to reactive violence, we also summarized other brain networks that include additional cortical (i.e., insula, gyrus (angular, supramarginal, temporal, fusiform, superior and middle frontal), ACC, and PCC) and subcortical brain structures (i.e., hippocampus, cerebellum, ventral striatum, and nucleus centralis superior) that might facilitate the onset of this type of violence. Moreover, we also described the neural pathways that might explain proactive violence and feelings of revenge, which are focused on the RSFC between the OFC, ventral striatal, angular gyrus, mid-occipital cortex, and cerebellum (Table 2). Initially, we concluded that the diminished RSFC between frontal structures such as the PFC (OFC and vmPFC) and frontopolar cortex (Brodmann area 10; PFC), limbic structures such as the amygdala and the anterior insula, parietal cortex regions such as the supramarginal gyrus (Brodmann area 40; parietal lobe), the angular region (posterior to the supramarginal gyrus), and the nucleus centralis superior (median raphe nucleus; brainstem) was related to a high predisposition to experiencing anger and/or responding to stressful and distressing situations with anger (high anger expression-out and low control-out) in a normative population and in participants with mental disorders. As previously stated, it appears that prefrontal structures tend to maintain inhibitory projections to other brain structures involved in emotional reactivity, such as the amygdala and/or the insula, and so the failure to regulate this reactivity might lead to high irritability or hostile reactions [8–15]. Although these studies did not analyze the RSFC between these brain structures, all of the manuscripts that were included in this systematic review found a diminished RSFC connectivity between the PFC and amygdala, which has been associated with proneness to experiencing feelings of anger and difficulties in controlling anger expression [34,35,39,46,47,50]. In fact, alterations in the dorsal and ventral PFC, amygdala, and angular gyrus have commonly been associated with rule-breaking behaviors, alterations in moral judgement and reasoning, and emotion regulation [8]. In this regard, we reinforced the hypothesis that diminished RSFC between the frontal and limbic systems might be characteristic of violent populations, since one of the studies that was included in this review concluded that a group of violent and impulsive soldiers presented a lower RSFC between the left dorsolateral PFC and the basolateral amygdala (bilateral) than a non-violent group [47,50]. Conversely, research conducted with normative young adults demonstrated that individuals with higher RSFC between the mOFC and the basolateral amygdala showed less aggressive strategies on an anger induction laboratory task [46]. Moreover, another study stated that reactive violent offenders presented a diminished RSFC between the left mOFC and left amygdala, but an increase in paralimbic RSFC after an emotion induction task [47]. Behav. Sci. 2019, 9, 11 11 of 19 Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: ventromedial prefrontal cortex. Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: ventromedial prefrontal cortex. Left mOFC Left amygdala Before emotional induction task (violent offenders) ventromedial prefrontal cortex. Left mOFC Left Lef unc t a u my s/ag my dag la d ala ⬆ Before emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left amygdala Functional Before emotional induction task (violent offenders) Brain Structure (From) Brain Structure (To) Functional Connectivity Aggression Assessment Brain structure (from) Brain structure (to) LefP t o u snc ter u is o/ra i my nsu gld aa la Aggression assessment ventromedial prefrontal cortex. Left mOFC Left amygdala Before emotional induction task (violent offenders) Left amygdala cF ounc nnetc it o ina vitly ⬇ ⬆ Before emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Brain structure (from) Left mOF Bra Ci n structure (to) P Lef oster t ai my or g ins da u ll aa Aggression assessment Af ter emotional induction task (violent offenders) Trait aggression Trait aggression Lef cot nn unc ecu tisv /a itmy y gdala ventromedial prefrontal cortex. Lef Lef t a t my mOF gda Cl a Left amygdala ⬆ Bef Befo or re emo e emoti tio ona nal l i indu nduc ct ti io on n t ta as sk k ( (v vi io ol lent ent o of ff fender enders s) ) Left mOFC Rig Fht Lef unc p t o ta is o my ter naig lo da r il ns a ula ⬇ After emotional induction task (violent offenders) Brain structure (from) Brain structure (to) Posterior insula Aggression assessment Trait aggression Left amygdala After emotional induction task (violent offenders) Left mOFC Left mOFC ⬇ ⬆ Trait aggr ⬆ Tr ession ait aggression Lef cot nn unc ecu tisv /a itmy y gdala Right R isg uht per pio o srter temp ior io ns rau l lg ay rus Amygdala (bilateral) Amygdala (bilateral) Left mOFC Left mOFC Lef t amygdala Left ⬆a mygdala Before emo ⬆ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Lef Lef t a t my mOF gda Cl a FLef unc t ta io my nag l dala ⬇ Bef After ore emo emoti ti o o na na ll i i n ndu ducc ti ti o o n n ta ta ss k k ( ( vi vi o o ll ent ento o ff ff ender ender ss )) Left amygdala ⬇ After emotional induction task (violent offenders) vmPFC Lef vmP t mOF FC C ⬇ ⬇ ⬆ Trait aggr ⬆ ⬆ Tr Tr ession a ai it t a ag gg gr res ess si io on n Posterior insula Trait aggrB es ra siio n ns tructure (from) Brain structure (to) Aggression assessment Amygdala (bilateral) Violent populations (no-self reported) Right superior temporal gyrus Left uncus/amygdala Left uncus/amygdala connectivity vmPFC Right posterior insula Nucleus centralis superior (median raphe ⬇ ⬆ Trait aggression Left amygdala Left amygdala ⬇ Before emo ⬇ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Lef Lef t a t my mOF gda Cl a Left amygdala ⬇ Af After ter em emo oti tio ona nal l i indu nduc cti tio on n ta tas sk k ( (vi vio ol lent ent o of ff fender enders s) ) Nucleus centralis superior (median raphe nucleus) VioFr lent ontopolar pC op au ul d aa ti te o cortex ns nu (c no leu -(Br s sel (Lef r fodmann ir gep ht) t mOF o rted) Car ea 10) ⬇ ⬆ Trait aggr ⬆ Tr ession ait aggression Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Posterior insula Posterior insula Trait aggression Right superior temporal gyrus Amygdala (bilateral) Nucleus centralis nu su cp leu ers io ) r (median raphe Left mOFC Left mOFC Lef t amygdala Left ⬆a mygdala Before emo ⬆ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Right posterior insula CaudmP ate F nu C c (lreu ight) s (r ig vmP ht) FC Adjacen ⬇ t structures ⬇ ⬆ Trait aggression Young violent offenders Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Left mOFC Left mOFC Lef t amygdala Left ⬇a mygdala After em ⬇ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) Violent populLef atio t ns amy (no g- da sel la Lef f rep t mOF orted) C ⬇ ⬆ ⬆ Trait aggression After emotional induction task (violent offenders) vmPFC nucleus) Bilateral supramarginal gyrus Trait aggression vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Left uncus/amygdala Left uncus/amygdala Amygdala (bilateral) Right superior temporal gyrus Nucleus centralis superior (median raphe PmP recu Fneu C (rs ig (ht) left) Adjacent structures ⬇ Young violent offenders Left amygdala Left amygdala ⬇ Before emo ⬇ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Right posterior insula Right posterior insula vmPFC ⬇ ⬆ Trait aggression CauF dr ao te nto nu pc o lleu ars c (o rr ig tex ht) ( Brodmann area 10) ⬇ ⬆ Trait aggression AmyvmP gdala F C (r ight) Bi Inf laer ter io ar l s fr uo p nta rama l gy rg ru ina s (lr g ig yht) rus ⬇ ⬆⬆ Tr Tr aa it it aa gg gg rr es es ss io io n n Posterior insula Poster ⬆ ior insula Left amygdala Left amygdala ⬆ After em ⬆ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) Amygdala (right) Violent pInferior opulations fr ontal (no-sel gyr f rep us or (right) ted) Trait aggression nucleus) Suprama Precu rgin neu al g s y (l ref us t) ( right) Adjacent structures ⬆ Young violent offenders Table 2. Resting functional con Ta nec ble tivit 2.y Re aR n st id g in ht it gs sfunct u ro ple er iin io or n a temp a nl gc eo o rn rpr a n lec o gn y tivit r en uses y. a m nR d OF ig it ht C: s r s o m ule ped er in iia o r a l n temp og rb er it o o pr rfr ao lo n g n y en tra u es l sc .o m rtex OF , C: OF m C: ed oia rblit o o rfr bit on ofr tao l n co ta rl tex co,r t P ex FC: , OF prC: efro orn btit ao l fr co o rn tex tal , c vo m rtP ex FC: , PFC: prefrontal cortex, vmPFC: Nucleus centralis superior (median raphe mPFC (right) Adjacent structures Young violent offenders Amygdala (right) Infer Ang ior u fr la or nta gylr g uy s r(u ri sg (ht) rig ht) ⬆ ⬆ Trait aggression Left mOFC Left mOFC Lef t amygdala Left ⬇a mygdala After em ⬇ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) CauF dr ao te nto nu pc o lleu ars c (o rr ig tex ht) ( Brodmann area 10) ⬇ ⬆ Trait aggression vmPFC Su Rig pht ra ma cerr ebe gBi in lla la a lter rg hem y arlu ssu i s (p p rr iher g aht) ma e rginal gyrus Adj Lef act ent ⬇a my str g u da ctu lar es ⬆ ⬆ Trait aggression Young Vio vi lent olent inm of aftes ender s Violent populations (no-self reported) Vio lent popuAngular lations (no gyr -sel us f rep (right) orted) nucleus) Precuneus (left) ventromedial prefrontal cortexv . entromedial prefrontal cortex. vmPFC Pos Ang terio ur l a cri ng gyu ru la sted (rig cht) ortex ⬆ ⬆ Trait aggression Right posterior insula Right posterior insula mPFC (right) Adjacent structures ⬇ Young violent offenders Amygdala (right) Bi R la ig ter hta c l er cer ebe ebe Il nf la ll er r a r hem io hem r fr is oip nta sher pher l e g y e rus (right) Lef Bila t ter amy al g O da FC la ⬆ ⬆ Trait aggression V Vi io ol lent ent i inm nma ates tes ⬆ ⬇ Left amygdala Left amygdala ⬆ After em ⬆ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) vmPFC Caudate nucleus (right) C Posterior audate nucingulated cleus (right) cortex Trait aggression vmPFC SupramargBi inla alter gy arlu ssu (p rr ig aht) ma rginal gyrus Adjacent structures ⬆ Trait aggression Young violent offenders ⬇ ⬆ vmPFC Poster Do io rr s o cme ingdi ula alted PFC co r tex ⬆ ⬆ Trait aggression Right superior temporal gyrus Right superior temporal gyrus Precuneus (left) Bilateral cerebellar hemisphere Func Bilatter iona al lO FC Functional Violent inmates CerebellarAng veru m lis ar gyrus (right) Left OFC ⬇ ⬇ Violent inmates mPFC (right) mP Dorsomedial FC (riAdj ght) a cen PFC t structures Adjacen ⬇ t structures ⬇ Young violent offenders Young violent offenders Right cerebellar hemisphere Left amygdala Violent inmates Bra Am in s ytg rda uct la ur (e ri g (fro ht)m ) Brain struc Inf tur er e B i o ra (fro r ifn rm osnta t )r uc l g tur yre u s (t ( or)i ght) Brain st⬆ r ucture (to) ⬆ Ag⬆ g re Tr sa siito a n ga gs rs es es ss io m ne nt Aggression assessment Anger expression Dorsomedial PFC Violent populations (no-self reported) Vio lent populations (no-self reported) Supramarginal gyrus (right) Adjacent structures Young violent offenders vmPFC Posterior cingulated cortex connectivity connectivity ⬆ Trait aggression Lef Ct er do ebe rslo la la rter ver al m Pis F C Right do Lef ⬆r st oO laF ter C al PFC ⬆ ⬇ V Vi io ol lent ent i inm nma ates tes Precuneus (left) Precuneus (left) Left mOFC Left mOFC Left amygdala Left amygdala Before emotional induction task Bef (vio olrent e emo offti ender onal si)ndu ction task (violent offenders) Bilateral cerebellAng ar hem ulairs p gher yrue s (right) Bila⬆ ter al OFC ⬆ ⬇ Violent inmates Anger expr Am essy io gn da la (bilateral) Left mOFC ⬇ Anger control-out Anger expression Caudate nucleus (right) Caudate nucleus (right) ⬇ Right cerebellar hemisphere Left amygdala ⬆ Violent inmates Trait aggression Trait aggression Dorsomedial PFC Amyg Lef dat lado ba rs so ol la ater tera al l ( P bi FC la teral) R Lef ight t do do rr ss oo la la ter ter aa l lP P FF C C ⬇ ⬆ Impulsive Vio al nd ent ai g nm gres ates sive group Supramarginal gyrus (right) Supramarginal g Adj yrua sc ( ent rig ht) str uctures Adjacent ⬆ structures ⬆ Young violent offenders Young violent offenders Left uncus/amygdala Left uncus/amygdala vmPFC CerebelP la or s ter ver io m r is ci ngulated cortex Lef ⬆ t OFC ⬇ ⬆ Trait aggression Violent inmates Amygdala (bilateral) Left mOFC ⬇ Anger control-out mPFC (right) Pari mP etaF l C (s u (r p iAdj g ra ht) ma a cr en gitn s atr l u and ctur aes ng ular gyrus) Adjacen ⬇ ⬇ t structures ⬇ Young violent offenders Young violent offenders Left amygdala Bilater Lef alt ca er my ebe gda llal ra hem isphere Bilateral OFC Before emo ⬇ tional induction task Bef (vio olrent e emo offti ender onal si)ndu Vc io tilo ent n ta inm sk ( a v tes iol ent offenders) Anger expression ⬇ ⬇ Amygdala (bilateral) Amygdala bas Left olater mOFC al Lef (bilt amOF teral)C Lef Lef t Lef t do fut ⬇ rss mOF io fo la rter m gy Ca l P ru Fs C ⬇ ⬇ Anger contr ⬆ Tra ol-out it aggression Impul⬆ si ve Traa ind t ag a gg rg es res sio sn ive group Right cerebellar hemisphere Right cerebellar hem Lef is t p aher mye g dala Left ⬆a mygdala ⬆ Violent inmates Violent inmates Do Po rs ster ome iodi r ia ns l P uF la C Posterior insula Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates H Am ipp yg oda camp la (u bi sl a (r ter ight) al) Lef Am t P cF a en y r ro i g tr et nta da o ame ll la ( l s( o di u bi be ( p a lr a la ter a s ma my ua pl rer ) g g d iin o aa r l a la a nd nd mi ang ddl ule ar fr g oy nta rul s ) ⬆ ⬆ Anger expression-out Impulsive and aggressive group Precuneus (left) Precuneus (left) ⬆ Cerebellar vermis Left OFC ⬇ Violent inmates Amygdala (bilateral) Left mOFC vmPFC LefLi t f vmP ng u⬇ ⬇ su ifa o F lr C g m gy yrusr us ⬇ ⬇⬆ Ang Traer it a cg og ntr res os li-o on ut ⬆ Trait aggression Bilateral cerebellar hemisphere Bilateral cerebellar hem Bila is ter pher al O e FC Bila⬇ ter al OFC ⬇ Violent inmates Violent inmates Anger expressio Lef n t mOFC Left mOFC Left amygdala Left amygdala After emotional induction task (vi Af oter lent em ofo fti ender onal si)n duction task (violent offenders) Amygdala basolateral (bilateral) Left dor ⬇s olateral PFC ⬇ ⬇ Impulsive and aggressive group Hippocampus (right) Parietal Left cF en r (supramar o tr nta ome l lo di be ( al a ginal smy uper g gy d iand o r au r l a s a )nd angular middle frontal ⬆ ⬆ Anger expression-out Impulsive and aggressive group Supramarginal gyrus (right) Supramarginal g Adj yrua sc ( ent rig ht) str uctures Adjacent ⬆ ⬆ structures ⬆ Young violent offenders Young violent offenders Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Nucleus centralis superior (median Nr u ac p leu he s centr Pa arliiet s a su l p (ser up io rr a ma (me rg di in an al ra and phe angular gyrus) Li Lef ngt uc au l neu gyru s s Cerebellar vermis Cerebellar vermLef is t OFC Lef ⬇ t OFC ⬇ Violent inmates Violent inmates Right posterior insula Right posterior insula Amygdala (bilateral) gyrus) Left mOFC Left fu⬇ s iform gyrus ⬇ Anger control-out Proactive aggression Frontopolar cortex gy r(u Br s)o dmann area F r1 o0 nto ) polar cortex ⬇ (Brodmann area 10) ⬇ ⬆ Trait aggression ⬆ Trait aggression Right cer Lef ebe t lmOF lar hem C isphere Right Lef cert ebe mOF llarC hem Lef Lef is t t p a aher my mye g g da dal la a Lef Lef t amy t ⬆a my gda glda a la Before emo ⬆ tional V indu iolent ctioin nm taa stes k (Bef v ioo lent re emo offender tionals ) i ndu Vic otlient on tia nm sk a (v tes io lent offenders) ⬆ ⬆ Left amygdala Amyg Lef dalt aa ba my so glda ater la al (bilateral) Left dorsolateral PFC After emotional induction task (vi Af oter lent em ofo fti ender o Ina mp l s u i)ndu l sive cti ao nd n ta ag sg kr (es vis o il ve ent gr oo fu fender p s) HippocampusH (right) ippocampus (right) Left cF en ro tr nta ome l lo di be ( al a smy uper gd io ar l a a nd middle frontal ⬆ ⬆ Anger ⬆ ⬇ expression-out Impulsive and aggressive group nucleus) Left anter nu ior c lc eu ing s)u late cortex Left Lef ca⬆ lc t a cr u ine neu cs o rtex ⬆ ⬆ Anger expression-out Impulsive and aggressive soldiers Left dorsolateral PFC Left dorsola Rter ight al do PFC rs olateral PFC Right dorsolateral PFC Violent inmates Violent inmates Right superior temporal gyrus Right superior ⬆ temp oral gyrus ⬆ Frontal lobe Pariet (superior al (suprama and rgimiddle nal and a fr ng ontal ular gyrus) Lingual gyrus Proactive aggV res entr sioa nl striatal Angular gyrus Bilateral cerebellar hemisphere Bilateral cerebellar hem Bila is ter pher al O e FC Bila⬆ ⬇ ter al OFC ⬇ ⬆ Pr V oia oclt ent ive ia nm gga res tes s ion Violent inmates Left uncus/amygdala Left uncus/amygdala Left fusiform gyrus gyrus) Left superior occipital cortex vmPFC Left antervmP ioBi r c la i F ng ter C u alla s te u p cr oa rma tex rginal gyrus BilaterLef al st ucp ar ⬇ la c a ma rine rgic na orltex gy rus ⬇ ⬆ ⬆ Trait aggression Impul⬆ si ve Tr aa nd it a ag gg grres esssiio ve n soldiers Left amygdala Left amygdala Before emotional induction task (Bef vioo lent re emo offender tionals ) i nduction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: med⬇ ia l orbitofrontal cortex, OFC: ⬇ o rbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Violent Am p yo gp da ulla at iba ons so ( la no ter -sa el l f ( bi rep later o V rited) o al l) ent p Am oLef py ug l t a da c ten io la ns tr ba o (me no sol - di a sLef el ter alf a a t rl ep my do (bi o r g r l sa d ted) oter a la la ter a l)a l PFC Left dor ⬇s olateral PFC ⬇ Impulsive and aggressive group I Imp mpu ul ls si ive ve a and nd a ag gg gr res ess si ive ve g gr ro ou up p Hippocampus (right) Frontal lo gyr be (us) superior and middle frontal Lef ⬆t cuneus ⬆ ⬆ Anger expression-out Ventral striatal Angular gyrus ⬆ Proactive aggression Physical aggC res ers ebe ionl lar vermis Cerebellar ver Pm osLef is ter it oO r F ins C ula PosterLef io ⬆r t ins OF uC la Violent inmates Violent inmates ⬇ ⬇ Lingual gyrus Proactive aggression Left superior occipital cortex Amygdala (right) Amygda Inf laer (riio grht) fro ntal gyrus (right) Inferior frLef onta ⬆t c l u gneu yrus s ( right) ⬆ ⬆ Trait aggression ⬆ Trait aggression Caudate nucleus (right) Caudate nucleus Lef (rigt ht) fug si y fr ou rm gy s) rus Left fusiform gyrus Left anterior cingulate cortex ventromedLef ial t p cr aefr lcao rin ne tac l o cro tex rtex . ⬆ Impulsive and aggressive soldiers Left mOFC Left amygdala ⬆ Before emotional induction task (violent offenders) Physical ag Lef gres t do Lef sO io r F n s t C o mOF l ( alter eft) C a l PFC Lef Lef t do t mOF rsola RC ter iLef g ht a Lef l t do P ang t FC r as my u olla ag rter da reg alla i o Pn F C RLef ight t a do my ⬇r sg oda later la al PFC After emotiona ⬆l P iV n hy du io slic ent cti ao l n a inm g ta gr s a es k tes ( svi iAf oo nl ter ent em off oender tionals ) i ndu Vc io tilo ent n ta inm sk (a vi tes ol ent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: med⬆ ⬇ ia l orbitofrontal cortex, OFC: ⬇ o r⬆ b itofrontal cortex, PFC: prefrontal cortex, vmPFC: Proactive aggression Left centromedial amygdala Left centromedial amygdala Lef ⬆t cuneus ⬆ Impulsive and aggressive group Impulsive and aggressive group Lef Lef t p t r cecu uneu neu s s Ventral striatal Ang Ang ular u g la yrr u gy s r (u ris g ht) Angular ⬆ g yrus (right) ⬆ Proactive aggression Lingual gyrus Lingual gyrus mPFC (right) mPFC (right) Adj acent structures Adjacent ⬇ str uctures ⬇ Young violent offenders Young violent offenders Proactive aggression Right anterior cingulated cortex Left superior occipital cortex ⬆ Impulsive and aggressive soldiers Left uncus/amygdala OFC (left) Left angular region ⬇ ⬆ Physical aggression Amygdala basolateral (bilateral) Amygdala basolaR Lef ter iga t ht ldo (p bi r ol ss a o ter ter later ia olr )a ilns Pu FC la Rig Lef ht p t do oster r ⬇s o io la rter ins au l l P aF C ⬇ Impu⬆ ls i P ve hya snd ica la a gg gg res res si sve ion gr o u p I mp u l s i ve a nd a g g r es si ve g r o u p Left anterior cingulate cortex ventromedLef ial t p cr aefr lcao rin ne tac l o cro tex rtex . ⬆ Impulsive and aggressive soldiers Left mOFC Left mOFC Left amygdalLef a Lef t ca t lp ca recu rine Lef neu c t oa rs my tex g dala ⬆ ⬆ Before emotional inductiBef on o ta re emo sk (vio ti lent ona l o f indu fender ctio s) n task (violent offenders) Physical aggressio vmP n FC Left vmP amy Pg o Fs da C ter la i or cingulated cortex PosterF io unc r ci⬆ ng ti ou na lalted cortex ⬇⬆ ⬆ Trait aggression Bef ore emotional ⬆ indu Trac it t ia og n gtra es sk s i(o vn io lent offenders) Anter Left aimy or ig ns da ulla a Left amygdala OFC After emotional induction task (vi Af ol ter ent em off oender tionals ) i nduction task (violent offenders) ⬇ ⬆ ⬆ Ventral striatal Precuneus (left) Precuneu Angular s (left) gyr Left us cuneus Left cuneus Proactive aggression Ventral striatal Right anterior cingulAng ated uc la or r tex gyr us Lef ⬆t cuneus ⬆ ⬆ Proactive aggression Impulsive and aggressive soldiers Brain structure (from) Brain structure (to) Posterior insula Aggression assessment Right superior temporal gyrus Right superior temporal gyrus ⬆ ⬆ Des Phy tru sic cta ive l a g ag grg es res sis oin on Left fusiform gyrus Left fusiform gyrus Left superior occipital cortex Left uncus/aLef myt gLef s du ap lt a er c a io lc Lef ra o rict ne cu ip nc cio ta u rl tex s c /a o my rtex g dala OFC (left) Lef Dot ra so ng me uldi ara r l eg PF io Cn Do cor nn soe me ⬇ c tidi via ty l P FC ⬆ Physical aggression Anterior insula OFC Lef Left t a cnter entrio ome r cidi ng au l a la my te c go d ra tex la Lef Left t a cnter entrio ome r cidi ng Lef au l a la t my te ca c lg c o d a ra r tex ilne a cortex Left ca⬇ ⬆ lc arine cortex ⬆ Imp Imp uu ls ls ive ivea a nd nd a a gg gg rr es es ss ive ive s g or ldi ou er ps Imp Imp uu ls ls ive ivea a nd nd a a gg gg rr es es ss ive ive s g or ldi ou er ps SupramaLef rgit nmOF al gyr C u s (right) SupramarLef gint amOF l gyru C Adj s ( Lef ra ig ct ent ht) amy str g u da ctu lar es AdjLef acLef ent t a t my ⬆ ⬆ sp tr ru ecu gc da tu neu lra es s Befo ⬆r e emo ⬆ tio Y na ou l ng indu vic otlient on to afsfk ender (v Bef iolo sent re emo offender tiY oo na us ng l) i ndu vioc lent tion otfa fs ender k (vio sl ent offenders) Physical aggression Left amygdala Left amygdala Func⬆ ti onal ⬇ ⬆ ⬇ Before emotional inductiBef on o ta re emo sk (vio ti lent ona l o f indu fender ctio s) n task (violent offenders) Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Violent populations (no-self repoV rted) iolent populations (no-self Li rep ng ou rted) al gy rus Lingual gyrus ⬆ Destructive aggression Physical aggression Ventral striatum Right anterior cingulated cortex Left cuneus Impulsive and aggressive soldiers Brain structure (from) Brain structure (to) Posterior Lef insu t lsa u perior oc Pc o is pter itailo c ro ir ns tex u la ⬆ Aggression assessment Ang Traiter a g ex gr p es res sis oin o n Anger expression Anterior insula ⬆ ⬆ P Phy hys si ic ca al l a ag gg gr res ess si io on n Left superior occipital cortex Left superi⬆ o r occipital cortex Right cerebellar hemisphere Right cerebellar hemis Lef pher t ae my gdala Lef Left t a cmy alca gr da ine lac ortex Violent inmates Violent inmates OFC (left) Lef Lef t t ua nc ng uu sl /a ar my reg gd io an la Left co unn ncu e⬆ s c / ta iv my ityg dala ⬆ ⬆ Physical aggression Anterior insula OFC Right pos⬇ ter ior insula Anter Vientr or ca ing l str ulia ate tum co rtex ⬇ Caudate nucleus (right) Caudate nucleus (rigLef ht) t cuneus Left cuneus Left amygdala Left amygdala Left precuneus Before emotional induction task (v Bef iolo ent re emo offender tionasl) i nduction task (violent offenders) Left mOFC Left mOFC Left amygdala ⬇ Left amygdala ⬇ ⬇ ⬇ After emotional inductioAf n ta ter sk em (vi oo ti lent onal o i fn fender ductio s) n task (violent offenders) Amygdala (bilateral) Am Lef yg t da amy la ( g bi da la lter a Lef Lef al) t t mOF mOFC C Left mOFC ⬆ ⬆ Des ⬇⬆ Ang Tr tru aer i ctt ia ve cg og ntr a rg es o gs lri-es o on u s Af i t o ter n emotional⬇ indu Ang cer tio c no ta ntr sk o l(-vi ou ot lent offenders) OFC (left) Anterior insula Left angular region ⬇ ⬇ ⬇Physical ⬆ P aggr hysiession cal aggression Left cuneus Lef ⬆t cuneus Bilateral cerebellar hemisphere Bila Rter ight al a cer nter ebe io lr la c ri ng hem uP li a Bi o ste s p lter a d her ter c io o e a r r ltex iO ns F u C la Left Bi P su o lp s ater ter eriio a ol rr O o ins c FcC iu p lia t al cortex ⬆ Violent inmates ImpulV siive olent and inm agg ar tes ess ive soldiers Trait aggression ⬇ ⬇ Amygdala (bilateral) Right superior temporal gyrus ⬆ Physical aggression Reveng Lef e fe t e alnter ing mP s io F r C ci ( ng rig uht) late cortex Left amP nter FiC o r( r cAnter iig ng ht) Lef Adj u la t io a te cc ra en c c lc i o ng a tr r tex sitr u ne lu ac c te tu or cr tex o es rtex Adj Lef act en ca t ls ctr ar u ine ctuc ro es rtex Impu Y ls oiu ve ng a nd vio a lent ggres off sender ive sos ldi ers Imp Yo uu ls ng ive vi ao nd lent ago gfr fes ender sives s oldiers Left ca⬆ ⬇ lc arine cortex ⬇ ⬆ Right posterior insula Right posterior insula Anterior insula vmP OFC FC ⬇ ⬇ ⬆ Trait aggression Parietal (suprV ama entr rg ailn s a tr l ia and tum ang ulP ar a r g iy et ra uls ()s upramarginal and angular gyrus) Left precuneus Left precuneus Left mOFC Left mOFC Left amygdala Left amygdala After emotional induction task (vi Af olter ent em offo ender tionasl) i nduction task (violent offenders) Cerebellar vermis Left amygda Cler a ebellar ver Lef mis t a Lef my Lef t g t mOF da OF la C C Left ⬇ ⬇ O FC ⬆ ⬇⬇ ⬆ ViAf olent ter iem nm oa ti tes ona l inductioAf n ta ter sk V em ( ivi oo lo ent ti lent ona inm l o i fndu f aender tesc tio s) n task (violent offenders) Anterior insula Violent populations (no-OFC self reported) ⬇ Physical aggression ⬆ Des ⬆ Destr Tr tru ai cttuctive ia ve gg a rg es gsaggr ries on sio ession n Revenge feeliP Anter ng recu s neu ior isns (lu ef lt) a Precuneu Lef s (t lef su t) p erior occipital cortex Left superi⬆ o r occipital cortex ⬆ Physical aggression Right anter Lef iort c mOF inguC la ted cortex Right anter Lef iot r mOF cingu R C lLef ia gte ht t d a cc my er or ebe tex gda l lu la m Left suLef pert io ⬆ ⬆ ar my ocg cda ipilta a l cortex Before emo ⬆ ⬆ Imp tiu ona lsive l indu and c ta ig og n rtes assk ive (v is Bef o ollent di orer e emo osf fender Imp tio u na s ls ) ilve indu and ct i ao g n gr ta es sk si ve (vi o so lent ldier of sf enders) Amygdala (bilateral) Right superior temporal R giy g rht us s uperior temporal gyrus Nucleus centr Hipa plo is c a smp uper ui so (rr i(g me ht) di an raphe Hip Fp ro onta camp l lAnter o u be ( s (rs iig u oht) p r er ci ng ioru a la nd te mi cor ddl texe F fr ro onta ntall lobe (superior and middle frontal ⬆ Anger expression-out ⬆ Anger expression-out ⬆ ⬆ Right OFC Left calcarine cortex Left ca⬆ lc arine cortex ⬆ Revenge feelings Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left dorsolateral PFC Left dorsolaterR a Ri lig g P ht ht FC do p vmP ors ster olF a iC o ter r i ans l P uF la C RiR giht ght do pro ss o⬆ ter l ater iora i lns PF uC la ⬆ Violent inmates Violent inmates CaudaF te ro nu nto clp eu ols a r ( V rc i entr g or ht) tex a l ( sBr trio adma tum nn area 10) ⬇ ⬆ ⬆ Tr Tra ai it t a ag gg gr res ess si io on n Supramarginal gyrus (right) Supramarginal gyrR Adj uis g ( ht a r Lef ic g a ent ht) ng t c u u str l neu au r cg tu sy r ru es s Adjacent Lef ⬇ s t tr cu uc neu turs es Young violent offenders Young violent offenders Lef Rt ig uht nc c uer s/ebe amy llg ud m a la Left unc⬆ u s/amygdala ⬆ Left amygdala Left amygdala After emotional induction task (vi Af olter ent em offo ender tionasl) i nduction task (violent offenders) Anterior insula Violent populations Ventral (no-V sel istriatu o fl r ent epo pro mAnterior ted) pul ations (no cingulate -self repo cortex rted) ⬆ ⬆ Physical aggression Anter nuic o lr eu ins s) ula gyrus) g⬆ y rus) ⬆ Physical aggression Revenge feelingR s ight OFC Left superior occipital cortex Left superior occipital cortex Left amygdala Left amygdala ⬆ ⬇ Before emo ⬇ tiona⬆ l iR ndu evenge ction fee tas li k ng (v siBef olent ore emo offender tiona s) l induction task (violent offenders) Right superior temporal gyrus Right superior temporal gyrus Amygdala basolateral (bilateral)Am ygdala basolatera Lef l (bi t do later rso alla ) teral PFC Left dorsol⬇ a teral PFC ⬇ Impulsive and aggressive groupI mpulsive and aggressive group Nucleus centralis superior (median raphe mPFC (r Anter ight) ior cingulate cortex Adjacent structures ventromedial p⬇ refr ontal cortex. Young violent offenders Right cer Lef ebe t lmOF lar hem C isphere Right cerebellar hem Rig iLef Lef Lef s ht pher t a t t p ng a ar my my eecu ula g gneu r da da gl l y a a s r us Lef Lef t at my ⬆ p rg ecu daneu la s Before emotional V indu iolent ctioin nm taa stes k (v iolent offenders) V iolent inmates Right OFC Right P m ositer doic o cri p ins itau l lc ao rtex Poster ⬆ ⬆ ior insula ⬆ ⬇ Revenge feelings Caudate nucleus (right) Caudate nucleus (right) Proactive aggressvmP ion FC Proactive aggrF es ro sinto oBi n l p ao ter lar a lc s ou rtex pra ma (Bro rg dma inalnn gya ru rea s 10) ⬇ ⬆ Trait aggression Right anterior cingulated cortex Right anterior cingu Rlia gte ht d cc er or ebe texl lum ⬇ ⬆ ⬆ Impulsi⬆ ve Tr and ai t aa gg gg rr es es ss ive ion s oldiers Impulsive and aggressive soldiers Violent populations (no-self repor V ted) iolent populations (no-self reported) Revenge feelings nucleus) Left fusiform gyrus Left fusiform gyrus Revenge feelings Precuneus (left) Right OFC Lef Left t u cnc alc u asr/ia ne my co gr d tex ala Left ca⬆ lc arine cortex ⬆ Revenge feelings LaborBi ato larter y ta als c kLef er R iebe gt ht mOF l lO ar F C hem C isphere Bilateral cerebe Left llmOF aR r ihem ght CLef Bi m isl p ia t do her ter amy cc a eil p g O ida ta FC ll a c ortex BiLef later t ⬆ ⬇ ⬇ a a my l Og Fda C la After ⬇ ⬇ em otional⬇ i V n Rdu ie o venge lc ent tion inm f ta ee s a lk tes ing (vi so Af lent tero em ffender otiona s)V l iin odu lent cti inm on ta ates sk (violent offenders) Left centromedial amygdalmP a FC Lef (rit gcht) en tromedial amP myF gC da (lra ig ht) Adjacent structures ⬆ Adjacent structur⬇ es ⬆ Impul⬇ si ve and aggressive Yo u gr ng ou vi pI o mp lent ulo sifve fender ands a Y go gu res ng s ivi ve o lg ent rouo p f fenders Ventral striatal Ventral striata Ang l ular gyrus Angular gyrus Am Lef yt ga da my lag (da riglht) a Infer R io ig rht fr o anta ngu l lg ay r rg u y sr ( u rs ig ht) ⬆ ⬆ ⬇ Bef Func ore emo ⬆t ionati l ona ⬆ P l⬆ r i o ndu Tr aa ct ic i tve ta io g a n gg rtes g ar ss es k io ( sn v io io nl ent offender ⬆s ) P roactive aggression Caudate nucleus (right) Caudate nucleus (rLi igng ht)u al gyrus Lingual gyrus vmPFC SupramarginBi a Lef l lg ater y t r su u R as p li g ( er sr u ht iig p o ht) c r ra er o ma c ebe cirp g li lit u na am l lc g oy rtex rus Lef Adj t su ap cer ent i⬇ o s r tr ou cc citu pirtes al cortex ⬆ ⬆ Trait aggression Young violent offenders Brain structure P (fro oster m)i or insula Brain structure (to) Aggression assessment Laboratory tC as er kebe llar vermis Cerebella Lef r ver t R sim u gp ht is er p Lef io or s t ter temp OiF oC ro ir ns alu g la y rus Right Lef po t ⬆ ⬇ s O ter FC io r insula ⬇⬆ Aggressive Vs itr ola ent tegiinm es (a la tes bo ratory task) Violent inmates Right cerebellum Precuneus (left) Precuneus (left) Right OFC ⬆ ⬆ Revenge feelings Physical aggress R io ig n ht OFC Physical aggression RiAng ght m ulia do r g cy cr ip uista (r l ic go ht) rtex ⬆ connectivity ⬇ Revenge feelings Left amygdala Left amygdala ⬆ After ⬆ em otional induction task (vioAf lent tero em ffender otiona s) l induction task (violent offenders) Right OFC mPFC (right) mPFC (right) Adj acent structures Adjacent structures Revenge Young feelings violent offenders Young violent offenders Left mOFC Left mOFC Lef Lef t a t my cuneu gda sl a Left amygda Lef lat cu ⬇ neus Befor⬇ e emo tional inducBef tion orte emo ask (vti io olna ent l io ndu ffender ction s)t ask (violent offenders) Amygdala (right) Right cerebella Inf r hem er R io ig r iht sfp r o her anta ngeu l lg ay r rg u y sr ( u rs ig ht) Left amy ⬆ ⬆ gdala ⬆ ⬆ ⬆ Trait aggression Violent inmates Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Am Left ydo gda rs lo a lba ater so alla P ter FC al Left dorsoR lLef a iter ght R t a s i l g s u u P ht pp F er er C do i o imOFC o r rs r temp o temp later o a o rlr a a P l lF g g C yy r r uu ss RiR giht ght su do per rs io ⬆ o ⬆l r a temp teral o Pr F aC l gyrus ⬆⬆ Aggressive Vs itr ola ent tegiinm es (a la tes bo ratory task) Violent inmates Right angular gyrus Supramarginal gyrus (rig Su ht) p ramarginal gyrus (right) Adj acent structures Adjacent structur⬆ es ⬆ Young violent offenders Young violent offenders Labora Ta torble y ta s 2k . O Re vmP FC st in (F lef C gt) funct iona Tr l a cio t n an gg ec res tivit sion y O a Fn Cd P (o lit ef ster s Lef t)r io o t le r a ng c in ing u a lu a n r la g rted e eg r ipr o cn oo r tex nen es. mOFC: Lef m t a ed ng ⬇ ⬆ ia u lla o r rrb eg itio ofr n ontal cortex, OFC: o⬇ r bitofron ⬆ t⬆ P a hy l Tr cs a o iic r ta ta ex lg ag ,g rP g es r F es sC: io sin o pr n efrontal cor⬆ tex Phy , v sm ica P lF aC: ggression ⬆ Aggressive strategies (laboratory task) Precuneus (left) Precuneus (left) ⬇ Left anterior cingulate cortex Left anterior cingulLef a Lef tet t cu o cnc a rtex lc u asr /ia ne my co gr d tex ala Left uncus Lef /amy t ca gld ca ar l⬆ a ine cortex ⬆ Impulsive and aggressive soldier Imp s ulsive and aggressive soldiers Right OFC Bilateral cerebella RriAng g hem ht m u il sia p do rher g cy ce r ip u ista (r l ic go ht) rtex Bilater ⬆a l OFC ⬇ ⬇ Revenge feelings Violent inmates Right posterior insula Violent Am p yo g Am p da ull y a ag t iba da ons s lo a ( lba a no ter s -o sa el lla f ( ter bi rep l aa lter o rted) a V l) i o Am lent yg pda oplu al a ba tis oo ns la ter ( no Su Lef a-lp s ( el er t bi do fil o r aep r ter r mOFC sp o o a a lra l rted) )iter et a a ll lP oF bu Cl e Left dorso⬇ la teral PFC ⬇ Impulsive and aggressive group Impulsive and aggressive group Left amygdaR lai ght cerebe Lef llt aa r my hem gda isp la her R ig eht cerebellar hemisphere Left amygdala Left amygdala ⬆ Before emotiona ⬆l inducBef tion orte emo ask (vti io olna V ent il o i lo ndu ent ffender ic nm tion a stes )t as k (violent Vi o of lent fender inm s) a tes ⬇ ⬇ Left amygdala Left su Do per rsio ome r temp dial o PrF aC l g yrus Lef⬆ t mOFC After⬆ em Ag og ti ro es na s ⬆ il ve P indu hy str si a c cteg ti ao l n a ies g ta g ( r sles k a bo ( svi io ro n alto ent r y o ta ff s ender k ) s ⬆ ) P ⬆ hy Tr s a ic it a l a g a g g g r es r es s is o i o n n Right OFC Right midoccipital cortex ⬆ ⬆⬇ Ag Revenge gressive feelings strategies (laboratory task) Supramarginal gyrus (right) Lef Su t p mOF rama Cr gina Lef l gy t r s Adj u us p ( er arc iient g oht) r o s c tr cu ip citu tar l es co rtex v en Lef tLef rt oa m t my sed u Adj g pia da er a l ilc o a p ent r r o efr ⬇ cs c tr o ip u n ic tta tu all r cc es oo r r tex tex . Young vio Bef lent ore emo offender tios na l inductY io o n ut ng as k vi (o vlient olent of f o ender ffender s s) Posterior insula Posterior insula ⬆ ⬆ ⬆ Laboratory task vmPFC CerebellaP r o ver ster m io isr cingulated cortex Lef⬆ t OFC ⬆ Trait aggression Violent inmates Anterior insula Am Anter ygda R io lia g r ht (ibi ns s lu a uter la per ailo )O r F temp C oral gyrus OFC ⬇ Caudate nucleus (right) Caudate nuc lSu eu Lef p ser (t riifo g u r ht) s p ifa o r rim gy etal lr o u bu s le Left fusif⬇ o rm gyrus ⬇ Bilateral cerebellar hemis Bi plher ater ea l cerebellar hemisphere Bilateral OFC Bilateral OFC Violent inmates Violent inmates ⬇ ⬇ Anger exp Am ress y ig oda n la basolateral vmPFC ⬇ ⬆ Destructive aggression ⬆ Des ⬆ tr Tr u a citti ve ag g ar g es gr ses ios n io n Left centromedial amygdala Left centromedial amygdmOFC ala ⬆ ⬆ Impulsive and aggressive group Impulsive and aggressive group Right cerebellar hemisphere Right cerebellar hemLef ispher t amy e gdala Left amygdala Violent inmates Violent inmates Left mOFC Left mOFC Lef Lef t a t my cuneu gda sl a Left Lef unc t a u my s/ag my da Lef g la d t a clu ⬆ a neu s After ⬆ emotional inducti Af on ter ta s em k (o vi tio olna ent l io nfdu fender ction s )ta sk (violent offenders) Left dorsolateraDo l PF rs C o medial PFC Right dors⬇ o lateral PFC ⬇ Violent inmates Laboratory task Violent populations (no-self reported) Left superior temporal gyrus ⬆ ⬆ ⬆ Aggressive strategies (laboratory task) mPFC (right) mPFC (rig Adj ht) Li a ng cen uta s ltr gu yc ru tu sr es Adj Ling acu en a ⬇ ⬇l t g sy tr ru uc stu res ⬆⬇ Ag gres Yso ive ung str vi ao teg lent ieso (flfa ender borato s ry task) Young violent offenders Left amygdala Before emotional induction task (violent offenders) Functional ⬇ Cerebellar vermis Cerebellar vermis Left OFC Left OFC ⬇ ⬇ Violent inmates Violent inmates Amygdala (bilateral) Nucleus centralis sup er Su io p V r er entr (Lef me ior a di t p lmOF a a sr n tr iet ira a a C tu p l he lm obu le Ventra ⬇l striatum ⬇ Anger control-out Left precuneus Posterior iLef nsu t lp ar ecuneus Bilater Bra al i n cer stebe rucltlur are hem (froim sp )her e Bilateral cerebellar hem BraBi iin s lp a ster her truc ae lt O urF eC ( to) Bilater ⬇a l OFC ⬇ AggV re is os lent ion ia nm sseastes sm ent Violent inmates Anger exp Am ress y ig oda n la basolateral Right posterior insula Right posterior insula CauP d Anter r aecu te nu neu ioc rl i eu sns (l su ef (lr t) ai g ht) AmygdalAnter a P r ba ecu soineu lo arter ins s a (lu l ef (lbi a t) l amOFC teral) Frontop Lef olat r do cor rs tex ola (ter Bra oldma PFC nn area 10) ⬇ ⬆ Physical aggression Impuls ⬆i ve P ⬆hy Tr and sa ic i t a a l a g g a g g g rg r es es res ss ive iso io n g n r oup Left cuneus Left c⬆ u neus ⬆ ⬇ Right anterior cingulated cortex Right anterior cingulated cortex conne⬆ c tivity ⬆ Impulsive and aggressive soldier Imp s ulsive and aggressive soldiers Left amygdala Left amygdala After emotional inducti Af on ter ta s em k (o vi tio olna ent l io ndu ffender ction s )ta sk (violent offenders) Left dorsolaterLeft al PFsuperior C Left do temporal rsolateralgyr PFC us Right dorsolateral PFC ⬆ R ight dorsolateral P ⬆F C⬆ Aggressive strategies ⬆ (laboratory task) Violent inmates Violent inmates Pariet nu al c (ls Anter eu up sr )a ma ior rc g ii ng nau l la and te ca o ng rtex ul ar gyrus)Anter ior ci⬇ ng ulate cortex ⬆ Aggressive strategies (laboratory task) Left calcarine cortex Left calcarine cortex Cerebellar vermis Left mOF Cer Cebe lR lair g ver ht sm up is er Lef ior t temp OFC ora R l ig gy ht ru ss u Lef pert io ar my temp gdao lLef a ra l t ⬇ g O yr F u C s ⬇ ⬇ Violent Afiter nm em ates o tional induction ta V sik o l(ent violient nma otes ffender s) Amygdala (bilateral) Left mOFC ⬇ Anger control-out mPFC (right) Su Adj pera ic oen r p ta srtr iet ua ctu l lo res bu le Left fusif ⬇ ⬇ o rm gyrus Young violent offenders Lef Sup t r aa nter mar ig oi rn ca il ng gy ur lu ate s ( c ri o g rht) tex Lef Su t a p nter rama ior rg ciin ng alu glLef Adj y ate ru t s c a c o c ( aent r rli tex c g aht) rs itr ne uc ctu orr tex es Lef Adj t ca alc cent a⬆ ⬆ ri ne strcu oc rtu tex res ⬆ ⬆ Impu Y ls oiu ve ng a nd vio a lent ggres off sender ive sos ldi erIsmp ulsY ive oua ng nd vi ao glg ent ress oifve fender soldi ser s Trait aggression Amygdala basolateral (bi Am later yg ada l) la basolateral (bilater Lef alt ) dorsolateral PFC Left dorsolateral P⬇ F C ⬇ Impulsive and aggressive Imp gro uu ls p ive and aggressive group Revenge fe H eliip ng po sc ampus (right) Reveng Lef e fe t ce en liF ng tr ro o snta me vmP di l lo a F be ( l C a my sug pd er ailo ar and middle frontaBi l lateral sup⬆ r amarginal gyrus ⬆ ⬆ Anger expression-out Impulsive and aggressive group Amygdala basolateral ⬇ ⬆ Trait aggression Left superior occipital cortex Left superior occipital cortex Violent poLef pult ado tior ns so ( la no ter V -isa o el ll ent f P r F ep C p o or p ted) ulat ions (Lef no-t sdo elfr r sep ola oter rR ted) i ag l ht P F do C rsolateral PFC Right poster Rig io ht r ido nsu rsl⬆ o a l ateral PFC ⬆ Violent inmates Violent inmates Parietal (su mOFC pramarginal and angular gyrus) Lingual gyrus Precuneus (left) Right cerebellar hemisphere Right cerebeLef llart hem sup Lef er isip t oa her rmy oc ec gida pitla al cortex Left super Lef ior t o ⬆ ac my cip gida tall a co rtex ⬆ Violent inmates Violent inmates Left amygdala Left mOFC ⬇ ⬆ ⬆ Trait Af agter gres em sio on tio nal induction task (violent offender s) Left fusiform gyrus Left fusiform gyrus Aggressive strategies (laboratory task) gyrus) Amygdala (rR ig iht) ght cerebellum InferiR oirg fht ro c nta erebe l gy lr lu um s ( right) ⬆ ⬆ Trait aggression Right superior temporal gyrus Amyg Am daly a g ba da sl o al a (ter bila ater l (bi all) a teral) AmygdaSuperior la basolater parietal Lef al ( t bi do larter slobule ola alter ) al PFC Left dorso ⬇l ateral PFC ⬇ Impulsive and aggressive group Impulsive and aggressive group CH au ip dp ao te c a nu mp clu eu s s ( r Lef (ir g iht) g t ht) c en C a tr uo dme atedi nu alc a leu my F s r g (o r d Lef nta ia glht) a t l c l o en be ( trosme updi eri ao l ra a my ndg mi daddl la e frontal ⬆ ⬆ ⬆ ⬆ Ang er expresIsmp ionu -o ls u it ve and aggressive Imp gro uu ls p ive and aggressive group SupramaR rg ig in ht a lO gF yC ru s (right) Right OFAdj C acent structures Left ⬆ cu neus Young violent offenders Bilateral cerebellar hemisphere Bilateral cerebellar hem Bi Lef lia ster p t c her u alneu e O Fs C Lef Bil t ac⬆ ter ⬇ u neu al O s F C ⬆⬇ ⬆ V Rie o venge lent inm feea ltes ing s ⬆ R Ve ivenge olent i nm feelaites ngs vmPFC ⬇ ⬆ Trait aggression Lingual gyrus Lingual gyrus Proactive aggression Right angular gyrus Right angular gyrus Angular gyrus (right) mPFC (ri V giht) olent popula mP tions FC ( ( no rig -s ht) elf reported) Adj Lef t afcu en sit f o sr tr m gy ucturru es s Adjacent str Lef uc t tu fu rs es if orm gyrus Young violent offenderY s oung violent offenders Left anterior cingulate cog rtex yru s) Left calca ⬇r ine cortex ⬇ Impulsive and aggressive soldiers Right cerebellar hemisphere Lef Left t p ar my ecu gneu dala s Left pr⬆ ecu neus ⬆ Violent inmates Cerebellar vermis Cerebellar vermis Lef t OFC Lef ⬇ t OFC ⬇ Violent inmates Violent inmates Nucleu Lef s centr t cen atr lio s me sup di er ailo a rmy (me gd di aa la n raphe Left centromedial amygdala ⬆ ⬆ Impulsive and aggressive group Impulsive and aggressive group Left cuneus Left cuneus Right anter Ventr ior a cli ng stru ia lta ate l d cortex Right anterior cingulate Ang d co u rltex ar gyrus ⬆ Impul⬆ s iP ve roa and cti ve ag a gg res grs es ive si o sn o ldierIsmp ulsive and aggressive soldiers Right OFC RivmP ght R O F iF g C C ht midoccipital cortex P Ro ig ster ht i m or ido c⬆ i⬆ ng c ciu plia ta ted l co cr o tex rtex ⬆ ⬆ ⬆ ⬇ Revenge feelings ⬇⬆ R Tr evenge ait ag g fee res lisng ion s Precuneus (left) CauP dr aecu te nu neu cleu s (l sef F (r r t) o ig nto ht)p olar c Li ong rtex ua (lBr gy or dma us nn area 10) Lingu⬇ a l gyrus ⬆ Trait aggression Proactive aggression Left superior occipital cortex Bilateral cerebellar hemisphere Left Bi cla alter cara il ne Oc Fo C r tex Left calca⬇ ri ne cortex Violent inmates Left dorsolateral PFC Left dorsolaR ter iga ht l P do FC rs olateral PFC Right dorsolateral PFC Violent inmates Violent inmates ⬆ ⬆ nucleus) Left anterior cingulate co Lef rtex t a nterior cingulate cortex Lef t calcarine cortex Left calcarine cortex ⬆ ⬆ Impulsive and aggressive Imp solu di lser ive s and aggressive soldiers Physical aggression Laboratory task Laboratory task Dorsomedial PFC mPFC (right) Adjacent structures Young violent offenders Supramarginal gyrus (r Su igp ht) ra marginal gyrus (right) Adja Lef cent t c u str neu uctu s res Adjacent strucLef tures t ⬆ c u neus ⬆ ⬇ Young violent offenderY s oung violent offenders Ventral striatal Angular gyrus Left cuneus ⬆ Proactive aggression Cerebellar vermis Left superLef ior t oO cc FiC pi tal cortex Left superior ⬆ o ⬇ c cipital cortex Violent inmates Amygdala basolateral (bilateral) Amygdala basolater Lef at l do (bir ls ao ter laa ter l) al PFC Left dorsolateral PFC Impulsive and aggressive group Impulsive and aggressive group ⬇ ⬇ vmPFC Bilateral supramargiLef nalt g sy ur p u er s ior occipital coLef rtex ⬇t superior occipital cortex ⬆ Trait aggression OFC (left) Anger expression Left s Lef upt er aing or u temp lar reg ora io l n g yrus Left superior ⬆ ⬇ temporal gyrus ⬆ ⬆ Aggress ⬆ i ve Phy str si acteg al a ies gg ( rles abo sio rn ato ry⬆ ta Ag skg ) ressive strategies (laboratory task) Precuneus (left) Lef Rig t ht anter cerebe ior lclia ng r hem ulate is p c R o her irg tex ht e cerebe Lef llt aa rnter hem io is rp cher inge u Lef late Lef t c ca o t lrc a tex a my ri ne gda co la rtex Left amy Lef gda t cla al ca ⬆r ine cortex ⬆ Impulsive Va io nd lent agig nm res astes ive soldier Vs Ii mp olent uls ii nm ve a ates nd aggressive soldiers Left pr ⬆ ecu neus ⬆ Physical ag Lef gres t do sio rn so lateral PFC Right dorsolateral PFC Violent inmates Left fusiform gyrus Left fusiform gyrus Amygdala (right) Inferior frontal gyrus (right)Lef t cuneus Left cuneus Right anterior cingulated cortex ⬆ ⬆ ⬆ Trait aggression Impulsive and aggressive soldiers LefAm t cen ytr gda ome la di ba aslo a lmy ater g ad l ala Lef Am t Am cen yy g tr g da o da me la l a ba di (bi a so ll a l aa ter my ter aa g l mOFC ) ld ala Lef mOFC t mOF C ⬇ Impu⬆ ls i P ve hy a snd ica la a gg gg res res si sve ion gr o u p I mp u l s ⬇i ve Ang a nd er c a o gntr g r es o ls - io ve u t g r o u p Supramarginal gyrus (right) Adjacent structures ⬆ ⬆ Young violent offenders Left superior occipital cortex Left superior occipital cortex ⬆ Bilateral cerebellar hem Bi islp aher tera el cerebellar hemisphere Bilateral OFC BilateraLef l Ot Fc C a lca ⬇r ine cortex ⬇ Violent inmates Violent inmates OFC (left) Left angular region ⬇ ⬆ Physical aggression AmygdaAnter la basio olr a ter insa u lla (bi lateral) Left Li do ng rs u O o a F lla C g ter yr au l s P FC Ling⬇ ⬇ u al gyrus ⬆ Ag Imp gres uslisve ive str and ateg ag ies gr es (lasbo ive ra g to ro ry u ⬆ p ta Ag skg ) ressive strategies (laboratory task) ⬇ ⬇ Left precuneus Left precuneus Angular gyrus (right) Superior parietal lobule Parietal ( sSu upp ra er ma ior r g pia nra il et aa nd l loa bu ng lu e lar gyrus) ⬆ Destructive aggression Right cerebellar hemisphere Left amygdala Violent inmates Right anterior cingulated Rc ig oht rtex anter iorLef cing t cu ulneu ated s c ortex Left super Lef iot r co u cneu cipis t a l cortex ⬆ ⬆ ⬆ Impulsive and aggressive Imp solu di lser ive s and aggressive soldiers Cerebellar vermis Cerebellar vermis Left OFC Left OFC ⬇ ⬇ Violent inmates Violent inmates ⬆ Physical aggression Left Lef fust if co u rneu m gy s rus Left cuneus vmPFC Posterior cingulated coLef rtex t calcarine cortex Left calcarine cortex ⬆ ⬆ Trait aggression Anterior insula OFC ⬇ Left centromedial amygdala Hippocampus V (rentr ight) a l striatum Frontal lobe (super ⬆i or and middle frontal ⬆ Impulsive and aggressive group ⬆ Anger expression-out Left precuneus Left precuneus Bilateral cerebellar hemisphere Bilateral OFC ⬇ Violent inmates Left dorsolateral PFC Left dorsolateral PFC Right dorsolateral PFCR ight dorsolateral PF ⬆ C ⬆ Violent inmates Violent inmates Lingual gyrus ⬆ Destructive aggression Left anter Anter ior ic oir ng ins ulu alte a cortex Left anterior cingLef ulat te c a clo cr atex rine cortex Left cal⬆ ca rine cortex Impuls ⬆i ve Phy and sic a alg a g g rg es res sive sio s no ldiers Impulsive and aggressive soldiers Right anterior cingulated cortex Right anterior cingulated cortex ⬆ ⬆ Impulsive and aggressive soldiers I mpulsive and aggressive soldiers Dorsomedial P Lef FC t s uperior occipital coLef rtex ⬆ t superior occipital cortex ⬆ Anterior cingulate cortex gyrus) Left calcarine cortex Left calcarine cortex Cerebellar vermis Left OFC ⬇ Violent inmates Amygdala basolateral (Am bilay ter gda al) la basolateral (bilatera Lef l) t dorsolateral PFC Left dorsolateral PFC ⬇ ⬇ Impulsive and aggressiIve mp gu rl o su ive p and aggressive group Ventral striatum Left super Lef iot r co u cneu cipis t al cortex Left superior occipital cortex Anger expression Anterior insula ⬆ Physical aggression R evenge feelings P roactive aggressioLef n t superior occipital cortex Left superior⬆ o ccipital cortex Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Left fusiform gyrus Left fusiform gyrus Left anterior cingulate cortex Anter Left io cra c lc ing ariu ne lac te or ctex ortex Impulsive and aggressive soldiers Left cuneus Lef⬆ t cuneus Left Am ceny tr go da me ladi (bi all a ater my ag Lef l) d at la c entromedial amygdala Left mOFC ⬇ ⬆ ⬆ Impuls ⬇i ve Ang and er c ao gntr gres ols -io Ive mp ut gu rl o su ive p and aggressive group Ventral stria Rta iglht cerebellum Angular gyrus ⬆ ⬆ Proactive aggression Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group Lingual gyrus Lingual gyrus Revenge feelings Left superior occipital cortex Right OFC Left precuneus Left p ⬆ recuneus ⬆ Revenge feelings Parietal (supramarginal and angular gyrus) Right anterior cingulated cortex Phy siR ca ig l ht ag a gnter ressiio or n c ing R uilg aht te d ang cou rtex lar gyrus ⬆ ⬆ Impulsive and aggressive soldiers Impulsive and aggressive soldiers Left fusiform gyrus Left cuneus Left cuneus Left cuneus Lef Rit gc ht al c ca er riebe ne l clo urm tex Left calcarine cortex Left centromedial amygdala Impulsive and aggressive group Hippocampus (right) Frontal lobe (superior and middle frontal ⬆ ⬆ ⬆ Anger expression-out Right OFC ⬆ Revenge feelings Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings OFC (left) Left ang ⬆ ular region ⬇ ⬆ Physical aggression Lingual gyrus Left anterior cingulate Lef cortex t anter ior cingulate cortexLef t calcarine cortex Left calcarine cortex ⬆ ⬆ Impulsive and aggressiIve mp su ol ls di ive ers a nd aggressive soldiers Left R su ig p Lef ht er t ia o p ng rr o ecu u clc aineu rp g ity as r l u cs o rtex Left superior occipital cortex gyrus) Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Laboratory task ⬆ Physical aggression Left superior occipital c Lef ortex t su per Lef iot r co u cneu cipis t al cortex Left calcarine cortex Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Anterior insula OFC ⬇ Proactive aggression Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) ⬆ Destructive aggression Left anterior cingulate cortex Left calcarine cortex ⬆ Impulsive and aggressive soldiers Left super Lef iot r co u cneu cipis t a l cortex Left cuneus Laboratory task Ventral striatal Angular gyrus ⬆ ⬆ Proactive aggression Amygdala basolateral mOFC Ventral striatum Left precuneus Left sup Lef ert io p rr o ecu ccineu pitasl cortex Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Anterior insula ⬇ ⬆⬆ Ag gressive strategies (laboratory task) ⬆ Physical aggress ion Right anterior cingulate Rd igcht o r tex anter ior cingulated cortex Impulsive and aggressiIve mp su ol ls di ive ers a nd aggressive soldiers Physical aggression ⬆ ⬆ Superior parietal lobule Anterior cingulate cortex Left calcarine cortex Left Lef calc t a cr u ine neu cs o r tex Amygdala basolateral mOFC OFC (left) Left angular region ⬆ Physical aggression ⬇ ⬆ Aggressive strategies (laboratory task) Revenge feelings Left superior occipital c Lef ortex t su p Lef ert io p rr o ecu ccineu pitasl cortex Superior parietal lobule Right anterior cingulated cortex Impulsive and aggressive soldiers ⬆ Physical aggression Left calcarine R ci o g rht tex c erebellum Anterior insula OFC ⬇ Right OFC ⬆ ⬆ Revenge feelings ⬆ Destructive aggression Left superior occR ip ig itht al a cng ortex ula r gyrus Ventral striatum Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Anterior insula ⬆ ⬆ Physical aggression Anterior cingulate cortex Laboratory task Revenge feelings Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Right cerebellum Amygdala basolateral mOFC Right OFC ⬆ ⬆ Revenge feelings ⬇ ⬆ Aggressive strategies (laboratory task) Right angular gyrus Superior parietal lobule Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Laboratory task Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Amygdala basolateral mOFC ⬇ ⬆ Aggressive strategies (laboratory task) Superior parietal lobule Behav. Sci. 2019, 9, 11 12 of 19 Left mOFC Left amygdala ⬆ Before emotional induction task (violent offenders) Table 2. Cont. Left uncus/amygdala Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left amygdala ⬇ Before emotional induction task (violent offenders) Posterior insula ventromedial prefrontal cortex. Brain Structure (From) Brain Structure (To) Functional Connectivity Aggression Assessment Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Functional Right posterior insula Before emotional induction task (violent Brain structure (from) Brain structure (to) Aggression assessment Left amygdala ⬆ After emotional induction task (violent offenders) Left mOFC Left amygdala ventromedial prefrontal cortex. connectivity Right superior temporal gyrus offenders) Trait aggression Violent populations (no-self reported) Functional Left uncus/amygdala Before emotional induction task (violent Brain structure (from) Brain structure (to) Aggression assessment Left amygdala Caudate nucleus (right) Left mOFC ⬇ ⬆ Trait aggression Left mOFC Left amygdala Before emotional induction task (violent offenders) conne⬆ c tivity Amygdala (bilateral) Posterior insula offenders) vmPFC mPFC (right) Adjacent structures ⬇ ⬇ You ⬆ng Tr a vi ito a lent ggro es ff sender ion s Left uncus/amygdala Trait aggression Left amygdala Before emotional induction task (violent offenders) After emotional induction task (violent Nucleus centr Pa rlecu is sneu uper s i(o lef r (t) me dian raphe Posterior insula Left mOFC Left amygdala Left mOFC ⬇ ⬆ Trait aggression Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Amygnu dal ca leu (bi sl)a teral) offenders) Supramarginal gyrus (right) Adjacent structures ⬆ Young violent offenders Left mOFC Left amygdala After emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: med⬇ ia l orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: vmPFC ⬇ ⬆ Trait aggression Right cerebe vmP llaF r C hem isphere BilateralLef sut pa ra my ma gr da gil na a l gyrus ⬇ ⬆ ⬆ VTr iola ent it ai g nm gres ates sio n Right posterior insula Right posterior insula After emotional induction task (violent Nucleus centralis superior (median raphe ventromedial prefrontal cortex. Left amygdala After emotional induction task (violent offenders) Left amygdala ⬆ Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Bilatera Am l cer yg ebe dallla a r (r hem ight) i sphere InferiorBi frlo anta tera l lg O yr Fu C s (right) ⬆ ⬆V Tr io a lient t agig nm res astes ion Right superior temporal gyrus Right superior temporal gyrus offenders) nucleus) Angular gyrus (right) Cerebellar vermis Left OFC Func⬇ ti onal Violent inmates Violent populations (no-self reported) vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Brain structure (from) Brain structure (to) Aggression assessment Violent populations (no-self reported) Lef vmP t mOF FC C Posteri Lef or t cia ng my ug la da ted la cortex conne⬆ ⬆ c tivity Before emotional⬆ i ndu Traic t ta io gn grtes assk io (n v iolent offenders) Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Caudate nucleus (right) Amygdala (right) Inferior frontal gyrus (right) ⬆ ⬆ Trait aggression Lef Do t u rsnc ome us/di amy al P gF dC al a Trait Am aggy rg es da sio la n ba solateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group Caudate nucleus (right) mPFC (right) Adjacent structures Young violent offenders Left mOFC Ang Lef ula t ra g my yru gs da (r li ag ht) ⬆ Before emotional induction task (violent offenders) Table 2 Lef . Re t ast my ing g da funct la ional connectivity and its role in anger pronenes. mOFC: med⬇ ia l orbitofrontal cortex, OF Bef C: or o e emo rbitoti fro o na nt la il ndu cor ct tex ion , P taF sk C: (v pr ioefr lent o n oftfa ender l cort sex ) , vmPFC: Posterior insula Anger expression Left Lef fust ifmOF orm gy C rus ⬇ ⬆ Trait aggression mPFC (right) Precuneus (left) Adjacent structures Young violent offenders vmPFC Pos Lef tert io u rnc ciu ng s/u almy ated gdc ao la rtex ⬆ ⬆ Trait aggression Left Am ceny tr go da me ladi (bi all a ater my ag l) d ala ⬆ Impulsive and aggressive group ventromedial prefrontal cortex. Left amygdala ⬇ Before emotional induction task (violent offenders) Table Am 2 y .Lef gRe da t st lmOF ain (bi gl C a funct ter al)io nal connectivity and its rLef ole Lef t in a t my mOF an gg da e Cr l a pr onenes. mOFC: med⬇ ia l orbitofrontal cortex, OF Af C: ter o r em bito o ti fr oo na n⬇ lt a iAng n l du coer crti t ex o co nntr , ta Ps F ok lC: - ( o vi u pr o t lefr ent o o n ff tender al cor st)ex , vmPFC: Precuneus (left) Ling vmP ual F gC y rus ⬇ ⬇ ⬆ Trait aggression Supramarginal gyrus (right) Adjacent structures ⬆ Young violent offenders Do Po rs ster ome iodi r ia ns l P uF la C Parietal (suR pirg aht ma pro gs iter nali o ar nd ins au ng lau lar gyrus) Nucleus centralis superior (median raphe Left cuneus ventromedial prefrontal cortex. Right cerebellar hemisphere Left amygdala Violent inmates Func⬆ ti onal Anger expressio Lef n t mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Left amygdala ⬆ After emotional induction task (violent offenders) Supramarginal gyrus (right) FAdjacent rontopolarstr couct rtex ur (Br esodmann area 10) ⬇ Young violent ⬆ Tr of aifenders t aggression Brain structure (from) Brain structure (to) Aggression assessment Right superior temporal gyrus Hippocampus (right) Frontal lobe (superior and middle frontal ⬆ Anger expression-out Left anterinu or c clieu ngs u )l ate cortex Left calcarine cortex ⬆ ⬆ Impulsive and aggressive soldiers Bilateral cerebellar hemisphere Bilateral OFC conne⬇ c tivity Violent inmates Amygdala (bilateral) RightLef pot ster mOF iorC ins ula ⬇ Anger control-out Left mOFC Left amygdala Before emotional induction task (violent offenders) Func⬆ ti onal Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left amygdala ⬆ After emotional induction task (violent offenders) Right cer V ebellar iolent phemispher opulations (e no-self reported) Left Left amygdala superio gr y o ru cc s) ip ital cortex Violent inmates vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Brain structure (from) Brain structure (to) Aggression assessment Trait aggress C io er nebe llar vermis Left OFC ⬇ Violent inmates Right superior temporal gyrus Parietal (supramarginal and angular gyrus) Left uncus/amygdala connectivity ProactiveC aa gu gd res ate si nu on cleus (right) Left cuneus ventromedial prefrontal cortex. Am Lef yt ga da my lag (da riglht) a Inferior frontal gyrus (right) Before emotional induction task (violent offenders) ⬆ ⬇ ⬆ Trait aggression Left dorsolateral PFC Right Lef dor t smOF olater C a l PFC ⬆ ⬆V Tr io a lient t agig nm res astes ion Bilateral cer Viebellar olent poH hemispher pu ip la pto io cns amp (no u es -s (el rifg r ht) ep orted) Fronta Bilateral l lobe (su OFC perior and middle frontal ⬇ Violent ⬆ Ang inmates er expression-out Posterior insula Trait aggression Amygdala (bilateral) mPFC (right) Adjacent structures Young violent offenders Ventral striatal Lef Ang t u plra ecu r gneu yrus s ⬇ ⬆ Proactive aggression Angular gyrus (right) Amygdala basolateral (bilateral) Left dovmP rsolaF ter C al PFC ⬇ Impulsi ⬆ ve Tr a and it a a gg gg rr es es ss io ive n group Caudate nucleus (right) gyrus) ⬇ Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Left mOFC Left amygdala Functional After emotional induction task (violent offenders) Cerebellar vermis Left OFC Left mOFC ⬇ Violent ⬆ inmates Trait aggression Precuneus (left) Left mOFC LefLef t ca t lc aa my rine gda co la rtex ⬆ Before emotional induction task (violent offenders) Physical aB gra gries n ssit o vmP rn uc tur FC e (from) Poster Bra io in r c sitng ruc utlur ated e (tc o o )r tex Aggression assessment ⬆ ⬆ Trait aggression Amygdala (bilateral) Left fusiform gyrus P N ru oc alceu tive s c a entr ggra mP es lis s iF s ou C np (er rig io ht) r ( median raphe Adjacent structures ⬇ Young violent offenders connectivity Right posterior insula Left centromedial amygdala Frontopolar cortex vmP (Br FC o dmann area 10) ⬇ ⬆ Impulsi ⬆ ve Tr a and it a a gg gg rr es es ss io ive n group Supramarginal gyrus (right) Adjacent structures ⬇ You ⬆ng Tr a vi ito a lent ggro es ff sender ion s Left Lef sup t er unc iou r s o/c ac my ipig ta d la clo ar tex ⬆ Lef O t F aC my (lef gda t) la Lef Dot ra so ng me uldi ara r l eg PF io Cn ⬇ After emotiona ⬆l P indu hysic cti ao l n ag ta gr ses k ( svi ioo nl ent offenders) Left dorsolateral P PFC recu nuneu cleu ss ()l eft) Right dorsolateral LinguaPFC l gyrus Violent inmates Ventral striatal Angular gyrus Left amygdala ⬆ ⬇ Before emotiona ⬆ P l r io ndu actc ive tio a n gtg ar ses k ( sv io io nl ent offenders) Trait aggression Right superior temporal gyrus Nucleus centralis superior (median raphe Right cerebellar hemisphere Left amygdala Violent inmates Posterior insula ⬆ Anger expression ⬆ Physical aggression Frontopolar co Lef rtex t c ( u Br neu odma s nn area 10) ⬇ ⬆ Trait aggression Supramarg vmP inalF g C y rus (right) Bilater Adj al s au cent pra ma stru rg ctu ina res l g yrus ⬇ ⬆ Yo⬆ u ng Tr vi aio t la ent ggr oes ffender sion s Physical aggression Violent popul Anter ations io (r no ins -su ella f reported) Left OmOF FC C ⬇ ⬆ Trait aggression Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group nucleus) Left mOFC Left amygdala ⬆ Before emotional induction task (violent offenders) Bilateral cLef erebe t mOF llar hem C isphere Lef Bila t ter amy al g O da FC la ⬇ ⬇ After emotional iV ndu iolc ent tion inm tas ak tes (vi olent offenders) Amygdala (bilateral) ⬆ Destructive aggression Amygdala (bilateral) Left mOFC ⬇ ⬇ Anger control-out Left anterior cingulate cortex Left calcarine cortex ⬆ Impulsive and aggressive soldiers RightAm cery ebe gda lla la r hem (right) isp here Inferior Lef fro t nta amy l g gy da ru la s (right) ⬆ ⬆ ⬆V Tr io a lient t agig nm res astes ion OFC (left) Left angular region ⬇ ⬆ Physical aggression vmPFC ⬇ ⬆ Trait aggression Caudate nucleus (right) vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Left uncus/amygdala Cerebellar vermis Right p Lef ost ter OiF oC r insula ⬇ Violent inmates Left fusiform Ventr gyr al sus triatum ParietalLef (su t p sru ap ma eriro gri n oa clc i ap nd itaa l ng cor u tex lar gyrus) BilateralLef cert ebe amy lla g rda hem la isphere AngBi ulla arter gy ar lu O s F (r C ig ht) ⬇ ⬇ Before emotional V indu iolent ctioin nm taa stes k (v iolent offenders) Left amygdala ⬆ After emotional induction task (violent offenders) Left centr N omedial ucleus centr amygdala Anter a mP lis F su C io p r (er riins g io ht) u r l(a me dian raphe Adjacent structures Impulsive and Y⬆ ⬆ oaggr u P Png hy hy s s essive vi i ic co a all lent a ag gg g gr or r fes es foup ender s si io on n s ⬆ ⬇ Amygdala (right) Inferior frontal gyrus (right) ⬆ ⬆ Trait aggression Posterior insula LefAnter t dorsio olr a ter insa u lla P FC Right Ri g su ht p er do io rO s ro F temp lC ater a olr a PlF g C y rus ⬆ Violent inmates Fronto Lingual p Anter olar c igyr o or r tex cus ing (Br ulo adma te conn rtex a rea 10) ⬇ ⬇ ⬆ Trait aggression Hippocampus (right) Frontal lobe (superior and middle frontal ⬆ ⬆ Anger expression-out Left cuneus Cerebe vmP llar F ver C mis PosteriorLef cing t O ul F aC ted cortex ⬆ ⬇ ⬆V Tr io a lient t agig nm res astes ion ⬆ Destructive aggression Precu nuneu cleu ss ()l eft) Angular gyrus (right) Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Violent Am p yo gp da ulla at iba ons so ( la no ter -sa el l f ( bi rep later orted) al) Left dorsolateral PFC Impulsive and aggressive group Revenge feelings gyrus) ⬇ Left precuneus Left dorsolateral PFC Rig Do htr do some rsodi later al P aF l C PF C Violent inmates Left cuneus Ventral striatum ⬆ Supramarg vmP inalF g C y rus (right) Bilater Adj al s au cent pra ma stru rg ctu ina res l g yrus Yo⬆ u ng Tr vi aio t la ent ggr oes ffender sion s Right anterior cingulated cortex ⬇ ⬆ ⬆ Impulsive and aggressive soldiers Lef vmP t mOF FC C Posteri Lef or t cia ng my ug la da ted la cortex ⬆ ⬆ Before emotional⬆ i ndu Traic t ta io gn grtes assk io (n v iolent offenders) Right posterior insula Caud Anter ate nu ioc rl i eu nssu (lr ai ght) Left fusiform gyrus ⬆ Physical aggression Proactive aggression ⬆ Lef Rit gc ht al c ca er riebe ne l clo urm tex Anger Am exy p g rda ess lLef a io ba n t a so my later gda all a (bi lateral) Left dorsolateral PFC ⬆ After emI o mp tiona uls l iive ndu and cti o an g g ta res sks ( ivi veo g lent rouo pf fenders) Left anterior cingulate Left centr cortex omedial amygdala Left calcarine Anterior cortex cingulate cortex ⬇ Impulsive Iand mpuaggr lsive essive and agg soldiers ressive group Right cerR ebe ight lla O r hem FC isphere Left amygdala ⬆ Violent inmates Amygdala (right) Inferior frontal gyrus (right) ⬆ ⬆ ⬆ ⬆ ⬆ R Tr evenge ait agg free eslsiing ons Lef Do t u rsnc ome us/di amy al P gF dC al a Right superior temporal gyrus mPFC (right) Adj Li ang cen uta s ltr gu yc ru tu sr es ⬇ Young violent offenders Right angular gyrus Ventral striatal Left sup Ang erio u rl a or c c giy priu ta sl cortex ⬆ ⬆ Proactive aggression Left amygdala ⬇ Before emotional induction task (violent offenders) Amygdala (bilateral) Left mOFC ⬇ ⬇ Anger control-out Revenge feelings Left superiorLef occipital t fusiforcortex m gyrus Bilateral cerebellar hemisphere AngBi ulla arter gy ar lu O s F (r C ig ht) ⬇ Violent inmates Anger expression Posterior insula Violent Lef pot pcu en P la rtr tecu io ome ns neu (di no s a - l( s la ef el my f t) r ep gdo ar la ted) Impulsive and aggressive group Left cuneus ⬆ Physical aggress R io ig n ht OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Parietal (suprama Ling rgu in al a lg a ynd rusa ngular gyrus) Right cerebellum Cerebe vmP llar F ver C mis PosteriorLef cing t O ul F aC ted cortex ⬆ ⬇ ⬆V Tr io a lient t agig nm res astes ion AmyLef gda t lmOF a (bilC ater al) Lef Lef t a t my mOF gda Cl a ⬇ After emotiona⬇ l iAng nduer cti o co nntr tas ok l- ( o vi uo t l ent offenders) Caudate nucleus (right) Left cuneus ⬇ Lef Sup t r aa nter maR r ig o ig i rn ht ca i l ng O gF y uC r lu a te s ( c ri o g rht) tex Lef Adj t a cc aent lca rsitr ne uc ctu orr tex es ⬆ ⬆ Impu Y ls oiu ve ng a nd vio a lent ggres off sender ive sos ldi ers ⬆ ⬆ Revenge feelings Laboratory task OFC (left) Left angular region ⬆ Physical aggression Hippocampus (right) Frontal lobe (su Lef per t ic ou r neu and s middle frontal ⬆ ⬆ Anger expression-out Right angular gyrus Dorsomedial PFC Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Right posterior insula mPFC (right) ParietLeft al (su pr p Adj recuneus ama acr en gitn s atr l u and ctur aes ng ular gyrus) ⬇ Young violent offenders Right cerebellar hemisphere Left sup Lef erit oa rmy occ gida pitla al cortex ⬆ Violent inmates Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Left amygdala ⬆ After emotiona ⬆l P indu hysic cti ao l n ag ta gr ses k ( svi ioo n lent o ff ender s ) Right anterior cingulated Left anterio cortex r cingulate cortex Left cal g cy ar ru ine s) cortex ImpulsiveImp and ulaggr sive a essive nd aggsoldiers ressive soldiers Anger expressio R ni ght OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group Hip P Anter p recu ocaneu mp ior u isns s( l(u ef rla it) g ht) Fronta Rli g lo ht be ( susp uer per io O i ro F temp rC a ndo mi ralddl gyr e ufs r ontal ⬇ ⬆ Anger expression-out Left calcarine cortex ⬆ Bilateral cerebellar hemisphere Bi Lef later t cu alneu OFs C ⬇ Violent inmates Amygdala basolateral mOFC ⬆ Destructive aggression Proactive aggression Left superior occipital cortex Laboratory task Amygdala (bilateral) Left Lef fust ifmOF orm gy C r us ⬇ ⬆ Aggressi⬇ ve Ang stra er teg co ies ntr (o la l-bo ou rt ato ry task) Violent populations (no-self reported) gyrus) ⬇ Supramarginal gyrus (right) Left superiorAdj occipital acent str cortex uctures ⬆ Young violent offenders Cerebellar vermis LefLef t pr t ecu OFneu C s ⬇ Violent inmates Left centromedial amygdala Superior parietal lobule ⬆ Impulsive and aggressive group Ventral striatum Right anter Ventr ior a cli ng stru ia lta ate l d cortex Ang Lefu t lc au r neu gyrs u s ⬆ Impul⬆ s iP ve roa and cti ve ag a gg res grs es ive si o sn o ldiers Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Parietal (suprama Ling rgu in al a lg a ynd rusa ngular gyrus) ProactiveC aa gu gd Anter res ate si nu oin o c rl i eu nssu (lr ai ght) ⬆ ⬆ Physical aggression Right cerebellar hemisphere LefLef t ca t lc aa my rine gda co la rtex ⬆ Violent inmates Left dorsolateral PFC Right dorsolateral PFC Violent inmates Anterior cingulate cortex Physical aggression Left precuneus Amygdala basolateral mOFC Hippocampus (right) Frontal lobe (su Lef per t ic ou r neu and s middle frontal ⬆ ⬆ Anger expression-out V mP entr FC al (srtr ig ia ht) ta l Adj Ang acen ulta s rtr gu yc rtu usr es ⬇ Young violent offenders R Bi ig la ht ter aa nter l cer io ebe r cilng laru hem lated isp co her rtex e Left sup Bi erlia o ter r o aclc O ipF it C a l cortex ⬆ ⬆ ⬇ Impul⬆ s iP ve r V oa ia o nd clt ent i ve ag ia g nm g res ga rs es tes ive s i o sn o ldiers Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ ⬆ Ag Imp gres uslisve ive str and ateg ag ies gr es (lasbo ive ra g to ro ry u p ta sk) Revenge feelings Left calcarine cortex OFC (left) Left angular region ⬇ ⬆ Physical aggression Superiorg p ya ru riset ) al lobule Left anter Precu iorneu cing s u (llef ate t) cortex Left calcarine cortex ⬆ Impulsive and aggressive soldiers Physical aggC res ers ebe ionl lar vermis Left OFC ⬇ Violent inmates Left fusiform gyrus Left su Rp ig er ht io c rer oc ebe cip li lt u am l c ortex ⬆ Physical aggression Left centromedial amygdala ⬆ Impulsive and aggressive group ProactiSu ve p arg ag ma res rs g ii o n n a l gyrus (right) Left s Adj uper acient or o sc tr cu ip citu tar l es co rtex Young violent offenders Right OFC ⬆ ⬆ ⬆ Revenge feelings Left do Or F sC ol ( alter eft) a l PFC RiLef ght t do ang rs u olla arter reg ali o Pn F C ⬇ ⬆ PV hy io slient cal a inm ggra es tes si on Anterior insula Lingu Oa F lC g yrus ⬇ ⬆ Right angular gyrus ⬆ Destructive aggression Ventral striatal Ang Lefu t lc au r neu gyrs u s ⬆ ⬆ Proactive aggression Right cerebellar hemisphere Left amygdala ⬆ Violent inmates Amygdala basolateral (bilateral) Left dorsolateral PFC Impu⬆ ls i P ve hya snd ica la a gg gg res res si sve ion gr o u p Left cuneus Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Anterior insula OFC Ventral striatum ⬇ Left precuneus Physical aggression Bilateral cerebellar hemisphere Bilateral OFC ⬇ Violent inmates ⬆ Destructive aggression Left anter Anter ior ic oir ng ins ulu alte a cortex Lef Left t c fa uls cia fo rirne m gy corrtex us ⬆ Impuls ⬆i ve Phy and sic a alg a g g rg es res sive sio s no ldiers Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Laboratory task Left centromedial amygdala Anterior cingulate cortex ⬆ Impulsive and aggressive group Left calcarine cortex OFC (left) Left angular region ⬆ Physical aggression Cerebellar vermis Left OFC ⬇ ⬇ Violent inmates VLi entr nga ula s ltr giy ar tu us m Left superior occipital cortex Left superior temporal gyrus Anterior insula ⬆ ⬆ Aggress ⬆ i ve Phy str si acteg al a ies gg ( rles abo sio rn ato ry task) Revenge feelings ⬆ Left superior occipital cortex Left dorsolateral PFC Right dorsolateral PFC ⬆ ⬆ PV hy io slient cal a inm ggra es tes si on Anterior cingulate cortex Lef Left t c cu uneu neus s AmAnter ygdalia o r ba ins sou la la ter al OFC ⬇ mOFC Right cerebellum Amygdala basolateral (bilateral) Left dorsolateral PFC Imp⬆ u lDes sive tra u nd cti ve ag g ar ges gr ses ive si o gn ro up Reveng Lef e fe t e alnter ings io r cingulate cortex Left calcarine cortex ⬇ ⬇ ⬆ Ag Imp gres uls siive ve s atr nd ateg agig es res (ls aibo ver s ao to ldi ryer ta s sk) Right OFC Left precuneus ⬆ ⬆ ⬆ Revenge feelings Superior parietal lobule Right anterior cingulated cortex Right angular gyrus ⬆ Impulsive and aggressive soldiers Lef Ventr t fusa il f o sr tr m gy iatum ru s Left superior occipital cortex Lef Rit gc ht al c ca er riebe ne l clo urm tex Left cen Anter trome iodi r ia ns l a umy la gdala ⬆ Impu⬆ ls i P ve hy a snd ica la a gg gg res res si sve ion g roup Right OFC ⬆ Right OFC Right midoccipital cortex ⬆ ⬇ ⬆ R Re evenge venge f fee eel li ing ngs s AnterLi iong r ci u ng al u gly ar te us c ortex Left R su ig pht er Lef ia o ng t r co u u cl neu c airp g is ty ar lu cs o rtex Laboratory task R evenge feelings Left cuneus Left precuneus Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Left anterior cingulate cortex Lef Rit gc ht al c ca er riebe ne l clo urm tex ⬆ Impulsive and aggressive soldiers Left calcarine cortex Laboratory task Right OFC ⬆ ⬆ Revenge feelings Amygdala basolateral mOFC Lef Left t R s su u ig p pht er er i ia o o ng r r o o u c clc c ai ir p p g i it ty a ar l lu c cs o o r rtex tex Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) ⬇ ⬆ Aggressive strategies (laboratory task) Superior parietal lobule Right OFC Right m Lef ido t c cc uineu pitas l c ortex ⬆ ⬇ Revenge feelings Amygdala basolateral mOFC ⬆ Aggressive strategies (laboratory task) Laboratory task Left precuneus Superior parietal lobule Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Left calcarine cortex Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Left superior occipital cortex Amygdala basolateral mOFC ⬇ ⬆ Aggressive strategies (laboratory task) Superior parietal lobule Behav. Sci. 2019, 9, 11 13 of 19 Although it appears that the diminished RSFC between the PFC and amygdala might be employed as a useful marker for proneness to violence, other brain networks should be considered in order to offer a broader understanding of the complex phenomenon of violence. Even though other limbic structures and their projections are involved in proneness to violence, we can conclude that high RSFC between the amygdala and the inferior frontal gyrus and left superior temporal gyrus was associated with high anger traits in several populations (normative and with mental disorders). Furthermore, the amygdala and the ACC maintained high RSFC with the fusiform and lingual gyrus, cuneus and precuneus calcarine cortex, and superior occipital cortex in impulsive and aggressive individuals. Recently, a research group demonstrated that violent individuals with schizophrenia presented hyperactivation of the ACC when perceiving negative images [51], especially in highly impulsive schizophrenic individuals [52]. This result coincides with the hypothesis that a large percentage of violent offenders present an attentional bias toward negative stimulus and/or a hostile attribution bias [53]. Moreover, other brain networks composed of the inferior frontal and temporal gyrus, ACC, and anterior insula are involved in voluntarily and actively sharing the emotional experience of other individuals (through intentional empathic processes), which is extremely important in behavioral regulation [8]. Thus, we sustain that this specific brain network facilitates the onset of violence due to attributing negative and hostile intentions to others, which is congruent with the scientific literature in this field. Regarding other limbic structures, the hippocampus and the anterior insula maintain anger expression facilitation projections with the supramarginal and angular gyrus, the superior and middle frontal gyrus, the ventral striatum, and the ACC. In this regard, the middle frontal gyrus plays an important role in hostile cognitive bias and angry rumination (or how often an individual tends to re-experience negative feelings) [54,55]. We also hypothesized that the heightened connectivity between the left/right orbitofrontal cortex (OFC) in violent inmates [49] may play a role in angry rumination. Furthermore, it was recently demonstrated that brainstem alterations (except its volume) seem to partly explain high irritability and proneness to react violently in males with autism [12,13]. Moreover, in two groups of violent inmates, the authors concluded that the PFC (mPFC and OFC) also maintained lower connectivity with adjacent areas and the cerebellar vermis, compared to non-violent males [41,42], with the cerebellum joined to the basal ganglia, and the supplementary motor area being important in impulse control [9]. Therefore, we might summarize that these RSFC patterns in a cognitive model where high anger traits that were linked to empathic alterations (i.e., perspective-taking disruptions, emotion-decoding deficits . . . ), hostile cognitive biases, and heightened anger rumination might lower the threshold for reacting with violence in ambiguous contexts, physically facilitating reactive violence. With regard to proactive violence, one study that was included in our review used self-reports to analyze the RSFC underlying this kind of violence. However, the authors did not compare reactive and proactive violence, and so it may be difficult to establish in this review whether there are differentiated neural pathways to each kind of violence [56]. Kolla, Dunlop, Meyer, and Downar [38] concluded that high RSFC between the ventral striatal and the angular gyrus was associated with high proactive violence strategies. Curiously, psychopaths (who usually but not always employ proactive violence) have been found to present structural abnormalities in the striatum—particularly increased volume—compared to non-psychopaths [57]. Moreover, it has been suggested that the angular gyrus belongs to the brain networks underlying moral reasoning [8]. Thus, these results offer information about which neural pathways underlie this kind of violence, which is defined as predatory, and is often characterized by premeditation and being cold-blooded [58]. Extending these findings, another study [42] revealed that revenge feelings were positively correlated with the RSFC between the OFC and the cerebellum, angular gyrus, and midoccipital cortex. Furthermore, recent research highlighted that psychopathic traits, as well as the risk of reoffending, maintained a positive relationship with the grey matter volume of the cerebellum [9]. If we try to explain why these neural pathways explain revenge feelings, we can assume that these neural pathways are associated with several processes that are important for revenge, such as the anticipation of consequences of violent behavior (good or bad) and reimagining different contexts to consume the desire for revenge [58]. Behav. Sci. 2019, 9, 11 14 of 19 Finally, one way to prevent these antisocial behaviors is to promote empathic abilities in violent populations through various psychological interventions. Thus, it has been hypothesized that there is an overlap between these brain regions that underlie violence and empathy, but the pattern of functional connectivity underlying each of them is inverse [57]. Regarding RSFC, a recent study demonstrated that individuals (men and women) with higher empathic abilities tend to present greater RSFC between the mPFC and the dorsal ACC, the precuneus, and the left superior temporal sulcus [58]. Conversely, low levels of empathy have been related to lower RSFC between the mPFC and ACC [30]. Moreover, it has been stated that high affective empathy tends to be related to stronger RSFC between the ventral anterior insula, OFC, amygdala, and perigenual anterior cingulated, and that high cognitive empathy is related to greater RSFC between the brainstem, superior temporal sulcus, and ventral anterior insula [59]. This statement is congruent with the assertion that there is a certain overlap between the brain structures that underlie violence and empathy, but they present inverse RSFC patterns. Thus, we might conclude that the brain RSFC in empathic abilities is more harmonious (i.e., positive RSFC between the PFC and the limbic system), than the pattern for violence (i.e., negative RSFC between PFC and the limbic system), which describes an imbalance in the brain functioning of individuals who tend to present proneness to violence. Based on the summarized results of our review and the brain RSFC underlying empathy, we proposed the facilitating and inhibiting brain networks for reactive violence described in Figure 2. Three important limitations of the studies carried out are the lack of a homogeneous population and their limited sample size. In fact, there is great diversity in the relevant variables, and not all of the studies reported or controlled the potential confounding effects of variables such as handedness, drug use, educational level, economic level, ethnicity, and psychopathology, among others. Furthermore, only a few studies included women, and so most of the research was conducted with males. Although small sample sizes kept us from properly estimating the differences between groups, most of the studies applied Bonferroni corrections for multiple comparisons. Moreover, they employed different anger trait questionnaires that measure different facets of anger (trait, physical, or verbal tendency to express anger, anger expression in general, proactive violence . . . ). Lastly, several of the articles that were included in our review based their conclusions on seed-based findings that are necessarily limited to a priori regions. In this regard, the absence of a finding in another region is very different from a study that may have used ICA. Hence, it is difficult to obtain unanimous conclusions about the association between RSFC and anger. In summary, the present review study confirmed that reduced frontal and limbic connectivity is a good correlate for several variables, such as trait anger and anger expression or control, which are important in violence proneness. Nevertheless, in order to offer a broader understanding of violence proneness, we need to contemplate other resting-state brain networks, including cortical regions (i.e., gyrus, parietal, temporal, ACC . . . ) and subcortical structures (i.e., hippocampus, insula, brain stem, cerebellum . . . ), in addition to the PFC and amygdala. Therefore, based on the studies summarized in this manuscript, along with those that analyzed the RSFC underlying empathic processes, we proposed a model to explain anger proneness to reactive violence (Figure 2). In sum, our review offered more insight into the importance of studying the brain RSFC underlying several important processes for violence proneness. It also reinforced the need to carry out further studies that analyze the importance of the RSFC using larger sample sizes, contemplating several populations, and employing a common anger assessment. Moreover, it would be necessary to check whether these RSFC could be considered temporally stable (as a ‘trait’), or whether they might change after interventions focused on promoting behavioral regulation and cognitive improvements. In fact, several studies demonstrated that after a focused intervention to promote cognitive and empathic changes in groups of intimate partner violence (IPV) perpetrators, these individuals improved specific cognitive and empathic abilities [60]. Thus, this research allows us to detect whether these changes correspond to specific brain network changes. Therefore, caution should be used in interpreting these results, in order to develop effective intervention programs to reduce proneness to violence. Behav. Sci. 2019, 9, 11 15 of 19 Figure 2. Proposed model of facilitating and inhibiting brain networks for reactive violence proneness. Behav. Sci. 2019, 9, 11 16 of 19 Author Contributions: Conceptualization: Á.R-M.; Methodology: Á.R-M. and M.G.; Writing-Original Draft Preparation: Á.R-M..; Writing-Review & Editing: M.L., E.G., L.M-B., Á.A-B., R.M-P., A.T-E. and L.M-A.; Funding Acquisition: Á.R-M. Funding: Project supported by a 2018 Leonardo Grant for Researchers and Cultural Creators, BBVA Foundation. The Foundation accepts no responsibility for the opinions, statements and contents included in the project and/or the results thereof, which are entirely the responsibility of the authors. Moreover, this work was supported by the Universitat of València (UV-INV-AE18-780697). Conflicts of Interest: The authors declare no conflict of interest. References 1. Glenn, A.L.; Raine, A. Neurocriminology: Implications for the punishment, prediction and prevention of criminal behaviour. Nat. Rev. Neurosci. 2014, 15, 54. [CrossRef] [PubMed] 2. Moya-Albiol, L.; Sariñana-González, S.; Vitoria-Estruch, S.; Romero-Martínez, Á. La neurocriminología como disciplina aplicada emergente. Vox Juris 2017, 33, 6. [CrossRef] 3. Nordstrom, B.R.; Gao, Y.; Glenn, A.L.; Peskin, M.; Rudo-Hutt, A.S.; Schug, R.A.; Yang, Y.; Raine, A. Neurocriminology. Adv. Genet. 2011, 75, 255–283. [PubMed] 4. Menon, R.S.; Gati, J.S.; Goodyear, B.G.; Luknowsky, D.C.; Thomas, C.G. Spatial and temporal resolution of functional magnetic resonance imaging. Biochem. Cell Biol. 1998, 76, 560–571. [CrossRef] [PubMed] 5. Zani, A.; Biella, G.; Proverbio, A.M. Brain imaging techniques: Invasiveness and spatial and temporal resolution. In The Cognitive Electrophysiology of Mind and Brain; Elsevier: Amsterdam, The Netherlands, 2003; pp. 417–422. 6. Hare, R.D.; Smith, A.M.; Forster, B.B.; MacKay, A.L.; Whittall, K.P.; Kiehl, K.A.; Smith, A.M.; Hare, R.D.; Liddle, P.F. Functional magnetic resonance imaging: The basics of blood-oxygen-level dependent (BOLD) imaging. Can. Assoc. Radiol. J. 1998, 49, 320–329. 7. Ekstrom, A. How and when the fMRI BOLD signal relates to underlying neural activity: The danger in dissociation. Brain Res. Rev. 2010, 62, 233–244. [CrossRef] [PubMed] 8. Raine, A.; Yang, Y. Neural foundations to moral reasoning and antisocial behavior. Soc. Cogn. Affect. Neurosci. 2006, 1, 203–213. [CrossRef] 9. Leutgeb, V.; Leitner, M.; Wabnegger, A.; Klug, D.; Scharmüller, W.; Zussner, T.; Schienle, A. Brain abnormalities in high-risk violent offenders and their association with psychopathic traits and criminal recidivism. Neuroscience 2015, 308, 194–201. [CrossRef] [PubMed] 10. Romero-Martínez, Á.; Moya-Albiol, L. Neuropsychology of perpetrators of domestic violence: The role of traumatic brain injury and alcohol abuse and/or dependence. Rev. Neurol. 2013, 57, 515–522. 11. Romero-Martínez, A.; Moya-Albiol, L. Neuropsychological impairments associated with the relation between cocaine abuse and violence: Neurological facilitation mechanisms. Adicciones 2015, 27, 64–74. [CrossRef] 12. Lundwall, R.A.; Stephenson, K.G.; Neeley-Tass, E.S.; Cox, J.C.; South, M.; Bigler, E.D.; Anderberg, E.; Prigge, M.D.; Hansen, B.D.; Lainhart, J.E.; et al. Relationship between brain stem volume and aggression in children diagnosed with autism spectrum disorder. Res. Autism Spectr. Disord. 2017, 34, 44–51. [CrossRef] [PubMed] 13. Glenn, A.L.; Raine, A.; Yaralian, P.S.; Yang, Y. Increased volume of the striatum in psychopathic individuals. Biol. Psychiatry 2010, 67, 52–58. [CrossRef] [PubMed] 14. Romero-Martínez, Á.; Moya-Albiol, L. ¿Facilitan los esteroides anabolizantes-androgénicos la expresión de la violencia? Rev. Esp. Drogodepend. 2015, 40, 12–26. 15. Siever, L.J. Neurobiology of aggression and violence. Am. J. Psychiatry 2008, 165, 429–442. [CrossRef] 16. Glenn, A.L.; Raine, A. Psychopathy and instrumental aggression: Evolutionary, neurobiological, and legal perspectives. Int. J. Law Psychiatry 2009, 32, 253–258. [CrossRef] 17. Raine, A.; Meloy, J.R.; Bihrle, S.; Stoddard, J.; LaCasse, L.; Buchsbaum, M.S. Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. Behav. Sci. Law 1998, 16, 319–332. [CrossRef] 18. Blair, R.J.R. The amygdala and ventromedial prefrontal cortex in morality and psychopathy. Trends Cogn. Sci. 2007, 11, 387–392. [CrossRef] [PubMed] Behav. Sci. 2019, 9, 11 17 of 19 19. Blair, R. Dysfunctions of medial and lateral orbitofrontal cortex in psychopathy. Ann. N. Y. Acad. Sci. 2007, 1121, 461–479. [CrossRef] 20. Lee, M.H.; Smyser, C.D.; Shimony, J.S. Resting-state fMRI: A review of methods and clinical applications. Am. J. Neuroradiol. 2013, 34, 1866–1872. [CrossRef] 21. Di, X.; Biswal, B.B. Dynamic brain functional connectivity modulated by resting-state networks. Brain Struct. Funct. 2015, 220, 37–46. [CrossRef] 22. Smitha, K.; Akhil Raja, K.; Arun, K.; Rajesh, P.; Thomas, B.; Kapilamoorthy, T.; Kesavadas, C. Resting state fMRI: A review on methods in resting state connectivity analysis and resting state networks. Neuroradiol. J. 2017, 30, 305–317. [CrossRef] [PubMed] 23. Binder, J.R.; Frost, J.A.; Hammeke, T.A.; Bellgowan, P.; Rao, S.M.; Cox, R.W. Conceptual processing during the conscious resting state: A functional MRI study. J. Cogn. Neurosci. 1999, 11, 80–93. [CrossRef] [PubMed] 24. Mazoyer, B.; Zago, L.; Mellet, E.; Bricogne, S.; Etard, O.; Houdé, O.; Crivello, F.; Joliot, M.; Petit, L.; Tzourio-Mazoyer, N. Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res. Bull. 2001, 54, 287–298. [CrossRef] 25. Shulman, G.L.; Fiez, J.A.; Corbetta, M.; Buckner, R.L.; Miezin, F.M.; Raichle, M.E.; Petersen, S.E. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 1997, 9, 648–663. [CrossRef] [PubMed] 26. Vatansever, D.; Menon, D.K.; Manktelow, A.E.; Sahakian, B.J.; Stamatakis, E.A. Default mode network connectivity during task execution. Neuroimage 2015, 122, 96–104. [CrossRef] [PubMed] 27. Greicius, M.D.; Krasnow, B.; Reiss, A.L.; Menon, V. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. USA 2003, 100, 253–258. [CrossRef] [PubMed] 28. Mars, R.B.; Neubert, F.; Noonan, M.P.; Sallet, J.; Toni, I.; Rushworth, M.F. On the relationship between the “default mode network” and the “social brain”. Front. Hum. Neurosci. 2012, 6, 189. [CrossRef] [PubMed] 29. Smith, V.; Mitchell, D.J.; Duncan, J. Role of the default mode network in cognitive transitions. bioRxiv 2018, 295683. [CrossRef] [PubMed] 30. Kim, S.J.; Kim, S.; Kim, H.E.; Han, K.; Jeong, B.; Kim, J.; Namkoong, K.; Kim, J.W. Altered Functional Connectivity of the Default Mode Network in Low-Empathy Subjects. Yonsei Med. J. 2017, 58, 1061–1065. [CrossRef] 31. Beaty, R.E.; Kaufman, S.B.; Benedek, M.; Jung, R.E.; Kenett, Y.N.; Jauk, E.; Neubauer, A.C.; Silvia, P.J. Personality and complex brain networks: The role of openness to experience in default network efficiency. Hum. Brain Mapp. 2016, 37, 773–779. [CrossRef] 32. Zhao, J.; Tomasi, D.; Wiers, C.E.; Shokri-Kojori, E.; Demiral, S.B.; ¸ Zhang, Y.; Volkow, N.D.; Wang, G. Correlation between Traits of Emotion-Based Impulsivity and Intrinsic Default-Mode Network Activity. Neural Plast. 2017, 2017, 9297621. [CrossRef] [PubMed] 33. Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med. 2009, 6, e1000100. [CrossRef] 34. Park, A.T.; Leonard, J.A.; Saxler, P.; Cyr, A.B.; Gabrieli, J.D.E.; Mackey, A.P. Amygdala-medial prefrontal connectivity relates to stress and mental health in early childhood. Soc. Cogn. Affect. Neurosci. 2018. [CrossRef] 35. Fulwiler, C.E.; King, J.A.; Zhang, N. Amygdala-orbitofrontal resting-state functional connectivity is associated with trait anger. Neuroreport 2012, 23, 606–610. [CrossRef] [PubMed] 36. Abram, S.V.; Wisner, K.M.; Grazioplene, R.G.; Krueger, R.F.; MacDonald, A.W.; DeYoung, C.G. Functional coherence of insula networks is associated with externalizing behavior. J. Abnorm. Psychol. 2015, 124, 1079–1091. [CrossRef] [PubMed] 37. Klasen, M.; Wolf, D.; Eisner, P.D.; Habel, U.; Repple, J.; Vernaleken, I.; Schlüter, T.; Eggermann, T.; Zerres, K.; Zepf, F.D.; et al. Neural networks underlying trait aggression depend on MAOA gene alleles. Brain Struct. Funct. 2018, 223, 873–881. [CrossRef] [PubMed] 38. Kolla, N.J.; Dunlop, K.; Meyer, J.H.; Downar, J. Corticostriatal connectivity in antisocial personality disorder by MAO-A genotype and its relationship to aggressive behavior. Int. J. Neuropsychopharmacol. 2018. [CrossRef] 39. Hoptman, M.J.; D’Angelo, D.; Catalano, D.; Mauro, C.J.; Shehzad, Z.E.; Kelly, A.M.; Castellanos, F.X.; Javitt, D.C.; Milham, M.P. Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophr. Bull. 2010, 36, 1020–1028. [CrossRef] [PubMed] Behav. Sci. 2019, 9, 11 18 of 19 40. Wagner, G.; Krause-Utz, A.; de la Cruz, F.; Schumann, A.; Schmahl, C.; Bar, K.J. Resting-state functional connectivity of neurotransmitter producing sites in female patients with borderline personality disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 2018, 83, 118–126. [CrossRef] 41. Hasler, R.; Preti, M.; Meskaldji, D.; Prados, J.; Adouan, W.; Rodriguez, C.; Toma, S.; Hiller, N.; Ismaili, T.; Hofmeister, J.; et al. Inter-hemispherical asymmetry in default-mode functional connectivity and BAIAP2 gene are associated with anger expression in ADHD adults. Psychiatry Res. Neuroimaging 2017, 269, 54–61. [CrossRef] 42. McGlade, E.; Rogowska, J.; Yurgelun-Todd, D. Sex differences in orbitofrontal connectivity in male and female veterans with TBI. Brain Imaging Behav. 2015, 9, 535–549. [CrossRef] [PubMed] 43. Goswami, R.; Dufort, P.; Tartaglia, M.C.; Green, R.E.; Crawley, A.; Tator, C.H.; Wennberg, R.; Mikulis, D.J.; Keightley, M.; Davis, K.D.; et al. Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions. Brain Struct. Funct. 2016, 221, 1911–1925. [CrossRef] [PubMed] 44. Dailey, N.S.; Smith, R.; Vanuk, J.R.; Raikes, A.C.; Killgore, W.D.S. Resting-state functional connectivity as a biomarker of aggression in mild traumatic brain injury. Neuroreport 2018, 29, 1413–1417. [CrossRef] [PubMed] 45. Gilam, G.; Maron-Katz, A.; Kliper, E.; Lin, T.; Fruchter, E.; Shamir, R.; Hendler, T.; et al. Tracing the Neural Carryover Effects of Interpersonal Anger on Resting-State fMRI in Men and Their Relation to Traumatic Stress Symptoms in a Subsample of Soldiers. Front. Behav. Neurosci. 2017, 11, 252. [CrossRef] [PubMed] 46. Buades-Rotger, M.; Engelke, C.; Kramer, U.M. Trait and state patterns of basolateral amygdala connectivity at rest are related to endogenous testosterone and aggression in healthy young women. Brain Imaging Behav. 2018. [CrossRef] [PubMed] 47. Siep, N.; Tonnaer, F.; van de Ven, V.; Arntz, A.; Raine, A.; Cima, M. Anger provocation increases limbic and decreases medial prefrontal cortex connectivity with the left amygdala in reactive aggressive violent offenders. Brain Imaging Behav. 2018, 1–13. [CrossRef] [PubMed] 48. Chen, C.; Zhou, J.; Liu, C.; Witt, K.; Zhang, Y.; Jing, B.; Li, C.; Wang, X.; Li, L. Regional homogeneity of resting-state brain abnormalities in violent juvenile offenders: A biomarker of brain immaturity? J. Neuropsychiatry Clin. Neurosci. 2015, 27, 27–32. [CrossRef] 49. Leutgeb, V.; Wabnegger, A.; Leitner, M.; Zussner, T.; Scharmüller, W.; Klug, D.; Schienle, A. Altered cerebellar-amygdala connectivity in violent offenders: A resting-state fMRI study. Neurosci. Lett. 2016, 610, 160–164. [CrossRef] 50. Varkevisser, T.; Gladwin, T.E.; Heesink, L.; van Honk, J.; Geuze, E. Resting-state functional connectivity in combat veterans suffering from impulsive aggression. Soc. Cogn. Affect. Neurosci. 2017, 12, 1881–1889. [CrossRef] 51. Tikasz, A.; Potvin, S.; Lungu, O.; Joyal, C.C.; Hodgins, S.; Mendrek, A.; Dumais, A. Anterior cingulate hyperactivations during negative emotion processing among men with schizophrenia and a history of violent behavior. Neuropsychiatr. Dis. Treat. 2016, 12, 1397–1410. 52. Hoptman, M.J.; Antonius, D.; Mauro, C.J.; Parker, E.M.; Javitt, D.C. Cortical thinning, functional connectivity, and mood-related impulsivity in schizophrenia: Relationship to aggressive attitudes and behavior. Am. J. Psychiatry 2014, 171, 939–948. [CrossRef] [PubMed] 53. Wang, Y.; Zhu, W.; Xiao, M.; Zhang, Q.; Zhao, Y.; Zhang, H.; et al. Hostile attribution bias mediates the relationship between structural variations in the left middle frontal gyrus and trait angry rumination. Front. Psychol. 2018, 9, 526. [CrossRef] [PubMed] 54. Anestis, M.D.; Anestis, J.C.; Selby, E.A.; Joiner, T.E. Anger rumination across forms of aggression. Personal. Individ. Differ. 2009, 46, 192–196. [CrossRef] 55. Wang, X.; Yang, L.; Yang, J.; Gao, L.; Zhao, F.; Xie, X.; Lei, L. Trait anger and aggression: A moderated mediation model of anger rumination and moral disengagement. Personal. Individ. Differ. 2018, 125, 44–49. [CrossRef] 56. Wrangham, R.W. Two types of aggression in human evolution. Proc. Natl. Acad. Sci. USA 2018, 115, 245–253. [CrossRef] [PubMed] 57. Moya-Albiol, L.; Herrero, N.; Bernal, M.C. The neural bases of empathy. Rev. Neurol. 2010, 50, 89–100. [PubMed] Behav. Sci. 2019, 9, 11 19 of 19 58. Takeuchi, H.; Taki, Y.; Nouchi, R.; Sekiguchi, A.; Hashizume, H.; Sassa, Y.; Kotozaki, Y.; Miyauchi, C.M.; Yokoyama, R.; Iizuka, K.; et al. Association between resting-state functional connectivity and empathizing/systemizing. Neuroimage 2014, 99, 312–322. [CrossRef] 59. Cox, C.L.; Uddin, L.Q.; Di Martino, A.; Castellanos, F.X.; Milham, M.P.; Kelly, C. The balance between feeling and knowing: Affective and cognitive empathy are reflected in the brain’s intrinsic functional dynamics. Soc. Cogn. Affect. Neurosci. 2011, 7, 727–737. [CrossRef] [PubMed] 60. Romero-Martínez, Á.; Lila, M.; Martínez, M.; Pedrón-Rico, V.; Moya-Albiol, L. Improvements in empathy and cognitive flexibility after court-mandated intervention program in intimate partner violence perpetrators: The role of alcohol abuse. Int. J. Environ. Res. Public Health 2016, 13, 394. [CrossRef] © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Behavioral Sciences Multidisciplinary Digital Publishing Institute

The Brain Resting-State Functional Connectivity Underlying Violence Proneness: Is It a Reliable Marker for Neurocriminology? A Systematic Review

Loading next page...
 
/lp/multidisciplinary-digital-publishing-institute/the-brain-resting-state-functional-connectivity-underlying-violence-jfBmcvvZ4C
Publisher
Multidisciplinary Digital Publishing Institute
Copyright
© 1996-2019 MDPI (Basel, Switzerland) unless otherwise stated
ISSN
2076-328X
DOI
10.3390/bs9010011
Publisher site
See Article on Publisher Site

Abstract

behavioral sciences Review The Brain Resting-State Functional Connectivity Underlying Violence Proneness: Is It a Reliable Marker for Neurocriminology? A Systematic Review 1 , 1 2 2 Ángel Romero-Martínez * , Macarena González , Marisol Lila , Enrique Gracia , 3 3 3 Luis Martí-Bonmatí , Ángel Alberich-Bayarri , Rebeca Maldonado-Puig , 3 1 Amadeo Ten-Esteve and Luis Moya-Albiol Psychobiology Department, University of València, 46010 València, Spain; gonporma@alumni.uv.es (M.G.); Luis.Moya@uv.es (L.M.-A.) Department of Social Psychology, University of Valencia, 46010 València, Spain; Marisol.Lila@uv.es (M.L.); Enrique.Gracia@uv.es (E.G.) Biomedical Imaging Research Group (GIBI230), La Fe Health Research Institute, 46026 Valencia, Spain; marti_lui@gva.es (L.M.-B.); alberich_ang@gva.es (A.A.-B.); rebecagibi230@gmail.com (R.M.-P.); ten_ama@gva.es (A.T.-E.) * Correspondence: Angel.Romero@uv.es; Tel.: +3-496-386-4302; Fax: +3-496-386-4668 Received: 9 November 2018; Accepted: 11 January 2019; Published: 15 January 2019 Abstract: Introduction: There is growing scientific interest in understanding the biological mechanisms affecting and/or underlying violent behaviors in order to develop effective treatment and prevention programs. In recent years, neuroscientific research has tried to demonstrate whether the intrinsic activity within the brain at rest in the absence of any external stimulation (resting-state functional connectivity; RSFC) could be employed as a reliable marker for several cognitive abilities and personality traits that are important in behavior regulation, particularly, proneness to violence. Aims: This review aims to highlight the association between the RSFC among specific brain structures and the predisposition to experiencing anger and/or responding to stressful and distressing situations with anger in several populations. Methods: The scientific literature was reviewed following the PRISMA quality criteria for reviews, using the following digital databases: PubMed, PsycINFO, Psicodoc, and Dialnet. Results: The identification of 181 abstracts and retrieval of 34 full texts led to the inclusion of 17 papers. The results described in our study offer a better understanding of the brain networks that might explain the tendency to experience anger. The majority of the studies highlighted that diminished RSFC between the prefrontal cortex and the amygdala might make people prone to reactive violence, but that it is also necessary to contemplate additional cortical (i.e., insula, gyrus [angular, supramarginal, temporal, fusiform, superior, and middle frontal], anterior and posterior cingulated cortex) and subcortical brain structures (i.e., hippocampus, cerebellum, ventral striatum, and nucleus centralis superior) in order to explain a phenomenon as complex as violence. Moreover, we also described the neural pathways that might underlie proactive violence and feelings of revenge, highlighting the RSFC between the OFC, ventral striatal, angular gyrus, mid-occipital cortex, and cerebellum. Conclusions. The results from this synthesis and critical analysis of RSFC findings in several populations offer guidelines for future research and for developing a more accurate model of proneness to violence, in order to create effective treatment and prevention programs. Keywords: anger state; brain; inmates; mental illness; resting functional connectivity; violence Behav. Sci. 2019, 9, 11; doi:10.3390/bs9010011 www.mdpi.com/journal/behavsci Behav. Sci. 2019, 9, 11 2 of 19 1. Introduction There is growing scientific interest in understanding the biological mechanisms affecting and/or underlying violent behaviors, in order to develop effective treatment and prevention programs [1–3]. In this regard, the relatively recent appearance of the field of neurocriminology represents an important advance in our understanding of these problems by applying the neuroscientific perspective to their study. In fact, neurocriminology aims to establish the neurobiological basis for crime and violence. Specifically, this neuroscientific subdiscipline has incorporated several tools and/or procedures, such as neuroimaging techniques, genetic markers, and hormonal measurements, among others, to predict these antisocial behaviors [3]. Neuroimaging techniques are non-invasive, and make it possible to visualize brain structures and functional connectivity in brain networks, thanks to their good spatial and functional resolution. Indeed, functional magnetic resonance imaging (fMRI) has offered insight into the functional synchrony between brain structures, that is, how the activation of several brain structures is temporally coordinated [4,5]. These techniques have usually relied on showing changes in the activation of different brain networks by analysing the blood oxygen level-dependent (BOLD) presented in these brain regions, which is especially sensitive to the increase in blood flow in the cerebral capillaries of the activated neuronal regions [6,7]. Studies using fMRI to assess brain networks have demonstrated that altered functional connectivity across distant brain regions might make individuals prone to violence [8–15]. In fact, most of the research in this field has highlighted that the alteration in the cerebral connectivity between the key nodes involved in emotional and cognitive behavioral regulation might explain this proneness to violence. Particularly, the inhibitory malfunction of the frontal lobe (i.e., prefrontal structures, frontal gyrus . . . ) would lead to an overactivation of the limbic system (i.e., amygdala, hypothalamus, hippocampus . . . ), which under certain stimuli might facilitate impulsive and/or reactive violence. In this regard, it has been suggested that the activation of frontal structures facilitates self-regulation and control over emotion-related behaviors by attenuating limbic responses to emotional stimuli and/or the context [8–15]. By contrast, several authors demonstrated that individuals characterized by predatory and instrumental violence (proactive) might present normal prefrontal cortex (PFC) functioning, and an increase in dorsolateral PFC activation has even been described during emotion processing tasks in these individuals [16–19]. Furthermore, studies have indicated that the reduction in amygdala activation during emotion processing might be characteristic of instrumental violence [19]. In this case, unimpaired or even higher frontal activation is related to the ability to control impulses and/or emotional processing, but also to certain alterations in empathic abilities. Unfortunately, the majority of the previously mentioned studies analyzed the functional activation of these brain structures in response to certain tasks (i.e., exposure to a stimulus, emotional induction tasks . . . ), and so little is known about whether these brain structures and their connections in the absence of external stimulation might be employed as reliable markers of proneness to violence. In recent years, neuroscientific research has not only been interested in brain functioning during a task, but it has also focused on the intrinsic activity within the brain at rest without any external stimulation (resting-state functional connectivity; RSFC). In this direction, several studies have demonstrated the existence of resting intrinsic brain connectivity (networks) when an individual is awake and alert [20–22]. Synchronicity across a group of distant brain regions during resting periods has been called the default mode network (DMN; precuneus/posterior cingulate cortex, medial PFC and medial, lateral, and inferior parietal cortex). Although it has been suggested that the DMN is relatively deactivated during a demanding task [23–25], some authors have maintained that it might make an active contribution to cognitive processing [26,27], or even be important for cognitive abilities [28–30] or a correlate of certain personality traits [31,32]. With regard to the aforementioned, it should be mentioned that the activation of individual brain structures that encompass the DMN does not necessarily mean that the DMN is activated. In fact, it is necessary to consider how these brain structures establish and maintain networks with other brain structures outside the DMN during Behav. Sci. 2019, 9, 11 3 of 19 the resting state. Since evidence about whether the DMN or other brain networks might be important in violence proneness is less clear, it would be important to summarize the main results of this field of research. In light of the above, this review aims to highlight the association between the RSFC among specific brain structures and the predisposition to experiencing anger and/or responding to stressful and distressing situations with anger. Specifically, we will focus on the following concepts related to violence: reactive violence (characterized by impulsivity, emotional drive, and lack of self-control); proactive violence (characterized by planning, high awareness of the purpose of this conduct, and low emotionality); trait anger (frequency of experiencing feelings of anger); and anger expression (frequency of externally and/or internally manifesting angry feelings). The present study will first describe the main findings on the association between RSFC and self-reported anger in non-violent normative individuals and in others with mental disorders. Then, we will describe the association between RSFC and changes in anger levels after laboratory tasks in non-violent and violent populations. Next, with the main purpose of analyzing whether these connections could be employed as reliable markers of violence proneness, we will analyze the RSFC in highly violent populations (i.e., young offenders, inmates, and soldiers) in comparison with non-violent individuals. Finally, considering the existing data, we will discuss the implications for clinical practice and further research. 2. Methods Search Strategy A literature search on the existence of a relationship between brain RSFC and proneness to violence was carried out following the PRISMA quality criteria for reviews [33], using the following digital databases: PubMed, PsycINFO, Psicodoc, and Dialnet. The search terms were the following: Resting functional connectivity or resting fMRI or default mode network) and (violence or aggressive or anger). All of the papers that were selected for final inclusion met the following criteria: (a) they employed fMRI techniques to assess brain RSFC; (b) they were empirical studies; (c) they involved research with human subjects; and (d) they were written in English. Moreover, other criteria were not common to all of the papers, as they either: (a) examined anger through self-reports; (b) examined aggressive behavior through laboratory tasks; (c) examined RSFC in highly violent populations; (d) or assessed the relationship (i.e., correlational, regression analysis . . . ) between RSFC and aggressive behavior as a trait and/or response to a laboratory task. Articles mentioning RSFC or aggressive behavior separately, but without examining the relationship between the two, were excluded. Moreover, studies were excluded if they did not directly examine anger or anger expression (i.e., externalizing behaviors, but not aggressive, criminal records . . . ), or they did not explicitly mention that the participants were highly violent (PRISMA flow diagram; Figure 1). Article selection was entrusted to two researchers. In cases of disagreement, a third member of the team helped them reach a consensus. Behav. Sci. 2019, 9, 11 4 of 19 Figure 1. Flow chart of literature search with reasons for exclusion. 3. Results After a systematic scientific literature search, we identified 181 abstracts, of which 34 texts were fully read because they seemed to present all of the inclusion criteria. Ultimately, only 17 of these papers were included in the review (Figure 1). In all, 17 studies investigated the relationship between brain RSFC and several aspects of violence proneness (e.g., self-reported anger, changes in anger levels after a laboratory task-paradigm, or brain RSFC in a highly violent population). First, we will present the association between RSFC and self-reported anger in a non-violent normative population, followed by groups of non-violent patients with several mental disorders or brain damage (e.g., schizophrenia, bipolar disorder, attention deficit hyperactivity disorder (ADHD), and individuals with brain damage from traumatic brain injury). It should be noted that three studies mainly focused on the association between the RSFC and self-reported anger in carriers of specific alleles, and so we described the association by mentioning the specific allele subgroup. Third, we will describe whether brain RSFC predicts anger level changes after a laboratory method for inducing anger in a non-violent normative population, as well as in violent groups. Finally, we will describe the RSFC in different samples of highly violent populations (young offenders, inmates, and impulsive/violent soldiers). The main characteristics of the participants in each study are summarized in Table 1 (age, gender, education level, drug use, and handedness). Behav. Sci. 2019, 9, 11 5 of 19 Table 1. Main sociodemographic characteristics and details about the participants in each study and the assessment methods used. ADHD: attention deficit hyperactivity disorder, fMRI: functional magnetic resonance imaging, TBI: traumatic brain injury. Handedness Violent Behavior Methods of Authors Sample Characteristics Age Gender Education Drug Use (Right/Left) Assessment Analysis Park et al. Healthy young children (n = 79) 6.06  0.96 49% 51%  - - - Child Behavior Checklist Seed-based (2018) [34] Fulwiler et al. Spielberger State–Trait Anger Healthy males (n = 16) 34  14.42  - No current drug use Right-handed ROI (2012) [35] Expression Inventory-2 Abram et al. Psychiatry healthy sample Externalizing Spectrum 26 50% 50%  - No current drug use Right-handed ICA (2015) [36] (n = 244) Inventory, brief form Klasen et al. Buss–Perry Aggression Healthy young adults (n = 83) 23.8  3.6  - - Right-handed ROI (2018) [37] Questionnaire Buss–Perry Aggression Antisocial personality disorder Kolla et al. 36.2  8.7 Questionnaire subjects (n = 21)  - No current drug use - ROI (2018) [38] 34.2  7.7 Reactive–Proactive Controls (n = 19) Aggression Questionnaire Patients with schizophrenia or 36.7  10.5 88% 12% Buss Perry Aggression Hoptman et al. schizoaffective disorder (n = 25) 12.3  2.1 (years) Questionnaire CPZ equivalents - ROI (2010) [39] 15.5  3.0 (years) Life history of aggression Controls (n = 21) 40.4  10.8 76% 24% Number total of arrests Unmedicated female patients 26.7  6.4 Wagner et al. 12.1  1.6 (years) Buss–Perry Aggression with BPD (n = 33)  No current drug use . ROI (2018) [40] 11.8  1.5 (years) Questionnaire Controls (n = 33) 26.4  6.2 48h free of Hasler et al. ADHD (n = 30) 38.7  9.9 70% 30% Spielberger State–Trait Anger CO challenge - methylphenidate Right handed (2017) [41] Controls (n = 15) 32.2  5.5 26% 73% Expression Inventory-2 regressor before fMRI Veterans males with TBI (n = 24) Buss–Perry Aggression McGlade et al. 37.75  9.59  14.33  2.10 (years) Veterans females with TBI - - QuestionnaireDisplaced Seed-based (2015) [42] 40.0 11.15 15.06  2.51 (years) (n = 17) Aggression Questionnaire Retired athletes with a history of Goswami et al. 50  12 17  1.8 Personality Assessment multiple concussions (n = 19);  No current drug use - Seed-based (2016) [43] 46  10 16  1.9 Inventory (aggression scale) Controls (n = 17) Dailey et al. Adults with TBI (n = 17) 21.86  2.79 26% 73% Buss–Perry Aggression - - - ROI (2018) [44] Healthy controls (n = 17) 23.88  3.26 29% 71% Questionnaire Spielberger State–Trait Anger Gilam et al. > secondary Brain functional Soldiers (n = 60) 18.62  0.88  No current drug use Right-handed Expression Inventory (2017) [45] education parcellation Geneva Emotion Wheel Buades-Rotger Social Threat Aggression Healthy young women (n = 39) 23.22  3.2 - No current drug use Right-handed ROI et al. (2018) [46] Paradigm Behav. Sci. 2019, 9, 11 6 of 19 Table 1. Cont. Handedness Violent Behavior Methods of Authors Sample Characteristics Age Gender Education Drug Use (Right/Left) Assessment Analysis Siep et al. Violent offenders (n = 18) 35.17  7.12 Current alcohol use - - Seed-based (2018) [47] Non-offender controls (n = 18) 37.06  15.24 No current drug use Chen et al. Young violent offenders (n = 30) 16.06  0.7 16.06 7.76  2.2 - Right-handed - ROI (2015) [48] Controls (n = 29)  0.4 10.06  0.0 Violent inmates of maximum 36.8 12.0 Leutgeb et al. 11.3  1.7 (years) security prison (n = 31)  Non-medicated Right-handed - Seed-based (2016) [49] 11.6  1.0 (years) Controls (n = 30) 35.1  9.0 Impulsive and violent soldiers Varkevisser et al. 36.54  6.27 67,9% middle Interviews and criminal (n = 28)  - - ROI (2017) [50] 34.53  7.59 53,3% middle records Controls (n = 30) Behav. Sci. 2019, 9, 11 7 of 19 3.1. Normative Population (Self-Reported Aggression) One study investigated whether RSFC was associated with trait anger in normative children (both genders). Its authors concluded that low functional connectivity between the bilateral amygdala and ventromedial prefrontal cortex (vmPFC) was related to higher levels of trait aggression (assessed by the Child Behavior Checklist), but this relationship did not remain significant after controlling for family income and maternal education [34]. Another study with young adults added to the previous results by studying whether the amygdala also presented connections with other prefrontal cortex (PFC) structures that facilitate proneness to experiencing anger feelings. In fact, Fulwiler, King, and Zhang [35] studied whether the amygdala’s functional connectivity with other PFC structures predicted trait aggression in young men. These authors demonstrated that, in men, low RSFC between the amygdala (bilateral) and left orbitofrontal cortex (OFC) was associated with high trait anger (measured by the State-Trait Anger Expression Inventory 2, STAXI-2), especially for the right amygdala and left middle orbitofrontal cortex (mOFC). Conversely, the high functional connectivity between these brain structures was related to high anger control-out; in other words, the higher the association between these two brain structures, the greater the effort to control the expression of anger toward others (persons or objects) [35]. Finally, the interconnections between the amygdala and the PFC have not only been studied as facilitators of anger. Abram, Wisner, Grazioplene, Krueger, MacDonald, and DeYoung [36] conducted a study with a relatively larger sample of healthy young adults (of both genders). They assessed whether RSFC was associated with several facets of callous aggression (assessed by externalizing spectrum inventory), such as relational, physical, and destructive aggression. In this regard, they concluded that there was a positive association between the anterior insula, ventral striatum (VStr), and anterior cingulate cortex (ACC), connectivity and physical aggression. However, they also found a negative association between anterior insula and OFC connectivity and physical aggression and destructive aggression. 3.2. Self-Reported Aggression Mediated by Genetic Markers Two studies included genetic markers as mediators of the relationship between RSFC and trait aggression in a sample of young males. One of these studies concluded that Monoamine oxidase A-L (MAOA-L) carriers (in comparison with MAOA-H carriers) showed that a higher RSFC between the ventromedial prefrontal cortex (vmPFC) and the right angular gyrus (AG), posterior cingulate cortex (PCC), and dorsomedial prefrontal cortex, was related to higher aggression traits. Nevertheless, when the RSFC between the vmPFC and bilateral supramarginal gyrus was high, the aggressive traits were low [37]. The other study revealed that in participants with antisocial personality traits with the MAOA-L variant, high RSFC between the ventral striatal and angular gyrus was related to high proactive aggression [38]. 3.3. Mental Disorders (Self-Reported Aggression) In order to avoid biased results, it is important to consider whether and how these variables are related in a normative population and in people with mental disorders, in order to be able to generalize the conclusions to the entire population. For example, in schizophrenic patients, low functional connectivity (bilaterally) between the amygdala and the ventromedial prefrontal cortex (vmPFC) was related to a higher total score on the Buss–Perry Aggression Questionnaire (BPAQ), a life history of aggression, and the total number of arrests. However, the functional connectivity between the bilateral amygdala and the bilateral orbitofrontal cortex (OFC), supragenual cingulate, subgenual cingulate, or dorsolateral prefrontal cortex (DLPFC) regions was unrelated to the aforementioned aggressive behavior scales in schizophrenic patients. These results remained significant even after controlling for the patients’ diagnosis (schizophrenia and schizoaffective disorder), age, and neuroleptic medication dosage [39]. Behav. Sci. 2019, 9, 11 8 of 19 Nevertheless, not all of the studies considered the connections between the amygdala and the PFC. Specifically in bipolar disorder, the assessment of functional connectivity and the BPAQ total score in a group of women with borderline personality disorder demonstrated that low functional connectivity between the serotonergic nucleus centralis superior (NCS) and the frontopolar cortex (FPC) was associated with higher BPAQ total scores in unmedicated bipolar patients. However, the RSFC between these brain structures was unrelated to a control group [40]. In ADHD patients, a study demonstrated that higher connectivity between the right hippocampus, the parietal lobe (supramarginal and angular gyrus), and the frontal lobe (superior and middle frontal gyrus) in carriers of the AG or GG variant of rs8079626 within the BAIAP2 gene (brain-specific angiogenesis inhibitor) was related to higher anger expression-out (or an unmanageable tendency to manifest anger externally) in ADHD patients [41]. In patients with brain damage after traumatic brain injury (TBI), the reduction in the functional connectivity between the left orbitofrontal cortex (OFC) and the left angular region was related to higher scores on the BPAQ physical aggression subscale in male veterans with TBI. Moreover, high RSFC between the right OFC and the right cerebellum and right angular gyrus was related to high scores on the Displaced Aggression Questionnaire (DAQ) Revenge Planning scale in this group. Conversely, connectivity between the right OFC and the right mid occipital cortex was negatively correlated with the scores on the DAQ Revenge Planning scale. Finally, it should be noted that the frontal cortex (FC) of these brain regions was unrelated to BPAQ and/or DAQ scores in female veterans with TBI [42]. Although a study that analyzed the RSFC of a group of retired athletes with a history of multiple concussions failed to find a significant relationship between the RSFC of the bilateral anterior temporal lobe (ATL) and the bilateral medial orbitofrontal cortex (mOFC) and the PAI aggression subscale [43], a recent study demonstrated that in a group of adults with TBI, high RSFC between the right hippocampus and midcingulate cortex was associated with elevated BPAQ scores. However, in a control group, higher self-reported aggression was associated with low RSFC between the right hippocampus and midcingulate cortex, as well as between the right hippocampus and mPFC [44]. Finally, it should be noted that the majority of the studies that analyzed the associations between brain RSFC and violence-related concepts found significant results related to the BPAQ questionnaire [39,40,42,44], but they failed to find these associations on other self-reports such as the PAI. In this regard, a possible explanation for this difference would be that the BPAQ is a self-report to analyze violence-related concepts, unlike the PAI (e.g. total score consists of the average of approximately 29 items), which is a broader personality self-report with only a few questions about violence. 3.4. Laboratory Assessment of Aggression The assessment of anger expression under controlled laboratory conditions offers an interesting alternative to self-reports, although these methods also have some limitations, such as artificial conditions, social biases, the simplification of violence measurement, etc. However, they offer complementary information to self-report assessments of violence-related concepts. 3.4.1. Non-Violent Groups A group of men were submitted to a modified version of the Ultimatum Game, which was employed to induce anger. During this laboratory task, participants have to split a specific amount of money with another player by using negotiation strategies. However, the other player breaks the rules of the game and confronts his opponent directly and insults him/her. Participants experienced an increase in the right amygdala and right inferior frontal gyrus (IFG) functional connectivity after this laboratory task, which, in turn, was associated with higher trait anger scores. Moreover, it should also be noted that individuals with high pre-task functional connectivity in the right amygdala had low anger levels during the task [45]. Behav. Sci. 2019, 9, 11 9 of 19 Another study analyzed whether being exposed to a modified version of a reaction time task (Social Threat Aggression Paradigm) to promote anger induction would produce changes in the RSFC among different brain structures in a sample of healthy young women. On this task, participants had to punish an opponent if he/she (loser) presented longer reaction times than the participant (winner). The punishment consisted of an aversive tone whose intensity was manipulated by the winner. The authors concluded that although the resting functional connectivity (before the laboratory task) among the basolateral amygdala (BLA), the medial orbitofrontal cortex (mOFC), and the lateral orbitofrontal cortex (OFC) (bilaterally) was unrelated to the anger levels in the Social Threat Aggression Paradigm (a laboratory task), participants who presented higher increases in BLA–mOFC connectivity after the task showed a less aggressive response to this task [46]. Moreover, high baseline RSFC between the BLA and the left superior temporal gyrus (STG) was correlated with high aggression levels on the laboratory task. By contrast, high basal connectivity between the BLA and the superior parietal lobule (SPL) was associated with lower aggression [46]. 3.4.2. Violent Group Two groups of men (reactive violent offenders and non-violent offenders) participated in a laboratory task to promote different emotional states (they had to pay attention to several audiotaped angry, happy, and/or neutral stories). This is an adapted version of the Anger Articulated Thoughts during Simulated Situations (ATSS) paradigm for fMRI. Authors of the study concluded that before the emotional task, reactive violent offenders showed a heightened RSFC between the left medial PFC (mPFC) and the left amygdala, as well as a diminished pre-task RSFC between the left amygdala and the uncus/amygdala and posterior insula. After the emotion task, violent offenders showed a significant decrease in the RSFC between the left mPFC and the left amygdala, but non-offender controls experienced an increase in RSFC. Furthermore, an increase was found in the RSFC between the left amygdala and the right posterior insula and right superior temporal gyrus in violent offenders after the task, but the control group showed a decreased RSFC between the left amygdala and the right posterior insula and right superior temporal gyrus, as well as the left uncus/amygdala [47]. 4. Violent Populations Finally, in order to complete the previously mentioned results, it is important to analyze whether individuals with a proneness to expressing anger present alterations in the RSFC among the brain structures that have been identified as responsible (at least in part) for violence-related concepts. First, violent juvenile offenders showed significantly lower resting regional connectivity between the following brain structures and their adjacent structures: the right caudate, right medial prefrontal cortex, and left precuneus. However, significantly higher RSFC was also found between the right supramarginal gyrus and its adjacent brain structures, compared to the non-violent control group [48]. One study compared the RSFC of a group of violent inmates to that of a non-violent group, and they concluded that the violent offender group showed an increase in the RSFC between the left amygdala and the right cerebellar hemisphere. Furthermore, these violent offenders also presented an increase in the RSFC with the dorsolateral prefrontal cortex (DLPFC) (bilateral). Nonetheless, inmates showed a decrease in RSFC between the left/right cerebellar hemisphere and the left/right orbitofrontal cortex (OFC), as well as between the vermis and the left OFC [49]. Varkevisser, Gladwin, Heesink, van Honk, and Geuze [50] compared the RSFC of a group of aggressive and impulsive soldiers to a non-violent group. Although no significant group differences in functional connectivity were found between the orbitofrontal cortex and basolateral amygdala, significant patterns of connectivity were found in impulsive and aggressive soldiers. First, these authors concluded that the left dorsolateral prefrontal cortex presents a negative association with the (bilateral) basolateral amygdala. Nevertheless, they found a positive association between the left centromedial (CeM) amygdala and a region spanning the left fusiform gyrus and lingual gyrus, as well as between the left anterior cingulate cortex (ACC) and a region spanning the left cuneus, calcarine cortex, Behav. Sci. 2019, 9, 11 10 of 19 and superior occipital cortex. Furthermore, they also found a positive association between the right ACC and a region spanning the left cuneus, calcarine cortex, superior occipital cortex, and precuneus. Finally, they demonstrated a positive relationship between the left anterior insular cortex (AIC) and the right temporal pole. However, in the control group, the associations among these brain structures presented the opposite connectivity pattern. 5. Discussion The results described here offer a better understanding of RSFC that might explain proneness to violence, particularly the neural pathways that underlie key variables of violence, such as reactive and proactive violence, trait anger, and anger expression and/or control. It should be noted that only one study failed to find a significant association between the RSFC of the bilateral anterior temporal lobe and mOFC and the anger trait; the other 16 manuscripts did find a significant association between these variables. Even though several studies highlighted that the diminished RSFC between the PFC and the amygdala increased proneness to reactive violence, we also summarized other brain networks that include additional cortical (i.e., insula, gyrus (angular, supramarginal, temporal, fusiform, superior and middle frontal), ACC, and PCC) and subcortical brain structures (i.e., hippocampus, cerebellum, ventral striatum, and nucleus centralis superior) that might facilitate the onset of this type of violence. Moreover, we also described the neural pathways that might explain proactive violence and feelings of revenge, which are focused on the RSFC between the OFC, ventral striatal, angular gyrus, mid-occipital cortex, and cerebellum (Table 2). Initially, we concluded that the diminished RSFC between frontal structures such as the PFC (OFC and vmPFC) and frontopolar cortex (Brodmann area 10; PFC), limbic structures such as the amygdala and the anterior insula, parietal cortex regions such as the supramarginal gyrus (Brodmann area 40; parietal lobe), the angular region (posterior to the supramarginal gyrus), and the nucleus centralis superior (median raphe nucleus; brainstem) was related to a high predisposition to experiencing anger and/or responding to stressful and distressing situations with anger (high anger expression-out and low control-out) in a normative population and in participants with mental disorders. As previously stated, it appears that prefrontal structures tend to maintain inhibitory projections to other brain structures involved in emotional reactivity, such as the amygdala and/or the insula, and so the failure to regulate this reactivity might lead to high irritability or hostile reactions [8–15]. Although these studies did not analyze the RSFC between these brain structures, all of the manuscripts that were included in this systematic review found a diminished RSFC connectivity between the PFC and amygdala, which has been associated with proneness to experiencing feelings of anger and difficulties in controlling anger expression [34,35,39,46,47,50]. In fact, alterations in the dorsal and ventral PFC, amygdala, and angular gyrus have commonly been associated with rule-breaking behaviors, alterations in moral judgement and reasoning, and emotion regulation [8]. In this regard, we reinforced the hypothesis that diminished RSFC between the frontal and limbic systems might be characteristic of violent populations, since one of the studies that was included in this review concluded that a group of violent and impulsive soldiers presented a lower RSFC between the left dorsolateral PFC and the basolateral amygdala (bilateral) than a non-violent group [47,50]. Conversely, research conducted with normative young adults demonstrated that individuals with higher RSFC between the mOFC and the basolateral amygdala showed less aggressive strategies on an anger induction laboratory task [46]. Moreover, another study stated that reactive violent offenders presented a diminished RSFC between the left mOFC and left amygdala, but an increase in paralimbic RSFC after an emotion induction task [47]. Behav. Sci. 2019, 9, 11 11 of 19 Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: ventromedial prefrontal cortex. Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: ventromedial prefrontal cortex. Left mOFC Left amygdala Before emotional induction task (violent offenders) ventromedial prefrontal cortex. Left mOFC Left Lef unc t a u my s/ag my dag la d ala ⬆ Before emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left amygdala Functional Before emotional induction task (violent offenders) Brain Structure (From) Brain Structure (To) Functional Connectivity Aggression Assessment Brain structure (from) Brain structure (to) LefP t o u snc ter u is o/ra i my nsu gld aa la Aggression assessment ventromedial prefrontal cortex. Left mOFC Left amygdala Before emotional induction task (violent offenders) Left amygdala cF ounc nnetc it o ina vitly ⬇ ⬆ Before emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Brain structure (from) Left mOF Bra Ci n structure (to) P Lef oster t ai my or g ins da u ll aa Aggression assessment Af ter emotional induction task (violent offenders) Trait aggression Trait aggression Lef cot nn unc ecu tisv /a itmy y gdala ventromedial prefrontal cortex. Lef Lef t a t my mOF gda Cl a Left amygdala ⬆ Bef Befo or re emo e emoti tio ona nal l i indu nduc ct ti io on n t ta as sk k ( (v vi io ol lent ent o of ff fender enders s) ) Left mOFC Rig Fht Lef unc p t o ta is o my ter naig lo da r il ns a ula ⬇ After emotional induction task (violent offenders) Brain structure (from) Brain structure (to) Posterior insula Aggression assessment Trait aggression Left amygdala After emotional induction task (violent offenders) Left mOFC Left mOFC ⬇ ⬆ Trait aggr ⬆ Tr ession ait aggression Lef cot nn unc ecu tisv /a itmy y gdala Right R isg uht per pio o srter temp ior io ns rau l lg ay rus Amygdala (bilateral) Amygdala (bilateral) Left mOFC Left mOFC Lef t amygdala Left ⬆a mygdala Before emo ⬆ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Lef Lef t a t my mOF gda Cl a FLef unc t ta io my nag l dala ⬇ Bef After ore emo emoti ti o o na na ll i i n ndu ducc ti ti o o n n ta ta ss k k ( ( vi vi o o ll ent ento o ff ff ender ender ss )) Left amygdala ⬇ After emotional induction task (violent offenders) vmPFC Lef vmP t mOF FC C ⬇ ⬇ ⬆ Trait aggr ⬆ ⬆ Tr Tr ession a ai it t a ag gg gr res ess si io on n Posterior insula Trait aggrB es ra siio n ns tructure (from) Brain structure (to) Aggression assessment Amygdala (bilateral) Violent populations (no-self reported) Right superior temporal gyrus Left uncus/amygdala Left uncus/amygdala connectivity vmPFC Right posterior insula Nucleus centralis superior (median raphe ⬇ ⬆ Trait aggression Left amygdala Left amygdala ⬇ Before emo ⬇ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Lef Lef t a t my mOF gda Cl a Left amygdala ⬇ Af After ter em emo oti tio ona nal l i indu nduc cti tio on n ta tas sk k ( (vi vio ol lent ent o of ff fender enders s) ) Nucleus centralis superior (median raphe nucleus) VioFr lent ontopolar pC op au ul d aa ti te o cortex ns nu (c no leu -(Br s sel (Lef r fodmann ir gep ht) t mOF o rted) Car ea 10) ⬇ ⬆ Trait aggr ⬆ Tr ession ait aggression Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Posterior insula Posterior insula Trait aggression Right superior temporal gyrus Amygdala (bilateral) Nucleus centralis nu su cp leu ers io ) r (median raphe Left mOFC Left mOFC Lef t amygdala Left ⬆a mygdala Before emo ⬆ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Right posterior insula CaudmP ate F nu C c (lreu ight) s (r ig vmP ht) FC Adjacen ⬇ t structures ⬇ ⬆ Trait aggression Young violent offenders Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Left mOFC Left mOFC Lef t amygdala Left ⬇a mygdala After em ⬇ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) Violent populLef atio t ns amy (no g- da sel la Lef f rep t mOF orted) C ⬇ ⬆ ⬆ Trait aggression After emotional induction task (violent offenders) vmPFC nucleus) Bilateral supramarginal gyrus Trait aggression vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Left uncus/amygdala Left uncus/amygdala Amygdala (bilateral) Right superior temporal gyrus Nucleus centralis superior (median raphe PmP recu Fneu C (rs ig (ht) left) Adjacent structures ⬇ Young violent offenders Left amygdala Left amygdala ⬇ Before emo ⬇ tional induction task (vio Bef lent or e emo offender tios na ) l induction task (violent offenders) Right posterior insula Right posterior insula vmPFC ⬇ ⬆ Trait aggression CauF dr ao te nto nu pc o lleu ars c (o rr ig tex ht) ( Brodmann area 10) ⬇ ⬆ Trait aggression AmyvmP gdala F C (r ight) Bi Inf laer ter io ar l s fr uo p nta rama l gy rg ru ina s (lr g ig yht) rus ⬇ ⬆⬆ Tr Tr aa it it aa gg gg rr es es ss io io n n Posterior insula Poster ⬆ ior insula Left amygdala Left amygdala ⬆ After em ⬆ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) Amygdala (right) Violent pInferior opulations fr ontal (no-sel gyr f rep us or (right) ted) Trait aggression nucleus) Suprama Precu rgin neu al g s y (l ref us t) ( right) Adjacent structures ⬆ Young violent offenders Table 2. Resting functional con Ta nec ble tivit 2.y Re aR n st id g in ht it gs sfunct u ro ple er iin io or n a temp a nl gc eo o rn rpr a n lec o gn y tivit r en uses y. a m nR d OF ig it ht C: s r s o m ule ped er in iia o r a l n temp og rb er it o o pr rfr ao lo n g n y en tra u es l sc .o m rtex OF , C: OF m C: ed oia rblit o o rfr bit on ofr tao l n co ta rl tex co,r t P ex FC: , OF prC: efro orn btit ao l fr co o rn tex tal , c vo m rtP ex FC: , PFC: prefrontal cortex, vmPFC: Nucleus centralis superior (median raphe mPFC (right) Adjacent structures Young violent offenders Amygdala (right) Infer Ang ior u fr la or nta gylr g uy s r(u ri sg (ht) rig ht) ⬆ ⬆ Trait aggression Left mOFC Left mOFC Lef t amygdala Left ⬇a mygdala After em ⬇ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) CauF dr ao te nto nu pc o lleu ars c (o rr ig tex ht) ( Brodmann area 10) ⬇ ⬆ Trait aggression vmPFC Su Rig pht ra ma cerr ebe gBi in lla la a lter rg hem y arlu ssu i s (p p rr iher g aht) ma e rginal gyrus Adj Lef act ent ⬇a my str g u da ctu lar es ⬆ ⬆ Trait aggression Young Vio vi lent olent inm of aftes ender s Violent populations (no-self reported) Vio lent popuAngular lations (no gyr -sel us f rep (right) orted) nucleus) Precuneus (left) ventromedial prefrontal cortexv . entromedial prefrontal cortex. vmPFC Pos Ang terio ur l a cri ng gyu ru la sted (rig cht) ortex ⬆ ⬆ Trait aggression Right posterior insula Right posterior insula mPFC (right) Adjacent structures ⬇ Young violent offenders Amygdala (right) Bi R la ig ter hta c l er cer ebe ebe Il nf la ll er r a r hem io hem r fr is oip nta sher pher l e g y e rus (right) Lef Bila t ter amy al g O da FC la ⬆ ⬆ Trait aggression V Vi io ol lent ent i inm nma ates tes ⬆ ⬇ Left amygdala Left amygdala ⬆ After em ⬆ otional induction task (violAf ent ter o fem fender otios na ) l induction task (violent offenders) vmPFC Caudate nucleus (right) C Posterior audate nucingulated cleus (right) cortex Trait aggression vmPFC SupramargBi inla alter gy arlu ssu (p rr ig aht) ma rginal gyrus Adjacent structures ⬆ Trait aggression Young violent offenders ⬇ ⬆ vmPFC Poster Do io rr s o cme ingdi ula alted PFC co r tex ⬆ ⬆ Trait aggression Right superior temporal gyrus Right superior temporal gyrus Precuneus (left) Bilateral cerebellar hemisphere Func Bilatter iona al lO FC Functional Violent inmates CerebellarAng veru m lis ar gyrus (right) Left OFC ⬇ ⬇ Violent inmates mPFC (right) mP Dorsomedial FC (riAdj ght) a cen PFC t structures Adjacen ⬇ t structures ⬇ Young violent offenders Young violent offenders Right cerebellar hemisphere Left amygdala Violent inmates Bra Am in s ytg rda uct la ur (e ri g (fro ht)m ) Brain struc Inf tur er e B i o ra (fro r ifn rm osnta t )r uc l g tur yre u s (t ( or)i ght) Brain st⬆ r ucture (to) ⬆ Ag⬆ g re Tr sa siito a n ga gs rs es es ss io m ne nt Aggression assessment Anger expression Dorsomedial PFC Violent populations (no-self reported) Vio lent populations (no-self reported) Supramarginal gyrus (right) Adjacent structures Young violent offenders vmPFC Posterior cingulated cortex connectivity connectivity ⬆ Trait aggression Lef Ct er do ebe rslo la la rter ver al m Pis F C Right do Lef ⬆r st oO laF ter C al PFC ⬆ ⬇ V Vi io ol lent ent i inm nma ates tes Precuneus (left) Precuneus (left) Left mOFC Left mOFC Left amygdala Left amygdala Before emotional induction task Bef (vio olrent e emo offti ender onal si)ndu ction task (violent offenders) Bilateral cerebellAng ar hem ulairs p gher yrue s (right) Bila⬆ ter al OFC ⬆ ⬇ Violent inmates Anger expr Am essy io gn da la (bilateral) Left mOFC ⬇ Anger control-out Anger expression Caudate nucleus (right) Caudate nucleus (right) ⬇ Right cerebellar hemisphere Left amygdala ⬆ Violent inmates Trait aggression Trait aggression Dorsomedial PFC Amyg Lef dat lado ba rs so ol la ater tera al l ( P bi FC la teral) R Lef ight t do do rr ss oo la la ter ter aa l lP P FF C C ⬇ ⬆ Impulsive Vio al nd ent ai g nm gres ates sive group Supramarginal gyrus (right) Supramarginal g Adj yrua sc ( ent rig ht) str uctures Adjacent ⬆ structures ⬆ Young violent offenders Young violent offenders Left uncus/amygdala Left uncus/amygdala vmPFC CerebelP la or s ter ver io m r is ci ngulated cortex Lef ⬆ t OFC ⬇ ⬆ Trait aggression Violent inmates Amygdala (bilateral) Left mOFC ⬇ Anger control-out mPFC (right) Pari mP etaF l C (s u (r p iAdj g ra ht) ma a cr en gitn s atr l u and ctur aes ng ular gyrus) Adjacen ⬇ ⬇ t structures ⬇ Young violent offenders Young violent offenders Left amygdala Bilater Lef alt ca er my ebe gda llal ra hem isphere Bilateral OFC Before emo ⬇ tional induction task Bef (vio olrent e emo offti ender onal si)ndu Vc io tilo ent n ta inm sk ( a v tes iol ent offenders) Anger expression ⬇ ⬇ Amygdala (bilateral) Amygdala bas Left olater mOFC al Lef (bilt amOF teral)C Lef Lef t Lef t do fut ⬇ rss mOF io fo la rter m gy Ca l P ru Fs C ⬇ ⬇ Anger contr ⬆ Tra ol-out it aggression Impul⬆ si ve Traa ind t ag a gg rg es res sio sn ive group Right cerebellar hemisphere Right cerebellar hem Lef is t p aher mye g dala Left ⬆a mygdala ⬆ Violent inmates Violent inmates Do Po rs ster ome iodi r ia ns l P uF la C Posterior insula Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates H Am ipp yg oda camp la (u bi sl a (r ter ight) al) Lef Am t P cF a en y r ro i g tr et nta da o ame ll la ( l s( o di u bi be ( p a lr a la ter a s ma my ua pl rer ) g g d iin o aa r l a la a nd nd mi ang ddl ule ar fr g oy nta rul s ) ⬆ ⬆ Anger expression-out Impulsive and aggressive group Precuneus (left) Precuneus (left) ⬆ Cerebellar vermis Left OFC ⬇ Violent inmates Amygdala (bilateral) Left mOFC vmPFC LefLi t f vmP ng u⬇ ⬇ su ifa o F lr C g m gy yrusr us ⬇ ⬇⬆ Ang Traer it a cg og ntr res os li-o on ut ⬆ Trait aggression Bilateral cerebellar hemisphere Bilateral cerebellar hem Bila is ter pher al O e FC Bila⬇ ter al OFC ⬇ Violent inmates Violent inmates Anger expressio Lef n t mOFC Left mOFC Left amygdala Left amygdala After emotional induction task (vi Af oter lent em ofo fti ender onal si)n duction task (violent offenders) Amygdala basolateral (bilateral) Left dor ⬇s olateral PFC ⬇ ⬇ Impulsive and aggressive group Hippocampus (right) Parietal Left cF en r (supramar o tr nta ome l lo di be ( al a ginal smy uper g gy d iand o r au r l a s a )nd angular middle frontal ⬆ ⬆ Anger expression-out Impulsive and aggressive group Supramarginal gyrus (right) Supramarginal g Adj yrua sc ( ent rig ht) str uctures Adjacent ⬆ ⬆ structures ⬆ Young violent offenders Young violent offenders Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Nucleus centralis superior (median Nr u ac p leu he s centr Pa arliiet s a su l p (ser up io rr a ma (me rg di in an al ra and phe angular gyrus) Li Lef ngt uc au l neu gyru s s Cerebellar vermis Cerebellar vermLef is t OFC Lef ⬇ t OFC ⬇ Violent inmates Violent inmates Right posterior insula Right posterior insula Amygdala (bilateral) gyrus) Left mOFC Left fu⬇ s iform gyrus ⬇ Anger control-out Proactive aggression Frontopolar cortex gy r(u Br s)o dmann area F r1 o0 nto ) polar cortex ⬇ (Brodmann area 10) ⬇ ⬆ Trait aggression ⬆ Trait aggression Right cer Lef ebe t lmOF lar hem C isphere Right Lef cert ebe mOF llarC hem Lef Lef is t t p a aher my mye g g da dal la a Lef Lef t amy t ⬆a my gda glda a la Before emo ⬆ tional V indu iolent ctioin nm taa stes k (Bef v ioo lent re emo offender tionals ) i ndu Vic otlient on tia nm sk a (v tes io lent offenders) ⬆ ⬆ Left amygdala Amyg Lef dalt aa ba my so glda ater la al (bilateral) Left dorsolateral PFC After emotional induction task (vi Af oter lent em ofo fti ender o Ina mp l s u i)ndu l sive cti ao nd n ta ag sg kr (es vis o il ve ent gr oo fu fender p s) HippocampusH (right) ippocampus (right) Left cF en ro tr nta ome l lo di be ( al a smy uper gd io ar l a a nd middle frontal ⬆ ⬆ Anger ⬆ ⬇ expression-out Impulsive and aggressive group nucleus) Left anter nu ior c lc eu ing s)u late cortex Left Lef ca⬆ lc t a cr u ine neu cs o rtex ⬆ ⬆ Anger expression-out Impulsive and aggressive soldiers Left dorsolateral PFC Left dorsola Rter ight al do PFC rs olateral PFC Right dorsolateral PFC Violent inmates Violent inmates Right superior temporal gyrus Right superior ⬆ temp oral gyrus ⬆ Frontal lobe Pariet (superior al (suprama and rgimiddle nal and a fr ng ontal ular gyrus) Lingual gyrus Proactive aggV res entr sioa nl striatal Angular gyrus Bilateral cerebellar hemisphere Bilateral cerebellar hem Bila is ter pher al O e FC Bila⬆ ⬇ ter al OFC ⬇ ⬆ Pr V oia oclt ent ive ia nm gga res tes s ion Violent inmates Left uncus/amygdala Left uncus/amygdala Left fusiform gyrus gyrus) Left superior occipital cortex vmPFC Left antervmP ioBi r c la i F ng ter C u alla s te u p cr oa rma tex rginal gyrus BilaterLef al st ucp ar ⬇ la c a ma rine rgic na orltex gy rus ⬇ ⬆ ⬆ Trait aggression Impul⬆ si ve Tr aa nd it a ag gg grres esssiio ve n soldiers Left amygdala Left amygdala Before emotional induction task (Bef vioo lent re emo offender tionals ) i nduction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: med⬇ ia l orbitofrontal cortex, OFC: ⬇ o rbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Violent Am p yo gp da ulla at iba ons so ( la no ter -sa el l f ( bi rep later o V rited) o al l) ent p Am oLef py ug l t a da c ten io la ns tr ba o (me no sol - di a sLef el ter alf a a t rl ep my do (bi o r g r l sa d ted) oter a la la ter a l)a l PFC Left dor ⬇s olateral PFC ⬇ Impulsive and aggressive group I Imp mpu ul ls si ive ve a and nd a ag gg gr res ess si ive ve g gr ro ou up p Hippocampus (right) Frontal lo gyr be (us) superior and middle frontal Lef ⬆t cuneus ⬆ ⬆ Anger expression-out Ventral striatal Angular gyrus ⬆ Proactive aggression Physical aggC res ers ebe ionl lar vermis Cerebellar ver Pm osLef is ter it oO r F ins C ula PosterLef io ⬆r t ins OF uC la Violent inmates Violent inmates ⬇ ⬇ Lingual gyrus Proactive aggression Left superior occipital cortex Amygdala (right) Amygda Inf laer (riio grht) fro ntal gyrus (right) Inferior frLef onta ⬆t c l u gneu yrus s ( right) ⬆ ⬆ Trait aggression ⬆ Trait aggression Caudate nucleus (right) Caudate nucleus Lef (rigt ht) fug si y fr ou rm gy s) rus Left fusiform gyrus Left anterior cingulate cortex ventromedLef ial t p cr aefr lcao rin ne tac l o cro tex rtex . ⬆ Impulsive and aggressive soldiers Left mOFC Left amygdala ⬆ Before emotional induction task (violent offenders) Physical ag Lef gres t do Lef sO io r F n s t C o mOF l ( alter eft) C a l PFC Lef Lef t do t mOF rsola RC ter iLef g ht a Lef l t do P ang t FC r as my u olla ag rter da reg alla i o Pn F C RLef ight t a do my ⬇r sg oda later la al PFC After emotiona ⬆l P iV n hy du io slic ent cti ao l n a inm g ta gr s a es k tes ( svi iAf oo nl ter ent em off oender tionals ) i ndu Vc io tilo ent n ta inm sk (a vi tes ol ent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: med⬆ ⬇ ia l orbitofrontal cortex, OFC: ⬇ o r⬆ b itofrontal cortex, PFC: prefrontal cortex, vmPFC: Proactive aggression Left centromedial amygdala Left centromedial amygdala Lef ⬆t cuneus ⬆ Impulsive and aggressive group Impulsive and aggressive group Lef Lef t p t r cecu uneu neu s s Ventral striatal Ang Ang ular u g la yrr u gy s r (u ris g ht) Angular ⬆ g yrus (right) ⬆ Proactive aggression Lingual gyrus Lingual gyrus mPFC (right) mPFC (right) Adj acent structures Adjacent ⬇ str uctures ⬇ Young violent offenders Young violent offenders Proactive aggression Right anterior cingulated cortex Left superior occipital cortex ⬆ Impulsive and aggressive soldiers Left uncus/amygdala OFC (left) Left angular region ⬇ ⬆ Physical aggression Amygdala basolateral (bilateral) Amygdala basolaR Lef ter iga t ht ldo (p bi r ol ss a o ter ter later ia olr )a ilns Pu FC la Rig Lef ht p t do oster r ⬇s o io la rter ins au l l P aF C ⬇ Impu⬆ ls i P ve hya snd ica la a gg gg res res si sve ion gr o u p I mp u l s i ve a nd a g g r es si ve g r o u p Left anterior cingulate cortex ventromedLef ial t p cr aefr lcao rin ne tac l o cro tex rtex . ⬆ Impulsive and aggressive soldiers Left mOFC Left mOFC Left amygdalLef a Lef t ca t lp ca recu rine Lef neu c t oa rs my tex g dala ⬆ ⬆ Before emotional inductiBef on o ta re emo sk (vio ti lent ona l o f indu fender ctio s) n task (violent offenders) Physical aggressio vmP n FC Left vmP amy Pg o Fs da C ter la i or cingulated cortex PosterF io unc r ci⬆ ng ti ou na lalted cortex ⬇⬆ ⬆ Trait aggression Bef ore emotional ⬆ indu Trac it t ia og n gtra es sk s i(o vn io lent offenders) Anter Left aimy or ig ns da ulla a Left amygdala OFC After emotional induction task (vi Af ol ter ent em off oender tionals ) i nduction task (violent offenders) ⬇ ⬆ ⬆ Ventral striatal Precuneus (left) Precuneu Angular s (left) gyr Left us cuneus Left cuneus Proactive aggression Ventral striatal Right anterior cingulAng ated uc la or r tex gyr us Lef ⬆t cuneus ⬆ ⬆ Proactive aggression Impulsive and aggressive soldiers Brain structure (from) Brain structure (to) Posterior insula Aggression assessment Right superior temporal gyrus Right superior temporal gyrus ⬆ ⬆ Des Phy tru sic cta ive l a g ag grg es res sis oin on Left fusiform gyrus Left fusiform gyrus Left superior occipital cortex Left uncus/aLef myt gLef s du ap lt a er c a io lc Lef ra o rict ne cu ip nc cio ta u rl tex s c /a o my rtex g dala OFC (left) Lef Dot ra so ng me uldi ara r l eg PF io Cn Do cor nn soe me ⬇ c tidi via ty l P FC ⬆ Physical aggression Anterior insula OFC Lef Left t a cnter entrio ome r cidi ng au l a la my te c go d ra tex la Lef Left t a cnter entrio ome r cidi ng Lef au l a la t my te ca c lg c o d a ra r tex ilne a cortex Left ca⬇ ⬆ lc arine cortex ⬆ Imp Imp uu ls ls ive ivea a nd nd a a gg gg rr es es ss ive ive s g or ldi ou er ps Imp Imp uu ls ls ive ivea a nd nd a a gg gg rr es es ss ive ive s g or ldi ou er ps SupramaLef rgit nmOF al gyr C u s (right) SupramarLef gint amOF l gyru C Adj s ( Lef ra ig ct ent ht) amy str g u da ctu lar es AdjLef acLef ent t a t my ⬆ ⬆ sp tr ru ecu gc da tu neu lra es s Befo ⬆r e emo ⬆ tio Y na ou l ng indu vic otlient on to afsfk ender (v Bef iolo sent re emo offender tiY oo na us ng l) i ndu vioc lent tion otfa fs ender k (vio sl ent offenders) Physical aggression Left amygdala Left amygdala Func⬆ ti onal ⬇ ⬆ ⬇ Before emotional inductiBef on o ta re emo sk (vio ti lent ona l o f indu fender ctio s) n task (violent offenders) Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Violent populations (no-self repoV rted) iolent populations (no-self Li rep ng ou rted) al gy rus Lingual gyrus ⬆ Destructive aggression Physical aggression Ventral striatum Right anterior cingulated cortex Left cuneus Impulsive and aggressive soldiers Brain structure (from) Brain structure (to) Posterior Lef insu t lsa u perior oc Pc o is pter itailo c ro ir ns tex u la ⬆ Aggression assessment Ang Traiter a g ex gr p es res sis oin o n Anger expression Anterior insula ⬆ ⬆ P Phy hys si ic ca al l a ag gg gr res ess si io on n Left superior occipital cortex Left superi⬆ o r occipital cortex Right cerebellar hemisphere Right cerebellar hemis Lef pher t ae my gdala Lef Left t a cmy alca gr da ine lac ortex Violent inmates Violent inmates OFC (left) Lef Lef t t ua nc ng uu sl /a ar my reg gd io an la Left co unn ncu e⬆ s c / ta iv my ityg dala ⬆ ⬆ Physical aggression Anterior insula OFC Right pos⬇ ter ior insula Anter Vientr or ca ing l str ulia ate tum co rtex ⬇ Caudate nucleus (right) Caudate nucleus (rigLef ht) t cuneus Left cuneus Left amygdala Left amygdala Left precuneus Before emotional induction task (v Bef iolo ent re emo offender tionasl) i nduction task (violent offenders) Left mOFC Left mOFC Left amygdala ⬇ Left amygdala ⬇ ⬇ ⬇ After emotional inductioAf n ta ter sk em (vi oo ti lent onal o i fn fender ductio s) n task (violent offenders) Amygdala (bilateral) Am Lef yg t da amy la ( g bi da la lter a Lef Lef al) t t mOF mOFC C Left mOFC ⬆ ⬆ Des ⬇⬆ Ang Tr tru aer i ctt ia ve cg og ntr a rg es o gs lri-es o on u s Af i t o ter n emotional⬇ indu Ang cer tio c no ta ntr sk o l(-vi ou ot lent offenders) OFC (left) Anterior insula Left angular region ⬇ ⬇ ⬇Physical ⬆ P aggr hysiession cal aggression Left cuneus Lef ⬆t cuneus Bilateral cerebellar hemisphere Bila Rter ight al a cer nter ebe io lr la c ri ng hem uP li a Bi o ste s p lter a d her ter c io o e a r r ltex iO ns F u C la Left Bi P su o lp s ater ter eriio a ol rr O o ins c FcC iu p lia t al cortex ⬆ Violent inmates ImpulV siive olent and inm agg ar tes ess ive soldiers Trait aggression ⬇ ⬇ Amygdala (bilateral) Right superior temporal gyrus ⬆ Physical aggression Reveng Lef e fe t e alnter ing mP s io F r C ci ( ng rig uht) late cortex Left amP nter FiC o r( r cAnter iig ng ht) Lef Adj u la t io a te cc ra en c c lc i o ng a tr r tex sitr u ne lu ac c te tu or cr tex o es rtex Adj Lef act en ca t ls ctr ar u ine ctuc ro es rtex Impu Y ls oiu ve ng a nd vio a lent ggres off sender ive sos ldi ers Imp Yo uu ls ng ive vi ao nd lent ago gfr fes ender sives s oldiers Left ca⬆ ⬇ lc arine cortex ⬇ ⬆ Right posterior insula Right posterior insula Anterior insula vmP OFC FC ⬇ ⬇ ⬆ Trait aggression Parietal (suprV ama entr rg ailn s a tr l ia and tum ang ulP ar a r g iy et ra uls ()s upramarginal and angular gyrus) Left precuneus Left precuneus Left mOFC Left mOFC Left amygdala Left amygdala After emotional induction task (vi Af olter ent em offo ender tionasl) i nduction task (violent offenders) Cerebellar vermis Left amygda Cler a ebellar ver Lef mis t a Lef my Lef t g t mOF da OF la C C Left ⬇ ⬇ O FC ⬆ ⬇⬇ ⬆ ViAf olent ter iem nm oa ti tes ona l inductioAf n ta ter sk V em ( ivi oo lo ent ti lent ona inm l o i fndu f aender tesc tio s) n task (violent offenders) Anterior insula Violent populations (no-OFC self reported) ⬇ Physical aggression ⬆ Des ⬆ Destr Tr tru ai cttuctive ia ve gg a rg es gsaggr ries on sio ession n Revenge feeliP Anter ng recu s neu ior isns (lu ef lt) a Precuneu Lef s (t lef su t) p erior occipital cortex Left superi⬆ o r occipital cortex ⬆ Physical aggression Right anter Lef iort c mOF inguC la ted cortex Right anter Lef iot r mOF cingu R C lLef ia gte ht t d a cc my er or ebe tex gda l lu la m Left suLef pert io ⬆ ⬆ ar my ocg cda ipilta a l cortex Before emo ⬆ ⬆ Imp tiu ona lsive l indu and c ta ig og n rtes assk ive (v is Bef o ollent di orer e emo osf fender Imp tio u na s ls ) ilve indu and ct i ao g n gr ta es sk si ve (vi o so lent ldier of sf enders) Amygdala (bilateral) Right superior temporal R giy g rht us s uperior temporal gyrus Nucleus centr Hipa plo is c a smp uper ui so (rr i(g me ht) di an raphe Hip Fp ro onta camp l lAnter o u be ( s (rs iig u oht) p r er ci ng ioru a la nd te mi cor ddl texe F fr ro onta ntall lobe (superior and middle frontal ⬆ Anger expression-out ⬆ Anger expression-out ⬆ ⬆ Right OFC Left calcarine cortex Left ca⬆ lc arine cortex ⬆ Revenge feelings Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left dorsolateral PFC Left dorsolaterR a Ri lig g P ht ht FC do p vmP ors ster olF a iC o ter r i ans l P uF la C RiR giht ght do pro ss o⬆ ter l ater iora i lns PF uC la ⬆ Violent inmates Violent inmates CaudaF te ro nu nto clp eu ols a r ( V rc i entr g or ht) tex a l ( sBr trio adma tum nn area 10) ⬇ ⬆ ⬆ Tr Tra ai it t a ag gg gr res ess si io on n Supramarginal gyrus (right) Supramarginal gyrR Adj uis g ( ht a r Lef ic g a ent ht) ng t c u u str l neu au r cg tu sy r ru es s Adjacent Lef ⬇ s t tr cu uc neu turs es Young violent offenders Young violent offenders Lef Rt ig uht nc c uer s/ebe amy llg ud m a la Left unc⬆ u s/amygdala ⬆ Left amygdala Left amygdala After emotional induction task (vi Af olter ent em offo ender tionasl) i nduction task (violent offenders) Anterior insula Violent populations Ventral (no-V sel istriatu o fl r ent epo pro mAnterior ted) pul ations (no cingulate -self repo cortex rted) ⬆ ⬆ Physical aggression Anter nuic o lr eu ins s) ula gyrus) g⬆ y rus) ⬆ Physical aggression Revenge feelingR s ight OFC Left superior occipital cortex Left superior occipital cortex Left amygdala Left amygdala ⬆ ⬇ Before emo ⬇ tiona⬆ l iR ndu evenge ction fee tas li k ng (v siBef olent ore emo offender tiona s) l induction task (violent offenders) Right superior temporal gyrus Right superior temporal gyrus Amygdala basolateral (bilateral)Am ygdala basolatera Lef l (bi t do later rso alla ) teral PFC Left dorsol⬇ a teral PFC ⬇ Impulsive and aggressive groupI mpulsive and aggressive group Nucleus centralis superior (median raphe mPFC (r Anter ight) ior cingulate cortex Adjacent structures ventromedial p⬇ refr ontal cortex. Young violent offenders Right cer Lef ebe t lmOF lar hem C isphere Right cerebellar hem Rig iLef Lef Lef s ht pher t a t t p ng a ar my my eecu ula g gneu r da da gl l y a a s r us Lef Lef t at my ⬆ p rg ecu daneu la s Before emotional V indu iolent ctioin nm taa stes k (v iolent offenders) V iolent inmates Right OFC Right P m ositer doic o cri p ins itau l lc ao rtex Poster ⬆ ⬆ ior insula ⬆ ⬇ Revenge feelings Caudate nucleus (right) Caudate nucleus (right) Proactive aggressvmP ion FC Proactive aggrF es ro sinto oBi n l p ao ter lar a lc s ou rtex pra ma (Bro rg dma inalnn gya ru rea s 10) ⬇ ⬆ Trait aggression Right anterior cingulated cortex Right anterior cingu Rlia gte ht d cc er or ebe texl lum ⬇ ⬆ ⬆ Impulsi⬆ ve Tr and ai t aa gg gg rr es es ss ive ion s oldiers Impulsive and aggressive soldiers Violent populations (no-self repor V ted) iolent populations (no-self reported) Revenge feelings nucleus) Left fusiform gyrus Left fusiform gyrus Revenge feelings Precuneus (left) Right OFC Lef Left t u cnc alc u asr/ia ne my co gr d tex ala Left ca⬆ lc arine cortex ⬆ Revenge feelings LaborBi ato larter y ta als c kLef er R iebe gt ht mOF l lO ar F C hem C isphere Bilateral cerebe Left llmOF aR r ihem ght CLef Bi m isl p ia t do her ter amy cc a eil p g O ida ta FC ll a c ortex BiLef later t ⬆ ⬇ ⬇ a a my l Og Fda C la After ⬇ ⬇ em otional⬇ i V n Rdu ie o venge lc ent tion inm f ta ee s a lk tes ing (vi so Af lent tero em ffender otiona s)V l iin odu lent cti inm on ta ates sk (violent offenders) Left centromedial amygdalmP a FC Lef (rit gcht) en tromedial amP myF gC da (lra ig ht) Adjacent structures ⬆ Adjacent structur⬇ es ⬆ Impul⬇ si ve and aggressive Yo u gr ng ou vi pI o mp lent ulo sifve fender ands a Y go gu res ng s ivi ve o lg ent rouo p f fenders Ventral striatal Ventral striata Ang l ular gyrus Angular gyrus Am Lef yt ga da my lag (da riglht) a Infer R io ig rht fr o anta ngu l lg ay r rg u y sr ( u rs ig ht) ⬆ ⬆ ⬇ Bef Func ore emo ⬆t ionati l ona ⬆ P l⬆ r i o ndu Tr aa ct ic i tve ta io g a n gg rtes g ar ss es k io ( sn v io io nl ent offender ⬆s ) P roactive aggression Caudate nucleus (right) Caudate nucleus (rLi igng ht)u al gyrus Lingual gyrus vmPFC SupramarginBi a Lef l lg ater y t r su u R as p li g ( er sr u ht iig p o ht) c r ra er o ma c ebe cirp g li lit u na am l lc g oy rtex rus Lef Adj t su ap cer ent i⬇ o s r tr ou cc citu pirtes al cortex ⬆ ⬆ Trait aggression Young violent offenders Brain structure P (fro oster m)i or insula Brain structure (to) Aggression assessment Laboratory tC as er kebe llar vermis Cerebella Lef r ver t R sim u gp ht is er p Lef io or s t ter temp OiF oC ro ir ns alu g la y rus Right Lef po t ⬆ ⬇ s O ter FC io r insula ⬇⬆ Aggressive Vs itr ola ent tegiinm es (a la tes bo ratory task) Violent inmates Right cerebellum Precuneus (left) Precuneus (left) Right OFC ⬆ ⬆ Revenge feelings Physical aggress R io ig n ht OFC Physical aggression RiAng ght m ulia do r g cy cr ip uista (r l ic go ht) rtex ⬆ connectivity ⬇ Revenge feelings Left amygdala Left amygdala ⬆ After ⬆ em otional induction task (vioAf lent tero em ffender otiona s) l induction task (violent offenders) Right OFC mPFC (right) mPFC (right) Adj acent structures Adjacent structures Revenge Young feelings violent offenders Young violent offenders Left mOFC Left mOFC Lef Lef t a t my cuneu gda sl a Left amygda Lef lat cu ⬇ neus Befor⬇ e emo tional inducBef tion orte emo ask (vti io olna ent l io ndu ffender ction s)t ask (violent offenders) Amygdala (right) Right cerebella Inf r hem er R io ig r iht sfp r o her anta ngeu l lg ay r rg u y sr ( u rs ig ht) Left amy ⬆ ⬆ gdala ⬆ ⬆ ⬆ Trait aggression Violent inmates Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Am Left ydo gda rs lo a lba ater so alla P ter FC al Left dorsoR lLef a iter ght R t a s i l g s u u P ht pp F er er C do i o imOFC o r rs r temp o temp later o a o rlr a a P l lF g g C yy r r uu ss RiR giht ght su do per rs io ⬆ o ⬆l r a temp teral o Pr F aC l gyrus ⬆⬆ Aggressive Vs itr ola ent tegiinm es (a la tes bo ratory task) Violent inmates Right angular gyrus Supramarginal gyrus (rig Su ht) p ramarginal gyrus (right) Adj acent structures Adjacent structur⬆ es ⬆ Young violent offenders Young violent offenders Labora Ta torble y ta s 2k . O Re vmP FC st in (F lef C gt) funct iona Tr l a cio t n an gg ec res tivit sion y O a Fn Cd P (o lit ef ster s Lef t)r io o t le r a ng c in ing u a lu a n r la g rted e eg r ipr o cn oo r tex nen es. mOFC: Lef m t a ed ng ⬇ ⬆ ia u lla o r rrb eg itio ofr n ontal cortex, OFC: o⬇ r bitofron ⬆ t⬆ P a hy l Tr cs a o iic r ta ta ex lg ag ,g rP g es r F es sC: io sin o pr n efrontal cor⬆ tex Phy , v sm ica P lF aC: ggression ⬆ Aggressive strategies (laboratory task) Precuneus (left) Precuneus (left) ⬇ Left anterior cingulate cortex Left anterior cingulLef a Lef tet t cu o cnc a rtex lc u asr /ia ne my co gr d tex ala Left uncus Lef /amy t ca gld ca ar l⬆ a ine cortex ⬆ Impulsive and aggressive soldier Imp s ulsive and aggressive soldiers Right OFC Bilateral cerebella RriAng g hem ht m u il sia p do rher g cy ce r ip u ista (r l ic go ht) rtex Bilater ⬆a l OFC ⬇ ⬇ Revenge feelings Violent inmates Right posterior insula Violent Am p yo g Am p da ull y a ag t iba da ons s lo a ( lba a no ter s -o sa el lla f ( ter bi rep l aa lter o rted) a V l) i o Am lent yg pda oplu al a ba tis oo ns la ter ( no Su Lef a-lp s ( el er t bi do fil o r aep r ter r mOFC sp o o a a lra l rted) )iter et a a ll lP oF bu Cl e Left dorso⬇ la teral PFC ⬇ Impulsive and aggressive group Impulsive and aggressive group Left amygdaR lai ght cerebe Lef llt aa r my hem gda isp la her R ig eht cerebellar hemisphere Left amygdala Left amygdala ⬆ Before emotiona ⬆l inducBef tion orte emo ask (vti io olna V ent il o i lo ndu ent ffender ic nm tion a stes )t as k (violent Vi o of lent fender inm s) a tes ⬇ ⬇ Left amygdala Left su Do per rsio ome r temp dial o PrF aC l g yrus Lef⬆ t mOFC After⬆ em Ag og ti ro es na s ⬆ il ve P indu hy str si a c cteg ti ao l n a ies g ta g ( r sles k a bo ( svi io ro n alto ent r y o ta ff s ender k ) s ⬆ ) P ⬆ hy Tr s a ic it a l a g a g g g r es r es s is o i o n n Right OFC Right midoccipital cortex ⬆ ⬆⬇ Ag Revenge gressive feelings strategies (laboratory task) Supramarginal gyrus (right) Lef Su t p mOF rama Cr gina Lef l gy t r s Adj u us p ( er arc iient g oht) r o s c tr cu ip citu tar l es co rtex v en Lef tLef rt oa m t my sed u Adj g pia da er a l ilc o a p ent r r o efr ⬇ cs c tr o ip u n ic tta tu all r cc es oo r r tex tex . Young vio Bef lent ore emo offender tios na l inductY io o n ut ng as k vi (o vlient olent of f o ender ffender s s) Posterior insula Posterior insula ⬆ ⬆ ⬆ Laboratory task vmPFC CerebellaP r o ver ster m io isr cingulated cortex Lef⬆ t OFC ⬆ Trait aggression Violent inmates Anterior insula Am Anter ygda R io lia g r ht (ibi ns s lu a uter la per ailo )O r F temp C oral gyrus OFC ⬇ Caudate nucleus (right) Caudate nuc lSu eu Lef p ser (t riifo g u r ht) s p ifa o r rim gy etal lr o u bu s le Left fusif⬇ o rm gyrus ⬇ Bilateral cerebellar hemis Bi plher ater ea l cerebellar hemisphere Bilateral OFC Bilateral OFC Violent inmates Violent inmates ⬇ ⬇ Anger exp Am ress y ig oda n la basolateral vmPFC ⬇ ⬆ Destructive aggression ⬆ Des ⬆ tr Tr u a citti ve ag g ar g es gr ses ios n io n Left centromedial amygdala Left centromedial amygdmOFC ala ⬆ ⬆ Impulsive and aggressive group Impulsive and aggressive group Right cerebellar hemisphere Right cerebellar hemLef ispher t amy e gdala Left amygdala Violent inmates Violent inmates Left mOFC Left mOFC Lef Lef t a t my cuneu gda sl a Left Lef unc t a u my s/ag my da Lef g la d t a clu ⬆ a neu s After ⬆ emotional inducti Af on ter ta s em k (o vi tio olna ent l io nfdu fender ction s )ta sk (violent offenders) Left dorsolateraDo l PF rs C o medial PFC Right dors⬇ o lateral PFC ⬇ Violent inmates Laboratory task Violent populations (no-self reported) Left superior temporal gyrus ⬆ ⬆ ⬆ Aggressive strategies (laboratory task) mPFC (right) mPFC (rig Adj ht) Li a ng cen uta s ltr gu yc ru tu sr es Adj Ling acu en a ⬇ ⬇l t g sy tr ru uc stu res ⬆⬇ Ag gres Yso ive ung str vi ao teg lent ieso (flfa ender borato s ry task) Young violent offenders Left amygdala Before emotional induction task (violent offenders) Functional ⬇ Cerebellar vermis Cerebellar vermis Left OFC Left OFC ⬇ ⬇ Violent inmates Violent inmates Amygdala (bilateral) Nucleus centralis sup er Su io p V r er entr (Lef me ior a di t p lmOF a a sr n tr iet ira a a C tu p l he lm obu le Ventra ⬇l striatum ⬇ Anger control-out Left precuneus Posterior iLef nsu t lp ar ecuneus Bilater Bra al i n cer stebe rucltlur are hem (froim sp )her e Bilateral cerebellar hem BraBi iin s lp a ster her truc ae lt O urF eC ( to) Bilater ⬇a l OFC ⬇ AggV re is os lent ion ia nm sseastes sm ent Violent inmates Anger exp Am ress y ig oda n la basolateral Right posterior insula Right posterior insula CauP d Anter r aecu te nu neu ioc rl i eu sns (l su ef (lr t) ai g ht) AmygdalAnter a P r ba ecu soineu lo arter ins s a (lu l ef (lbi a t) l amOFC teral) Frontop Lef olat r do cor rs tex ola (ter Bra oldma PFC nn area 10) ⬇ ⬆ Physical aggression Impuls ⬆i ve P ⬆hy Tr and sa ic i t a a l a g g a g g g rg r es es res ss ive iso io n g n r oup Left cuneus Left c⬆ u neus ⬆ ⬇ Right anterior cingulated cortex Right anterior cingulated cortex conne⬆ c tivity ⬆ Impulsive and aggressive soldier Imp s ulsive and aggressive soldiers Left amygdala Left amygdala After emotional inducti Af on ter ta s em k (o vi tio olna ent l io ndu ffender ction s )ta sk (violent offenders) Left dorsolaterLeft al PFsuperior C Left do temporal rsolateralgyr PFC us Right dorsolateral PFC ⬆ R ight dorsolateral P ⬆F C⬆ Aggressive strategies ⬆ (laboratory task) Violent inmates Violent inmates Pariet nu al c (ls Anter eu up sr )a ma ior rc g ii ng nau l la and te ca o ng rtex ul ar gyrus)Anter ior ci⬇ ng ulate cortex ⬆ Aggressive strategies (laboratory task) Left calcarine cortex Left calcarine cortex Cerebellar vermis Left mOF Cer Cebe lR lair g ver ht sm up is er Lef ior t temp OFC ora R l ig gy ht ru ss u Lef pert io ar my temp gdao lLef a ra l t ⬇ g O yr F u C s ⬇ ⬇ Violent Afiter nm em ates o tional induction ta V sik o l(ent violient nma otes ffender s) Amygdala (bilateral) Left mOFC ⬇ Anger control-out mPFC (right) Su Adj pera ic oen r p ta srtr iet ua ctu l lo res bu le Left fusif ⬇ ⬇ o rm gyrus Young violent offenders Lef Sup t r aa nter mar ig oi rn ca il ng gy ur lu ate s ( c ri o g rht) tex Lef Su t a p nter rama ior rg ciin ng alu glLef Adj y ate ru t s c a c o c ( aent r rli tex c g aht) rs itr ne uc ctu orr tex es Lef Adj t ca alc cent a⬆ ⬆ ri ne strcu oc rtu tex res ⬆ ⬆ Impu Y ls oiu ve ng a nd vio a lent ggres off sender ive sos ldi erIsmp ulsY ive oua ng nd vi ao glg ent ress oifve fender soldi ser s Trait aggression Amygdala basolateral (bi Am later yg ada l) la basolateral (bilater Lef alt ) dorsolateral PFC Left dorsolateral P⬇ F C ⬇ Impulsive and aggressive Imp gro uu ls p ive and aggressive group Revenge fe H eliip ng po sc ampus (right) Reveng Lef e fe t ce en liF ng tr ro o snta me vmP di l lo a F be ( l C a my sug pd er ailo ar and middle frontaBi l lateral sup⬆ r amarginal gyrus ⬆ ⬆ Anger expression-out Impulsive and aggressive group Amygdala basolateral ⬇ ⬆ Trait aggression Left superior occipital cortex Left superior occipital cortex Violent poLef pult ado tior ns so ( la no ter V -isa o el ll ent f P r F ep C p o or p ted) ulat ions (Lef no-t sdo elfr r sep ola oter rR ted) i ag l ht P F do C rsolateral PFC Right poster Rig io ht r ido nsu rsl⬆ o a l ateral PFC ⬆ Violent inmates Violent inmates Parietal (su mOFC pramarginal and angular gyrus) Lingual gyrus Precuneus (left) Right cerebellar hemisphere Right cerebeLef llart hem sup Lef er isip t oa her rmy oc ec gida pitla al cortex Left super Lef ior t o ⬆ ac my cip gida tall a co rtex ⬆ Violent inmates Violent inmates Left amygdala Left mOFC ⬇ ⬆ ⬆ Trait Af agter gres em sio on tio nal induction task (violent offender s) Left fusiform gyrus Left fusiform gyrus Aggressive strategies (laboratory task) gyrus) Amygdala (rR ig iht) ght cerebellum InferiR oirg fht ro c nta erebe l gy lr lu um s ( right) ⬆ ⬆ Trait aggression Right superior temporal gyrus Amyg Am daly a g ba da sl o al a (ter bila ater l (bi all) a teral) AmygdaSuperior la basolater parietal Lef al ( t bi do larter slobule ola alter ) al PFC Left dorso ⬇l ateral PFC ⬇ Impulsive and aggressive group Impulsive and aggressive group CH au ip dp ao te c a nu mp clu eu s s ( r Lef (ir g iht) g t ht) c en C a tr uo dme atedi nu alc a leu my F s r g (o r d Lef nta ia glht) a t l c l o en be ( trosme updi eri ao l ra a my ndg mi daddl la e frontal ⬆ ⬆ ⬆ ⬆ Ang er expresIsmp ionu -o ls u it ve and aggressive Imp gro uu ls p ive and aggressive group SupramaR rg ig in ht a lO gF yC ru s (right) Right OFAdj C acent structures Left ⬆ cu neus Young violent offenders Bilateral cerebellar hemisphere Bilateral cerebellar hem Bi Lef lia ster p t c her u alneu e O Fs C Lef Bil t ac⬆ ter ⬇ u neu al O s F C ⬆⬇ ⬆ V Rie o venge lent inm feea ltes ing s ⬆ R Ve ivenge olent i nm feelaites ngs vmPFC ⬇ ⬆ Trait aggression Lingual gyrus Lingual gyrus Proactive aggression Right angular gyrus Right angular gyrus Angular gyrus (right) mPFC (ri V giht) olent popula mP tions FC ( ( no rig -s ht) elf reported) Adj Lef t afcu en sit f o sr tr m gy ucturru es s Adjacent str Lef uc t tu fu rs es if orm gyrus Young violent offenderY s oung violent offenders Left anterior cingulate cog rtex yru s) Left calca ⬇r ine cortex ⬇ Impulsive and aggressive soldiers Right cerebellar hemisphere Lef Left t p ar my ecu gneu dala s Left pr⬆ ecu neus ⬆ Violent inmates Cerebellar vermis Cerebellar vermis Lef t OFC Lef ⬇ t OFC ⬇ Violent inmates Violent inmates Nucleu Lef s centr t cen atr lio s me sup di er ailo a rmy (me gd di aa la n raphe Left centromedial amygdala ⬆ ⬆ Impulsive and aggressive group Impulsive and aggressive group Left cuneus Left cuneus Right anter Ventr ior a cli ng stru ia lta ate l d cortex Right anterior cingulate Ang d co u rltex ar gyrus ⬆ Impul⬆ s iP ve roa and cti ve ag a gg res grs es ive si o sn o ldierIsmp ulsive and aggressive soldiers Right OFC RivmP ght R O F iF g C C ht midoccipital cortex P Ro ig ster ht i m or ido c⬆ i⬆ ng c ciu plia ta ted l co cr o tex rtex ⬆ ⬆ ⬆ ⬇ Revenge feelings ⬇⬆ R Tr evenge ait ag g fee res lisng ion s Precuneus (left) CauP dr aecu te nu neu cleu s (l sef F (r r t) o ig nto ht)p olar c Li ong rtex ua (lBr gy or dma us nn area 10) Lingu⬇ a l gyrus ⬆ Trait aggression Proactive aggression Left superior occipital cortex Bilateral cerebellar hemisphere Left Bi cla alter cara il ne Oc Fo C r tex Left calca⬇ ri ne cortex Violent inmates Left dorsolateral PFC Left dorsolaR ter iga ht l P do FC rs olateral PFC Right dorsolateral PFC Violent inmates Violent inmates ⬆ ⬆ nucleus) Left anterior cingulate co Lef rtex t a nterior cingulate cortex Lef t calcarine cortex Left calcarine cortex ⬆ ⬆ Impulsive and aggressive Imp solu di lser ive s and aggressive soldiers Physical aggression Laboratory task Laboratory task Dorsomedial PFC mPFC (right) Adjacent structures Young violent offenders Supramarginal gyrus (r Su igp ht) ra marginal gyrus (right) Adja Lef cent t c u str neu uctu s res Adjacent strucLef tures t ⬆ c u neus ⬆ ⬇ Young violent offenderY s oung violent offenders Ventral striatal Angular gyrus Left cuneus ⬆ Proactive aggression Cerebellar vermis Left superLef ior t oO cc FiC pi tal cortex Left superior ⬆ o ⬇ c cipital cortex Violent inmates Amygdala basolateral (bilateral) Amygdala basolater Lef at l do (bir ls ao ter laa ter l) al PFC Left dorsolateral PFC Impulsive and aggressive group Impulsive and aggressive group ⬇ ⬇ vmPFC Bilateral supramargiLef nalt g sy ur p u er s ior occipital coLef rtex ⬇t superior occipital cortex ⬆ Trait aggression OFC (left) Anger expression Left s Lef upt er aing or u temp lar reg ora io l n g yrus Left superior ⬆ ⬇ temporal gyrus ⬆ ⬆ Aggress ⬆ i ve Phy str si acteg al a ies gg ( rles abo sio rn ato ry⬆ ta Ag skg ) ressive strategies (laboratory task) Precuneus (left) Lef Rig t ht anter cerebe ior lclia ng r hem ulate is p c R o her irg tex ht e cerebe Lef llt aa rnter hem io is rp cher inge u Lef late Lef t c ca o t lrc a tex a my ri ne gda co la rtex Left amy Lef gda t cla al ca ⬆r ine cortex ⬆ Impulsive Va io nd lent agig nm res astes ive soldier Vs Ii mp olent uls ii nm ve a ates nd aggressive soldiers Left pr ⬆ ecu neus ⬆ Physical ag Lef gres t do sio rn so lateral PFC Right dorsolateral PFC Violent inmates Left fusiform gyrus Left fusiform gyrus Amygdala (right) Inferior frontal gyrus (right)Lef t cuneus Left cuneus Right anterior cingulated cortex ⬆ ⬆ ⬆ Trait aggression Impulsive and aggressive soldiers LefAm t cen ytr gda ome la di ba aslo a lmy ater g ad l ala Lef Am t Am cen yy g tr g da o da me la l a ba di (bi a so ll a l aa ter my ter aa g l mOFC ) ld ala Lef mOFC t mOF C ⬇ Impu⬆ ls i P ve hy a snd ica la a gg gg res res si sve ion gr o u p I mp u l s ⬇i ve Ang a nd er c a o gntr g r es o ls - io ve u t g r o u p Supramarginal gyrus (right) Adjacent structures ⬆ ⬆ Young violent offenders Left superior occipital cortex Left superior occipital cortex ⬆ Bilateral cerebellar hem Bi islp aher tera el cerebellar hemisphere Bilateral OFC BilateraLef l Ot Fc C a lca ⬇r ine cortex ⬇ Violent inmates Violent inmates OFC (left) Left angular region ⬇ ⬆ Physical aggression AmygdaAnter la basio olr a ter insa u lla (bi lateral) Left Li do ng rs u O o a F lla C g ter yr au l s P FC Ling⬇ ⬇ u al gyrus ⬆ Ag Imp gres uslisve ive str and ateg ag ies gr es (lasbo ive ra g to ro ry u ⬆ p ta Ag skg ) ressive strategies (laboratory task) ⬇ ⬇ Left precuneus Left precuneus Angular gyrus (right) Superior parietal lobule Parietal ( sSu upp ra er ma ior r g pia nra il et aa nd l loa bu ng lu e lar gyrus) ⬆ Destructive aggression Right cerebellar hemisphere Left amygdala Violent inmates Right anterior cingulated Rc ig oht rtex anter iorLef cing t cu ulneu ated s c ortex Left super Lef iot r co u cneu cipis t a l cortex ⬆ ⬆ ⬆ Impulsive and aggressive Imp solu di lser ive s and aggressive soldiers Cerebellar vermis Cerebellar vermis Left OFC Left OFC ⬇ ⬇ Violent inmates Violent inmates ⬆ Physical aggression Left Lef fust if co u rneu m gy s rus Left cuneus vmPFC Posterior cingulated coLef rtex t calcarine cortex Left calcarine cortex ⬆ ⬆ Trait aggression Anterior insula OFC ⬇ Left centromedial amygdala Hippocampus V (rentr ight) a l striatum Frontal lobe (super ⬆i or and middle frontal ⬆ Impulsive and aggressive group ⬆ Anger expression-out Left precuneus Left precuneus Bilateral cerebellar hemisphere Bilateral OFC ⬇ Violent inmates Left dorsolateral PFC Left dorsolateral PFC Right dorsolateral PFCR ight dorsolateral PF ⬆ C ⬆ Violent inmates Violent inmates Lingual gyrus ⬆ Destructive aggression Left anter Anter ior ic oir ng ins ulu alte a cortex Left anterior cingLef ulat te c a clo cr atex rine cortex Left cal⬆ ca rine cortex Impuls ⬆i ve Phy and sic a alg a g g rg es res sive sio s no ldiers Impulsive and aggressive soldiers Right anterior cingulated cortex Right anterior cingulated cortex ⬆ ⬆ Impulsive and aggressive soldiers I mpulsive and aggressive soldiers Dorsomedial P Lef FC t s uperior occipital coLef rtex ⬆ t superior occipital cortex ⬆ Anterior cingulate cortex gyrus) Left calcarine cortex Left calcarine cortex Cerebellar vermis Left OFC ⬇ Violent inmates Amygdala basolateral (Am bilay ter gda al) la basolateral (bilatera Lef l) t dorsolateral PFC Left dorsolateral PFC ⬇ ⬇ Impulsive and aggressiIve mp gu rl o su ive p and aggressive group Ventral striatum Left super Lef iot r co u cneu cipis t al cortex Left superior occipital cortex Anger expression Anterior insula ⬆ Physical aggression R evenge feelings P roactive aggressioLef n t superior occipital cortex Left superior⬆ o ccipital cortex Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Left fusiform gyrus Left fusiform gyrus Left anterior cingulate cortex Anter Left io cra c lc ing ariu ne lac te or ctex ortex Impulsive and aggressive soldiers Left cuneus Lef⬆ t cuneus Left Am ceny tr go da me ladi (bi all a ater my ag Lef l) d at la c entromedial amygdala Left mOFC ⬇ ⬆ ⬆ Impuls ⬇i ve Ang and er c ao gntr gres ols -io Ive mp ut gu rl o su ive p and aggressive group Ventral stria Rta iglht cerebellum Angular gyrus ⬆ ⬆ Proactive aggression Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group Lingual gyrus Lingual gyrus Revenge feelings Left superior occipital cortex Right OFC Left precuneus Left p ⬆ recuneus ⬆ Revenge feelings Parietal (supramarginal and angular gyrus) Right anterior cingulated cortex Phy siR ca ig l ht ag a gnter ressiio or n c ing R uilg aht te d ang cou rtex lar gyrus ⬆ ⬆ Impulsive and aggressive soldiers Impulsive and aggressive soldiers Left fusiform gyrus Left cuneus Left cuneus Left cuneus Lef Rit gc ht al c ca er riebe ne l clo urm tex Left calcarine cortex Left centromedial amygdala Impulsive and aggressive group Hippocampus (right) Frontal lobe (superior and middle frontal ⬆ ⬆ ⬆ Anger expression-out Right OFC ⬆ Revenge feelings Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings OFC (left) Left ang ⬆ ular region ⬇ ⬆ Physical aggression Lingual gyrus Left anterior cingulate Lef cortex t anter ior cingulate cortexLef t calcarine cortex Left calcarine cortex ⬆ ⬆ Impulsive and aggressiIve mp su ol ls di ive ers a nd aggressive soldiers Left R su ig p Lef ht er t ia o p ng rr o ecu u clc aineu rp g ity as r l u cs o rtex Left superior occipital cortex gyrus) Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Laboratory task ⬆ Physical aggression Left superior occipital c Lef ortex t su per Lef iot r co u cneu cipis t al cortex Left calcarine cortex Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Anterior insula OFC ⬇ Proactive aggression Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) ⬆ Destructive aggression Left anterior cingulate cortex Left calcarine cortex ⬆ Impulsive and aggressive soldiers Left super Lef iot r co u cneu cipis t a l cortex Left cuneus Laboratory task Ventral striatal Angular gyrus ⬆ ⬆ Proactive aggression Amygdala basolateral mOFC Ventral striatum Left precuneus Left sup Lef ert io p rr o ecu ccineu pitasl cortex Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Anterior insula ⬇ ⬆⬆ Ag gressive strategies (laboratory task) ⬆ Physical aggress ion Right anterior cingulate Rd igcht o r tex anter ior cingulated cortex Impulsive and aggressiIve mp su ol ls di ive ers a nd aggressive soldiers Physical aggression ⬆ ⬆ Superior parietal lobule Anterior cingulate cortex Left calcarine cortex Left Lef calc t a cr u ine neu cs o r tex Amygdala basolateral mOFC OFC (left) Left angular region ⬆ Physical aggression ⬇ ⬆ Aggressive strategies (laboratory task) Revenge feelings Left superior occipital c Lef ortex t su p Lef ert io p rr o ecu ccineu pitasl cortex Superior parietal lobule Right anterior cingulated cortex Impulsive and aggressive soldiers ⬆ Physical aggression Left calcarine R ci o g rht tex c erebellum Anterior insula OFC ⬇ Right OFC ⬆ ⬆ Revenge feelings ⬆ Destructive aggression Left superior occR ip ig itht al a cng ortex ula r gyrus Ventral striatum Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Anterior insula ⬆ ⬆ Physical aggression Anterior cingulate cortex Laboratory task Revenge feelings Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Right cerebellum Amygdala basolateral mOFC Right OFC ⬆ ⬆ Revenge feelings ⬇ ⬆ Aggressive strategies (laboratory task) Right angular gyrus Superior parietal lobule Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Laboratory task Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Amygdala basolateral mOFC ⬇ ⬆ Aggressive strategies (laboratory task) Superior parietal lobule Behav. Sci. 2019, 9, 11 12 of 19 Left mOFC Left amygdala ⬆ Before emotional induction task (violent offenders) Table 2. Cont. Left uncus/amygdala Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left amygdala ⬇ Before emotional induction task (violent offenders) Posterior insula ventromedial prefrontal cortex. Brain Structure (From) Brain Structure (To) Functional Connectivity Aggression Assessment Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Functional Right posterior insula Before emotional induction task (violent Brain structure (from) Brain structure (to) Aggression assessment Left amygdala ⬆ After emotional induction task (violent offenders) Left mOFC Left amygdala ventromedial prefrontal cortex. connectivity Right superior temporal gyrus offenders) Trait aggression Violent populations (no-self reported) Functional Left uncus/amygdala Before emotional induction task (violent Brain structure (from) Brain structure (to) Aggression assessment Left amygdala Caudate nucleus (right) Left mOFC ⬇ ⬆ Trait aggression Left mOFC Left amygdala Before emotional induction task (violent offenders) conne⬆ c tivity Amygdala (bilateral) Posterior insula offenders) vmPFC mPFC (right) Adjacent structures ⬇ ⬇ You ⬆ng Tr a vi ito a lent ggro es ff sender ion s Left uncus/amygdala Trait aggression Left amygdala Before emotional induction task (violent offenders) After emotional induction task (violent Nucleus centr Pa rlecu is sneu uper s i(o lef r (t) me dian raphe Posterior insula Left mOFC Left amygdala Left mOFC ⬇ ⬆ Trait aggression Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Amygnu dal ca leu (bi sl)a teral) offenders) Supramarginal gyrus (right) Adjacent structures ⬆ Young violent offenders Left mOFC Left amygdala After emotional induction task (violent offenders) Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: med⬇ ia l orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: vmPFC ⬇ ⬆ Trait aggression Right cerebe vmP llaF r C hem isphere BilateralLef sut pa ra my ma gr da gil na a l gyrus ⬇ ⬆ ⬆ VTr iola ent it ai g nm gres ates sio n Right posterior insula Right posterior insula After emotional induction task (violent Nucleus centralis superior (median raphe ventromedial prefrontal cortex. Left amygdala After emotional induction task (violent offenders) Left amygdala ⬆ Frontopolar cortex (Brodmann area 10) ⬇ ⬆ Trait aggression Bilatera Am l cer yg ebe dallla a r (r hem ight) i sphere InferiorBi frlo anta tera l lg O yr Fu C s (right) ⬆ ⬆V Tr io a lient t agig nm res astes ion Right superior temporal gyrus Right superior temporal gyrus offenders) nucleus) Angular gyrus (right) Cerebellar vermis Left OFC Func⬇ ti onal Violent inmates Violent populations (no-self reported) vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Brain structure (from) Brain structure (to) Aggression assessment Violent populations (no-self reported) Lef vmP t mOF FC C Posteri Lef or t cia ng my ug la da ted la cortex conne⬆ ⬆ c tivity Before emotional⬆ i ndu Traic t ta io gn grtes assk io (n v iolent offenders) Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Caudate nucleus (right) Amygdala (right) Inferior frontal gyrus (right) ⬆ ⬆ Trait aggression Lef Do t u rsnc ome us/di amy al P gF dC al a Trait Am aggy rg es da sio la n ba solateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group Caudate nucleus (right) mPFC (right) Adjacent structures Young violent offenders Left mOFC Ang Lef ula t ra g my yru gs da (r li ag ht) ⬆ Before emotional induction task (violent offenders) Table 2 Lef . Re t ast my ing g da funct la ional connectivity and its role in anger pronenes. mOFC: med⬇ ia l orbitofrontal cortex, OF Bef C: or o e emo rbitoti fro o na nt la il ndu cor ct tex ion , P taF sk C: (v pr ioefr lent o n oftfa ender l cort sex ) , vmPFC: Posterior insula Anger expression Left Lef fust ifmOF orm gy C rus ⬇ ⬆ Trait aggression mPFC (right) Precuneus (left) Adjacent structures Young violent offenders vmPFC Pos Lef tert io u rnc ciu ng s/u almy ated gdc ao la rtex ⬆ ⬆ Trait aggression Left Am ceny tr go da me ladi (bi all a ater my ag l) d ala ⬆ Impulsive and aggressive group ventromedial prefrontal cortex. Left amygdala ⬇ Before emotional induction task (violent offenders) Table Am 2 y .Lef gRe da t st lmOF ain (bi gl C a funct ter al)io nal connectivity and its rLef ole Lef t in a t my mOF an gg da e Cr l a pr onenes. mOFC: med⬇ ia l orbitofrontal cortex, OF Af C: ter o r em bito o ti fr oo na n⬇ lt a iAng n l du coer crti t ex o co nntr , ta Ps F ok lC: - ( o vi u pr o t lefr ent o o n ff tender al cor st)ex , vmPFC: Precuneus (left) Ling vmP ual F gC y rus ⬇ ⬇ ⬆ Trait aggression Supramarginal gyrus (right) Adjacent structures ⬆ Young violent offenders Do Po rs ster ome iodi r ia ns l P uF la C Parietal (suR pirg aht ma pro gs iter nali o ar nd ins au ng lau lar gyrus) Nucleus centralis superior (median raphe Left cuneus ventromedial prefrontal cortex. Right cerebellar hemisphere Left amygdala Violent inmates Func⬆ ti onal Anger expressio Lef n t mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Left amygdala ⬆ After emotional induction task (violent offenders) Supramarginal gyrus (right) FAdjacent rontopolarstr couct rtex ur (Br esodmann area 10) ⬇ Young violent ⬆ Tr of aifenders t aggression Brain structure (from) Brain structure (to) Aggression assessment Right superior temporal gyrus Hippocampus (right) Frontal lobe (superior and middle frontal ⬆ Anger expression-out Left anterinu or c clieu ngs u )l ate cortex Left calcarine cortex ⬆ ⬆ Impulsive and aggressive soldiers Bilateral cerebellar hemisphere Bilateral OFC conne⬇ c tivity Violent inmates Amygdala (bilateral) RightLef pot ster mOF iorC ins ula ⬇ Anger control-out Left mOFC Left amygdala Before emotional induction task (violent offenders) Func⬆ ti onal Table 2. Resting functional connectivity and its role in anger pronenes. mOFC: medial orbitofrontal cortex, OFC: orbitofrontal cortex, PFC: prefrontal cortex, vmPFC: Left amygdala ⬆ After emotional induction task (violent offenders) Right cer V ebellar iolent phemispher opulations (e no-self reported) Left Left amygdala superio gr y o ru cc s) ip ital cortex Violent inmates vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Brain structure (from) Brain structure (to) Aggression assessment Trait aggress C io er nebe llar vermis Left OFC ⬇ Violent inmates Right superior temporal gyrus Parietal (supramarginal and angular gyrus) Left uncus/amygdala connectivity ProactiveC aa gu gd res ate si nu on cleus (right) Left cuneus ventromedial prefrontal cortex. Am Lef yt ga da my lag (da riglht) a Inferior frontal gyrus (right) Before emotional induction task (violent offenders) ⬆ ⬇ ⬆ Trait aggression Left dorsolateral PFC Right Lef dor t smOF olater C a l PFC ⬆ ⬆V Tr io a lient t agig nm res astes ion Bilateral cer Viebellar olent poH hemispher pu ip la pto io cns amp (no u es -s (el rifg r ht) ep orted) Fronta Bilateral l lobe (su OFC perior and middle frontal ⬇ Violent ⬆ Ang inmates er expression-out Posterior insula Trait aggression Amygdala (bilateral) mPFC (right) Adjacent structures Young violent offenders Ventral striatal Lef Ang t u plra ecu r gneu yrus s ⬇ ⬆ Proactive aggression Angular gyrus (right) Amygdala basolateral (bilateral) Left dovmP rsolaF ter C al PFC ⬇ Impulsi ⬆ ve Tr a and it a a gg gg rr es es ss io ive n group Caudate nucleus (right) gyrus) ⬇ Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Left mOFC Left amygdala Functional After emotional induction task (violent offenders) Cerebellar vermis Left OFC Left mOFC ⬇ Violent ⬆ inmates Trait aggression Precuneus (left) Left mOFC LefLef t ca t lc aa my rine gda co la rtex ⬆ Before emotional induction task (violent offenders) Physical aB gra gries n ssit o vmP rn uc tur FC e (from) Poster Bra io in r c sitng ruc utlur ated e (tc o o )r tex Aggression assessment ⬆ ⬆ Trait aggression Amygdala (bilateral) Left fusiform gyrus P N ru oc alceu tive s c a entr ggra mP es lis s iF s ou C np (er rig io ht) r ( median raphe Adjacent structures ⬇ Young violent offenders connectivity Right posterior insula Left centromedial amygdala Frontopolar cortex vmP (Br FC o dmann area 10) ⬇ ⬆ Impulsi ⬆ ve Tr a and it a a gg gg rr es es ss io ive n group Supramarginal gyrus (right) Adjacent structures ⬇ You ⬆ng Tr a vi ito a lent ggro es ff sender ion s Left Lef sup t er unc iou r s o/c ac my ipig ta d la clo ar tex ⬆ Lef O t F aC my (lef gda t) la Lef Dot ra so ng me uldi ara r l eg PF io Cn ⬇ After emotiona ⬆l P indu hysic cti ao l n ag ta gr ses k ( svi ioo nl ent offenders) Left dorsolateral P PFC recu nuneu cleu ss ()l eft) Right dorsolateral LinguaPFC l gyrus Violent inmates Ventral striatal Angular gyrus Left amygdala ⬆ ⬇ Before emotiona ⬆ P l r io ndu actc ive tio a n gtg ar ses k ( sv io io nl ent offenders) Trait aggression Right superior temporal gyrus Nucleus centralis superior (median raphe Right cerebellar hemisphere Left amygdala Violent inmates Posterior insula ⬆ Anger expression ⬆ Physical aggression Frontopolar co Lef rtex t c ( u Br neu odma s nn area 10) ⬇ ⬆ Trait aggression Supramarg vmP inalF g C y rus (right) Bilater Adj al s au cent pra ma stru rg ctu ina res l g yrus ⬇ ⬆ Yo⬆ u ng Tr vi aio t la ent ggr oes ffender sion s Physical aggression Violent popul Anter ations io (r no ins -su ella f reported) Left OmOF FC C ⬇ ⬆ Trait aggression Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group nucleus) Left mOFC Left amygdala ⬆ Before emotional induction task (violent offenders) Bilateral cLef erebe t mOF llar hem C isphere Lef Bila t ter amy al g O da FC la ⬇ ⬇ After emotional iV ndu iolc ent tion inm tas ak tes (vi olent offenders) Amygdala (bilateral) ⬆ Destructive aggression Amygdala (bilateral) Left mOFC ⬇ ⬇ Anger control-out Left anterior cingulate cortex Left calcarine cortex ⬆ Impulsive and aggressive soldiers RightAm cery ebe gda lla la r hem (right) isp here Inferior Lef fro t nta amy l g gy da ru la s (right) ⬆ ⬆ ⬆V Tr io a lient t agig nm res astes ion OFC (left) Left angular region ⬇ ⬆ Physical aggression vmPFC ⬇ ⬆ Trait aggression Caudate nucleus (right) vmPFC Bilateral supramarginal gyrus ⬇ ⬆ Trait aggression Left uncus/amygdala Cerebellar vermis Right p Lef ost ter OiF oC r insula ⬇ Violent inmates Left fusiform Ventr gyr al sus triatum ParietalLef (su t p sru ap ma eriro gri n oa clc i ap nd itaa l ng cor u tex lar gyrus) BilateralLef cert ebe amy lla g rda hem la isphere AngBi ulla arter gy ar lu O s F (r C ig ht) ⬇ ⬇ Before emotional V indu iolent ctioin nm taa stes k (v iolent offenders) Left amygdala ⬆ After emotional induction task (violent offenders) Left centr N omedial ucleus centr amygdala Anter a mP lis F su C io p r (er riins g io ht) u r l(a me dian raphe Adjacent structures Impulsive and Y⬆ ⬆ oaggr u P Png hy hy s s essive vi i ic co a all lent a ag gg g gr or r fes es foup ender s si io on n s ⬆ ⬇ Amygdala (right) Inferior frontal gyrus (right) ⬆ ⬆ Trait aggression Posterior insula LefAnter t dorsio olr a ter insa u lla P FC Right Ri g su ht p er do io rO s ro F temp lC ater a olr a PlF g C y rus ⬆ Violent inmates Fronto Lingual p Anter olar c igyr o or r tex cus ing (Br ulo adma te conn rtex a rea 10) ⬇ ⬇ ⬆ Trait aggression Hippocampus (right) Frontal lobe (superior and middle frontal ⬆ ⬆ Anger expression-out Left cuneus Cerebe vmP llar F ver C mis PosteriorLef cing t O ul F aC ted cortex ⬆ ⬇ ⬆V Tr io a lient t agig nm res astes ion ⬆ Destructive aggression Precu nuneu cleu ss ()l eft) Angular gyrus (right) Left mOFC Left amygdala ⬇ After emotional induction task (violent offenders) Violent Am p yo gp da ulla at iba ons so ( la no ter -sa el l f ( bi rep later orted) al) Left dorsolateral PFC Impulsive and aggressive group Revenge feelings gyrus) ⬇ Left precuneus Left dorsolateral PFC Rig Do htr do some rsodi later al P aF l C PF C Violent inmates Left cuneus Ventral striatum ⬆ Supramarg vmP inalF g C y rus (right) Bilater Adj al s au cent pra ma stru rg ctu ina res l g yrus Yo⬆ u ng Tr vi aio t la ent ggr oes ffender sion s Right anterior cingulated cortex ⬇ ⬆ ⬆ Impulsive and aggressive soldiers Lef vmP t mOF FC C Posteri Lef or t cia ng my ug la da ted la cortex ⬆ ⬆ Before emotional⬆ i ndu Traic t ta io gn grtes assk io (n v iolent offenders) Right posterior insula Caud Anter ate nu ioc rl i eu nssu (lr ai ght) Left fusiform gyrus ⬆ Physical aggression Proactive aggression ⬆ Lef Rit gc ht al c ca er riebe ne l clo urm tex Anger Am exy p g rda ess lLef a io ba n t a so my later gda all a (bi lateral) Left dorsolateral PFC ⬆ After emI o mp tiona uls l iive ndu and cti o an g g ta res sks ( ivi veo g lent rouo pf fenders) Left anterior cingulate Left centr cortex omedial amygdala Left calcarine Anterior cortex cingulate cortex ⬇ Impulsive Iand mpuaggr lsive essive and agg soldiers ressive group Right cerR ebe ight lla O r hem FC isphere Left amygdala ⬆ Violent inmates Amygdala (right) Inferior frontal gyrus (right) ⬆ ⬆ ⬆ ⬆ ⬆ R Tr evenge ait agg free eslsiing ons Lef Do t u rsnc ome us/di amy al P gF dC al a Right superior temporal gyrus mPFC (right) Adj Li ang cen uta s ltr gu yc ru tu sr es ⬇ Young violent offenders Right angular gyrus Ventral striatal Left sup Ang erio u rl a or c c giy priu ta sl cortex ⬆ ⬆ Proactive aggression Left amygdala ⬇ Before emotional induction task (violent offenders) Amygdala (bilateral) Left mOFC ⬇ ⬇ Anger control-out Revenge feelings Left superiorLef occipital t fusiforcortex m gyrus Bilateral cerebellar hemisphere AngBi ulla arter gy ar lu O s F (r C ig ht) ⬇ Violent inmates Anger expression Posterior insula Violent Lef pot pcu en P la rtr tecu io ome ns neu (di no s a - l( s la ef el my f t) r ep gdo ar la ted) Impulsive and aggressive group Left cuneus ⬆ Physical aggress R io ig n ht OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Parietal (suprama Ling rgu in al a lg a ynd rusa ngular gyrus) Right cerebellum Cerebe vmP llar F ver C mis PosteriorLef cing t O ul F aC ted cortex ⬆ ⬇ ⬆V Tr io a lient t agig nm res astes ion AmyLef gda t lmOF a (bilC ater al) Lef Lef t a t my mOF gda Cl a ⬇ After emotiona⬇ l iAng nduer cti o co nntr tas ok l- ( o vi uo t l ent offenders) Caudate nucleus (right) Left cuneus ⬇ Lef Sup t r aa nter maR r ig o ig i rn ht ca i l ng O gF y uC r lu a te s ( c ri o g rht) tex Lef Adj t a cc aent lca rsitr ne uc ctu orr tex es ⬆ ⬆ Impu Y ls oiu ve ng a nd vio a lent ggres off sender ive sos ldi ers ⬆ ⬆ Revenge feelings Laboratory task OFC (left) Left angular region ⬆ Physical aggression Hippocampus (right) Frontal lobe (su Lef per t ic ou r neu and s middle frontal ⬆ ⬆ Anger expression-out Right angular gyrus Dorsomedial PFC Left dorsolateral PFC Right dorsolateral PFC ⬆ Violent inmates Right posterior insula mPFC (right) ParietLeft al (su pr p Adj recuneus ama acr en gitn s atr l u and ctur aes ng ular gyrus) ⬇ Young violent offenders Right cerebellar hemisphere Left sup Lef erit oa rmy occ gida pitla al cortex ⬆ Violent inmates Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Left amygdala ⬆ After emotiona ⬆l P indu hysic cti ao l n ag ta gr ses k ( svi ioo n lent o ff ender s ) Right anterior cingulated Left anterio cortex r cingulate cortex Left cal g cy ar ru ine s) cortex ImpulsiveImp and ulaggr sive a essive nd aggsoldiers ressive soldiers Anger expressio R ni ght OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ Impulsive and aggressive group Hip P Anter p recu ocaneu mp ior u isns s( l(u ef rla it) g ht) Fronta Rli g lo ht be ( susp uer per io O i ro F temp rC a ndo mi ralddl gyr e ufs r ontal ⬇ ⬆ Anger expression-out Left calcarine cortex ⬆ Bilateral cerebellar hemisphere Bi Lef later t cu alneu OFs C ⬇ Violent inmates Amygdala basolateral mOFC ⬆ Destructive aggression Proactive aggression Left superior occipital cortex Laboratory task Amygdala (bilateral) Left Lef fust ifmOF orm gy C r us ⬇ ⬆ Aggressi⬇ ve Ang stra er teg co ies ntr (o la l-bo ou rt ato ry task) Violent populations (no-self reported) gyrus) ⬇ Supramarginal gyrus (right) Left superiorAdj occipital acent str cortex uctures ⬆ Young violent offenders Cerebellar vermis LefLef t pr t ecu OFneu C s ⬇ Violent inmates Left centromedial amygdala Superior parietal lobule ⬆ Impulsive and aggressive group Ventral striatum Right anter Ventr ior a cli ng stru ia lta ate l d cortex Ang Lefu t lc au r neu gyrs u s ⬆ Impul⬆ s iP ve roa and cti ve ag a gg res grs es ive si o sn o ldiers Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Parietal (suprama Ling rgu in al a lg a ynd rusa ngular gyrus) ProactiveC aa gu gd Anter res ate si nu oin o c rl i eu nssu (lr ai ght) ⬆ ⬆ Physical aggression Right cerebellar hemisphere LefLef t ca t lc aa my rine gda co la rtex ⬆ Violent inmates Left dorsolateral PFC Right dorsolateral PFC Violent inmates Anterior cingulate cortex Physical aggression Left precuneus Amygdala basolateral mOFC Hippocampus (right) Frontal lobe (su Lef per t ic ou r neu and s middle frontal ⬆ ⬆ Anger expression-out V mP entr FC al (srtr ig ia ht) ta l Adj Ang acen ulta s rtr gu yc rtu usr es ⬇ Young violent offenders R Bi ig la ht ter aa nter l cer io ebe r cilng laru hem lated isp co her rtex e Left sup Bi erlia o ter r o aclc O ipF it C a l cortex ⬆ ⬆ ⬇ Impul⬆ s iP ve r V oa ia o nd clt ent i ve ag ia g nm g res ga rs es tes ive s i o sn o ldiers Amygdala basolateral (bilateral) Left dorsolateral PFC ⬇ ⬆ Ag Imp gres uslisve ive str and ateg ag ies gr es (lasbo ive ra g to ro ry u p ta sk) Revenge feelings Left calcarine cortex OFC (left) Left angular region ⬇ ⬆ Physical aggression Superiorg p ya ru riset ) al lobule Left anter Precu iorneu cing s u (llef ate t) cortex Left calcarine cortex ⬆ Impulsive and aggressive soldiers Physical aggC res ers ebe ionl lar vermis Left OFC ⬇ Violent inmates Left fusiform gyrus Left su Rp ig er ht io c rer oc ebe cip li lt u am l c ortex ⬆ Physical aggression Left centromedial amygdala ⬆ Impulsive and aggressive group ProactiSu ve p arg ag ma res rs g ii o n n a l gyrus (right) Left s Adj uper acient or o sc tr cu ip citu tar l es co rtex Young violent offenders Right OFC ⬆ ⬆ ⬆ Revenge feelings Left do Or F sC ol ( alter eft) a l PFC RiLef ght t do ang rs u olla arter reg ali o Pn F C ⬇ ⬆ PV hy io slient cal a inm ggra es tes si on Anterior insula Lingu Oa F lC g yrus ⬇ ⬆ Right angular gyrus ⬆ Destructive aggression Ventral striatal Ang Lefu t lc au r neu gyrs u s ⬆ ⬆ Proactive aggression Right cerebellar hemisphere Left amygdala ⬆ Violent inmates Amygdala basolateral (bilateral) Left dorsolateral PFC Impu⬆ ls i P ve hya snd ica la a gg gg res res si sve ion gr o u p Left cuneus Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Anterior insula OFC Ventral striatum ⬇ Left precuneus Physical aggression Bilateral cerebellar hemisphere Bilateral OFC ⬇ Violent inmates ⬆ Destructive aggression Left anter Anter ior ic oir ng ins ulu alte a cortex Lef Left t c fa uls cia fo rirne m gy corrtex us ⬆ Impuls ⬆i ve Phy and sic a alg a g g rg es res sive sio s no ldiers Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Laboratory task Left centromedial amygdala Anterior cingulate cortex ⬆ Impulsive and aggressive group Left calcarine cortex OFC (left) Left angular region ⬆ Physical aggression Cerebellar vermis Left OFC ⬇ ⬇ Violent inmates VLi entr nga ula s ltr giy ar tu us m Left superior occipital cortex Left superior temporal gyrus Anterior insula ⬆ ⬆ Aggress ⬆ i ve Phy str si acteg al a ies gg ( rles abo sio rn ato ry task) Revenge feelings ⬆ Left superior occipital cortex Left dorsolateral PFC Right dorsolateral PFC ⬆ ⬆ PV hy io slient cal a inm ggra es tes si on Anterior cingulate cortex Lef Left t c cu uneu neus s AmAnter ygdalia o r ba ins sou la la ter al OFC ⬇ mOFC Right cerebellum Amygdala basolateral (bilateral) Left dorsolateral PFC Imp⬆ u lDes sive tra u nd cti ve ag g ar ges gr ses ive si o gn ro up Reveng Lef e fe t e alnter ings io r cingulate cortex Left calcarine cortex ⬇ ⬇ ⬆ Ag Imp gres uls siive ve s atr nd ateg agig es res (ls aibo ver s ao to ldi ryer ta s sk) Right OFC Left precuneus ⬆ ⬆ ⬆ Revenge feelings Superior parietal lobule Right anterior cingulated cortex Right angular gyrus ⬆ Impulsive and aggressive soldiers Lef Ventr t fusa il f o sr tr m gy iatum ru s Left superior occipital cortex Lef Rit gc ht al c ca er riebe ne l clo urm tex Left cen Anter trome iodi r ia ns l a umy la gdala ⬆ Impu⬆ ls i P ve hy a snd ica la a gg gg res res si sve ion g roup Right OFC ⬆ Right OFC Right midoccipital cortex ⬆ ⬇ ⬆ R Re evenge venge f fee eel li ing ngs s AnterLi iong r ci u ng al u gly ar te us c ortex Left R su ig pht er Lef ia o ng t r co u u cl neu c airp g is ty ar lu cs o rtex Laboratory task R evenge feelings Left cuneus Left precuneus Right OFC Right midoccipital cortex ⬆ ⬇ Revenge feelings Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Left anterior cingulate cortex Lef Rit gc ht al c ca er riebe ne l clo urm tex ⬆ Impulsive and aggressive soldiers Left calcarine cortex Laboratory task Right OFC ⬆ ⬆ Revenge feelings Amygdala basolateral mOFC Lef Left t R s su u ig p pht er er i ia o o ng r r o o u c clc c ai ir p p g i it ty a ar l lu c cs o o r rtex tex Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) ⬇ ⬆ Aggressive strategies (laboratory task) Superior parietal lobule Right OFC Right m Lef ido t c cc uineu pitas l c ortex ⬆ ⬇ Revenge feelings Amygdala basolateral mOFC ⬆ Aggressive strategies (laboratory task) Laboratory task Left precuneus Superior parietal lobule Right anterior cingulated cortex ⬆ Impulsive and aggressive soldiers Left calcarine cortex Left superior temporal gyrus ⬆ ⬆ Aggressive strategies (laboratory task) Left superior occipital cortex Amygdala basolateral mOFC ⬇ ⬆ Aggressive strategies (laboratory task) Superior parietal lobule Behav. Sci. 2019, 9, 11 13 of 19 Although it appears that the diminished RSFC between the PFC and amygdala might be employed as a useful marker for proneness to violence, other brain networks should be considered in order to offer a broader understanding of the complex phenomenon of violence. Even though other limbic structures and their projections are involved in proneness to violence, we can conclude that high RSFC between the amygdala and the inferior frontal gyrus and left superior temporal gyrus was associated with high anger traits in several populations (normative and with mental disorders). Furthermore, the amygdala and the ACC maintained high RSFC with the fusiform and lingual gyrus, cuneus and precuneus calcarine cortex, and superior occipital cortex in impulsive and aggressive individuals. Recently, a research group demonstrated that violent individuals with schizophrenia presented hyperactivation of the ACC when perceiving negative images [51], especially in highly impulsive schizophrenic individuals [52]. This result coincides with the hypothesis that a large percentage of violent offenders present an attentional bias toward negative stimulus and/or a hostile attribution bias [53]. Moreover, other brain networks composed of the inferior frontal and temporal gyrus, ACC, and anterior insula are involved in voluntarily and actively sharing the emotional experience of other individuals (through intentional empathic processes), which is extremely important in behavioral regulation [8]. Thus, we sustain that this specific brain network facilitates the onset of violence due to attributing negative and hostile intentions to others, which is congruent with the scientific literature in this field. Regarding other limbic structures, the hippocampus and the anterior insula maintain anger expression facilitation projections with the supramarginal and angular gyrus, the superior and middle frontal gyrus, the ventral striatum, and the ACC. In this regard, the middle frontal gyrus plays an important role in hostile cognitive bias and angry rumination (or how often an individual tends to re-experience negative feelings) [54,55]. We also hypothesized that the heightened connectivity between the left/right orbitofrontal cortex (OFC) in violent inmates [49] may play a role in angry rumination. Furthermore, it was recently demonstrated that brainstem alterations (except its volume) seem to partly explain high irritability and proneness to react violently in males with autism [12,13]. Moreover, in two groups of violent inmates, the authors concluded that the PFC (mPFC and OFC) also maintained lower connectivity with adjacent areas and the cerebellar vermis, compared to non-violent males [41,42], with the cerebellum joined to the basal ganglia, and the supplementary motor area being important in impulse control [9]. Therefore, we might summarize that these RSFC patterns in a cognitive model where high anger traits that were linked to empathic alterations (i.e., perspective-taking disruptions, emotion-decoding deficits . . . ), hostile cognitive biases, and heightened anger rumination might lower the threshold for reacting with violence in ambiguous contexts, physically facilitating reactive violence. With regard to proactive violence, one study that was included in our review used self-reports to analyze the RSFC underlying this kind of violence. However, the authors did not compare reactive and proactive violence, and so it may be difficult to establish in this review whether there are differentiated neural pathways to each kind of violence [56]. Kolla, Dunlop, Meyer, and Downar [38] concluded that high RSFC between the ventral striatal and the angular gyrus was associated with high proactive violence strategies. Curiously, psychopaths (who usually but not always employ proactive violence) have been found to present structural abnormalities in the striatum—particularly increased volume—compared to non-psychopaths [57]. Moreover, it has been suggested that the angular gyrus belongs to the brain networks underlying moral reasoning [8]. Thus, these results offer information about which neural pathways underlie this kind of violence, which is defined as predatory, and is often characterized by premeditation and being cold-blooded [58]. Extending these findings, another study [42] revealed that revenge feelings were positively correlated with the RSFC between the OFC and the cerebellum, angular gyrus, and midoccipital cortex. Furthermore, recent research highlighted that psychopathic traits, as well as the risk of reoffending, maintained a positive relationship with the grey matter volume of the cerebellum [9]. If we try to explain why these neural pathways explain revenge feelings, we can assume that these neural pathways are associated with several processes that are important for revenge, such as the anticipation of consequences of violent behavior (good or bad) and reimagining different contexts to consume the desire for revenge [58]. Behav. Sci. 2019, 9, 11 14 of 19 Finally, one way to prevent these antisocial behaviors is to promote empathic abilities in violent populations through various psychological interventions. Thus, it has been hypothesized that there is an overlap between these brain regions that underlie violence and empathy, but the pattern of functional connectivity underlying each of them is inverse [57]. Regarding RSFC, a recent study demonstrated that individuals (men and women) with higher empathic abilities tend to present greater RSFC between the mPFC and the dorsal ACC, the precuneus, and the left superior temporal sulcus [58]. Conversely, low levels of empathy have been related to lower RSFC between the mPFC and ACC [30]. Moreover, it has been stated that high affective empathy tends to be related to stronger RSFC between the ventral anterior insula, OFC, amygdala, and perigenual anterior cingulated, and that high cognitive empathy is related to greater RSFC between the brainstem, superior temporal sulcus, and ventral anterior insula [59]. This statement is congruent with the assertion that there is a certain overlap between the brain structures that underlie violence and empathy, but they present inverse RSFC patterns. Thus, we might conclude that the brain RSFC in empathic abilities is more harmonious (i.e., positive RSFC between the PFC and the limbic system), than the pattern for violence (i.e., negative RSFC between PFC and the limbic system), which describes an imbalance in the brain functioning of individuals who tend to present proneness to violence. Based on the summarized results of our review and the brain RSFC underlying empathy, we proposed the facilitating and inhibiting brain networks for reactive violence described in Figure 2. Three important limitations of the studies carried out are the lack of a homogeneous population and their limited sample size. In fact, there is great diversity in the relevant variables, and not all of the studies reported or controlled the potential confounding effects of variables such as handedness, drug use, educational level, economic level, ethnicity, and psychopathology, among others. Furthermore, only a few studies included women, and so most of the research was conducted with males. Although small sample sizes kept us from properly estimating the differences between groups, most of the studies applied Bonferroni corrections for multiple comparisons. Moreover, they employed different anger trait questionnaires that measure different facets of anger (trait, physical, or verbal tendency to express anger, anger expression in general, proactive violence . . . ). Lastly, several of the articles that were included in our review based their conclusions on seed-based findings that are necessarily limited to a priori regions. In this regard, the absence of a finding in another region is very different from a study that may have used ICA. Hence, it is difficult to obtain unanimous conclusions about the association between RSFC and anger. In summary, the present review study confirmed that reduced frontal and limbic connectivity is a good correlate for several variables, such as trait anger and anger expression or control, which are important in violence proneness. Nevertheless, in order to offer a broader understanding of violence proneness, we need to contemplate other resting-state brain networks, including cortical regions (i.e., gyrus, parietal, temporal, ACC . . . ) and subcortical structures (i.e., hippocampus, insula, brain stem, cerebellum . . . ), in addition to the PFC and amygdala. Therefore, based on the studies summarized in this manuscript, along with those that analyzed the RSFC underlying empathic processes, we proposed a model to explain anger proneness to reactive violence (Figure 2). In sum, our review offered more insight into the importance of studying the brain RSFC underlying several important processes for violence proneness. It also reinforced the need to carry out further studies that analyze the importance of the RSFC using larger sample sizes, contemplating several populations, and employing a common anger assessment. Moreover, it would be necessary to check whether these RSFC could be considered temporally stable (as a ‘trait’), or whether they might change after interventions focused on promoting behavioral regulation and cognitive improvements. In fact, several studies demonstrated that after a focused intervention to promote cognitive and empathic changes in groups of intimate partner violence (IPV) perpetrators, these individuals improved specific cognitive and empathic abilities [60]. Thus, this research allows us to detect whether these changes correspond to specific brain network changes. Therefore, caution should be used in interpreting these results, in order to develop effective intervention programs to reduce proneness to violence. Behav. Sci. 2019, 9, 11 15 of 19 Figure 2. Proposed model of facilitating and inhibiting brain networks for reactive violence proneness. Behav. Sci. 2019, 9, 11 16 of 19 Author Contributions: Conceptualization: Á.R-M.; Methodology: Á.R-M. and M.G.; Writing-Original Draft Preparation: Á.R-M..; Writing-Review & Editing: M.L., E.G., L.M-B., Á.A-B., R.M-P., A.T-E. and L.M-A.; Funding Acquisition: Á.R-M. Funding: Project supported by a 2018 Leonardo Grant for Researchers and Cultural Creators, BBVA Foundation. The Foundation accepts no responsibility for the opinions, statements and contents included in the project and/or the results thereof, which are entirely the responsibility of the authors. Moreover, this work was supported by the Universitat of València (UV-INV-AE18-780697). Conflicts of Interest: The authors declare no conflict of interest. References 1. Glenn, A.L.; Raine, A. Neurocriminology: Implications for the punishment, prediction and prevention of criminal behaviour. Nat. Rev. Neurosci. 2014, 15, 54. [CrossRef] [PubMed] 2. Moya-Albiol, L.; Sariñana-González, S.; Vitoria-Estruch, S.; Romero-Martínez, Á. La neurocriminología como disciplina aplicada emergente. Vox Juris 2017, 33, 6. [CrossRef] 3. Nordstrom, B.R.; Gao, Y.; Glenn, A.L.; Peskin, M.; Rudo-Hutt, A.S.; Schug, R.A.; Yang, Y.; Raine, A. Neurocriminology. Adv. Genet. 2011, 75, 255–283. [PubMed] 4. Menon, R.S.; Gati, J.S.; Goodyear, B.G.; Luknowsky, D.C.; Thomas, C.G. Spatial and temporal resolution of functional magnetic resonance imaging. Biochem. Cell Biol. 1998, 76, 560–571. [CrossRef] [PubMed] 5. Zani, A.; Biella, G.; Proverbio, A.M. Brain imaging techniques: Invasiveness and spatial and temporal resolution. In The Cognitive Electrophysiology of Mind and Brain; Elsevier: Amsterdam, The Netherlands, 2003; pp. 417–422. 6. Hare, R.D.; Smith, A.M.; Forster, B.B.; MacKay, A.L.; Whittall, K.P.; Kiehl, K.A.; Smith, A.M.; Hare, R.D.; Liddle, P.F. Functional magnetic resonance imaging: The basics of blood-oxygen-level dependent (BOLD) imaging. Can. Assoc. Radiol. J. 1998, 49, 320–329. 7. Ekstrom, A. How and when the fMRI BOLD signal relates to underlying neural activity: The danger in dissociation. Brain Res. Rev. 2010, 62, 233–244. [CrossRef] [PubMed] 8. Raine, A.; Yang, Y. Neural foundations to moral reasoning and antisocial behavior. Soc. Cogn. Affect. Neurosci. 2006, 1, 203–213. [CrossRef] 9. Leutgeb, V.; Leitner, M.; Wabnegger, A.; Klug, D.; Scharmüller, W.; Zussner, T.; Schienle, A. Brain abnormalities in high-risk violent offenders and their association with psychopathic traits and criminal recidivism. Neuroscience 2015, 308, 194–201. [CrossRef] [PubMed] 10. Romero-Martínez, Á.; Moya-Albiol, L. Neuropsychology of perpetrators of domestic violence: The role of traumatic brain injury and alcohol abuse and/or dependence. Rev. Neurol. 2013, 57, 515–522. 11. Romero-Martínez, A.; Moya-Albiol, L. Neuropsychological impairments associated with the relation between cocaine abuse and violence: Neurological facilitation mechanisms. Adicciones 2015, 27, 64–74. [CrossRef] 12. Lundwall, R.A.; Stephenson, K.G.; Neeley-Tass, E.S.; Cox, J.C.; South, M.; Bigler, E.D.; Anderberg, E.; Prigge, M.D.; Hansen, B.D.; Lainhart, J.E.; et al. Relationship between brain stem volume and aggression in children diagnosed with autism spectrum disorder. Res. Autism Spectr. Disord. 2017, 34, 44–51. [CrossRef] [PubMed] 13. Glenn, A.L.; Raine, A.; Yaralian, P.S.; Yang, Y. Increased volume of the striatum in psychopathic individuals. Biol. Psychiatry 2010, 67, 52–58. [CrossRef] [PubMed] 14. Romero-Martínez, Á.; Moya-Albiol, L. ¿Facilitan los esteroides anabolizantes-androgénicos la expresión de la violencia? Rev. Esp. Drogodepend. 2015, 40, 12–26. 15. Siever, L.J. Neurobiology of aggression and violence. Am. J. Psychiatry 2008, 165, 429–442. [CrossRef] 16. Glenn, A.L.; Raine, A. Psychopathy and instrumental aggression: Evolutionary, neurobiological, and legal perspectives. Int. J. Law Psychiatry 2009, 32, 253–258. [CrossRef] 17. Raine, A.; Meloy, J.R.; Bihrle, S.; Stoddard, J.; LaCasse, L.; Buchsbaum, M.S. Reduced prefrontal and increased subcortical brain functioning assessed using positron emission tomography in predatory and affective murderers. Behav. Sci. Law 1998, 16, 319–332. [CrossRef] 18. Blair, R.J.R. The amygdala and ventromedial prefrontal cortex in morality and psychopathy. Trends Cogn. Sci. 2007, 11, 387–392. [CrossRef] [PubMed] Behav. Sci. 2019, 9, 11 17 of 19 19. Blair, R. Dysfunctions of medial and lateral orbitofrontal cortex in psychopathy. Ann. N. Y. Acad. Sci. 2007, 1121, 461–479. [CrossRef] 20. Lee, M.H.; Smyser, C.D.; Shimony, J.S. Resting-state fMRI: A review of methods and clinical applications. Am. J. Neuroradiol. 2013, 34, 1866–1872. [CrossRef] 21. Di, X.; Biswal, B.B. Dynamic brain functional connectivity modulated by resting-state networks. Brain Struct. Funct. 2015, 220, 37–46. [CrossRef] 22. Smitha, K.; Akhil Raja, K.; Arun, K.; Rajesh, P.; Thomas, B.; Kapilamoorthy, T.; Kesavadas, C. Resting state fMRI: A review on methods in resting state connectivity analysis and resting state networks. Neuroradiol. J. 2017, 30, 305–317. [CrossRef] [PubMed] 23. Binder, J.R.; Frost, J.A.; Hammeke, T.A.; Bellgowan, P.; Rao, S.M.; Cox, R.W. Conceptual processing during the conscious resting state: A functional MRI study. J. Cogn. Neurosci. 1999, 11, 80–93. [CrossRef] [PubMed] 24. Mazoyer, B.; Zago, L.; Mellet, E.; Bricogne, S.; Etard, O.; Houdé, O.; Crivello, F.; Joliot, M.; Petit, L.; Tzourio-Mazoyer, N. Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Res. Bull. 2001, 54, 287–298. [CrossRef] 25. Shulman, G.L.; Fiez, J.A.; Corbetta, M.; Buckner, R.L.; Miezin, F.M.; Raichle, M.E.; Petersen, S.E. Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 1997, 9, 648–663. [CrossRef] [PubMed] 26. Vatansever, D.; Menon, D.K.; Manktelow, A.E.; Sahakian, B.J.; Stamatakis, E.A. Default mode network connectivity during task execution. Neuroimage 2015, 122, 96–104. [CrossRef] [PubMed] 27. Greicius, M.D.; Krasnow, B.; Reiss, A.L.; Menon, V. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. USA 2003, 100, 253–258. [CrossRef] [PubMed] 28. Mars, R.B.; Neubert, F.; Noonan, M.P.; Sallet, J.; Toni, I.; Rushworth, M.F. On the relationship between the “default mode network” and the “social brain”. Front. Hum. Neurosci. 2012, 6, 189. [CrossRef] [PubMed] 29. Smith, V.; Mitchell, D.J.; Duncan, J. Role of the default mode network in cognitive transitions. bioRxiv 2018, 295683. [CrossRef] [PubMed] 30. Kim, S.J.; Kim, S.; Kim, H.E.; Han, K.; Jeong, B.; Kim, J.; Namkoong, K.; Kim, J.W. Altered Functional Connectivity of the Default Mode Network in Low-Empathy Subjects. Yonsei Med. J. 2017, 58, 1061–1065. [CrossRef] 31. Beaty, R.E.; Kaufman, S.B.; Benedek, M.; Jung, R.E.; Kenett, Y.N.; Jauk, E.; Neubauer, A.C.; Silvia, P.J. Personality and complex brain networks: The role of openness to experience in default network efficiency. Hum. Brain Mapp. 2016, 37, 773–779. [CrossRef] 32. Zhao, J.; Tomasi, D.; Wiers, C.E.; Shokri-Kojori, E.; Demiral, S.B.; ¸ Zhang, Y.; Volkow, N.D.; Wang, G. Correlation between Traits of Emotion-Based Impulsivity and Intrinsic Default-Mode Network Activity. Neural Plast. 2017, 2017, 9297621. [CrossRef] [PubMed] 33. Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med. 2009, 6, e1000100. [CrossRef] 34. Park, A.T.; Leonard, J.A.; Saxler, P.; Cyr, A.B.; Gabrieli, J.D.E.; Mackey, A.P. Amygdala-medial prefrontal connectivity relates to stress and mental health in early childhood. Soc. Cogn. Affect. Neurosci. 2018. [CrossRef] 35. Fulwiler, C.E.; King, J.A.; Zhang, N. Amygdala-orbitofrontal resting-state functional connectivity is associated with trait anger. Neuroreport 2012, 23, 606–610. [CrossRef] [PubMed] 36. Abram, S.V.; Wisner, K.M.; Grazioplene, R.G.; Krueger, R.F.; MacDonald, A.W.; DeYoung, C.G. Functional coherence of insula networks is associated with externalizing behavior. J. Abnorm. Psychol. 2015, 124, 1079–1091. [CrossRef] [PubMed] 37. Klasen, M.; Wolf, D.; Eisner, P.D.; Habel, U.; Repple, J.; Vernaleken, I.; Schlüter, T.; Eggermann, T.; Zerres, K.; Zepf, F.D.; et al. Neural networks underlying trait aggression depend on MAOA gene alleles. Brain Struct. Funct. 2018, 223, 873–881. [CrossRef] [PubMed] 38. Kolla, N.J.; Dunlop, K.; Meyer, J.H.; Downar, J. Corticostriatal connectivity in antisocial personality disorder by MAO-A genotype and its relationship to aggressive behavior. Int. J. Neuropsychopharmacol. 2018. [CrossRef] 39. Hoptman, M.J.; D’Angelo, D.; Catalano, D.; Mauro, C.J.; Shehzad, Z.E.; Kelly, A.M.; Castellanos, F.X.; Javitt, D.C.; Milham, M.P. Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophr. Bull. 2010, 36, 1020–1028. [CrossRef] [PubMed] Behav. Sci. 2019, 9, 11 18 of 19 40. Wagner, G.; Krause-Utz, A.; de la Cruz, F.; Schumann, A.; Schmahl, C.; Bar, K.J. Resting-state functional connectivity of neurotransmitter producing sites in female patients with borderline personality disorder. Prog. Neuropsychopharmacol. Biol. Psychiatry 2018, 83, 118–126. [CrossRef] 41. Hasler, R.; Preti, M.; Meskaldji, D.; Prados, J.; Adouan, W.; Rodriguez, C.; Toma, S.; Hiller, N.; Ismaili, T.; Hofmeister, J.; et al. Inter-hemispherical asymmetry in default-mode functional connectivity and BAIAP2 gene are associated with anger expression in ADHD adults. Psychiatry Res. Neuroimaging 2017, 269, 54–61. [CrossRef] 42. McGlade, E.; Rogowska, J.; Yurgelun-Todd, D. Sex differences in orbitofrontal connectivity in male and female veterans with TBI. Brain Imaging Behav. 2015, 9, 535–549. [CrossRef] [PubMed] 43. Goswami, R.; Dufort, P.; Tartaglia, M.C.; Green, R.E.; Crawley, A.; Tator, C.H.; Wennberg, R.; Mikulis, D.J.; Keightley, M.; Davis, K.D.; et al. Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions. Brain Struct. Funct. 2016, 221, 1911–1925. [CrossRef] [PubMed] 44. Dailey, N.S.; Smith, R.; Vanuk, J.R.; Raikes, A.C.; Killgore, W.D.S. Resting-state functional connectivity as a biomarker of aggression in mild traumatic brain injury. Neuroreport 2018, 29, 1413–1417. [CrossRef] [PubMed] 45. Gilam, G.; Maron-Katz, A.; Kliper, E.; Lin, T.; Fruchter, E.; Shamir, R.; Hendler, T.; et al. Tracing the Neural Carryover Effects of Interpersonal Anger on Resting-State fMRI in Men and Their Relation to Traumatic Stress Symptoms in a Subsample of Soldiers. Front. Behav. Neurosci. 2017, 11, 252. [CrossRef] [PubMed] 46. Buades-Rotger, M.; Engelke, C.; Kramer, U.M. Trait and state patterns of basolateral amygdala connectivity at rest are related to endogenous testosterone and aggression in healthy young women. Brain Imaging Behav. 2018. [CrossRef] [PubMed] 47. Siep, N.; Tonnaer, F.; van de Ven, V.; Arntz, A.; Raine, A.; Cima, M. Anger provocation increases limbic and decreases medial prefrontal cortex connectivity with the left amygdala in reactive aggressive violent offenders. Brain Imaging Behav. 2018, 1–13. [CrossRef] [PubMed] 48. Chen, C.; Zhou, J.; Liu, C.; Witt, K.; Zhang, Y.; Jing, B.; Li, C.; Wang, X.; Li, L. Regional homogeneity of resting-state brain abnormalities in violent juvenile offenders: A biomarker of brain immaturity? J. Neuropsychiatry Clin. Neurosci. 2015, 27, 27–32. [CrossRef] 49. Leutgeb, V.; Wabnegger, A.; Leitner, M.; Zussner, T.; Scharmüller, W.; Klug, D.; Schienle, A. Altered cerebellar-amygdala connectivity in violent offenders: A resting-state fMRI study. Neurosci. Lett. 2016, 610, 160–164. [CrossRef] 50. Varkevisser, T.; Gladwin, T.E.; Heesink, L.; van Honk, J.; Geuze, E. Resting-state functional connectivity in combat veterans suffering from impulsive aggression. Soc. Cogn. Affect. Neurosci. 2017, 12, 1881–1889. [CrossRef] 51. Tikasz, A.; Potvin, S.; Lungu, O.; Joyal, C.C.; Hodgins, S.; Mendrek, A.; Dumais, A. Anterior cingulate hyperactivations during negative emotion processing among men with schizophrenia and a history of violent behavior. Neuropsychiatr. Dis. Treat. 2016, 12, 1397–1410. 52. Hoptman, M.J.; Antonius, D.; Mauro, C.J.; Parker, E.M.; Javitt, D.C. Cortical thinning, functional connectivity, and mood-related impulsivity in schizophrenia: Relationship to aggressive attitudes and behavior. Am. J. Psychiatry 2014, 171, 939–948. [CrossRef] [PubMed] 53. Wang, Y.; Zhu, W.; Xiao, M.; Zhang, Q.; Zhao, Y.; Zhang, H.; et al. Hostile attribution bias mediates the relationship between structural variations in the left middle frontal gyrus and trait angry rumination. Front. Psychol. 2018, 9, 526. [CrossRef] [PubMed] 54. Anestis, M.D.; Anestis, J.C.; Selby, E.A.; Joiner, T.E. Anger rumination across forms of aggression. Personal. Individ. Differ. 2009, 46, 192–196. [CrossRef] 55. Wang, X.; Yang, L.; Yang, J.; Gao, L.; Zhao, F.; Xie, X.; Lei, L. Trait anger and aggression: A moderated mediation model of anger rumination and moral disengagement. Personal. Individ. Differ. 2018, 125, 44–49. [CrossRef] 56. Wrangham, R.W. Two types of aggression in human evolution. Proc. Natl. Acad. Sci. USA 2018, 115, 245–253. [CrossRef] [PubMed] 57. Moya-Albiol, L.; Herrero, N.; Bernal, M.C. The neural bases of empathy. Rev. Neurol. 2010, 50, 89–100. [PubMed] Behav. Sci. 2019, 9, 11 19 of 19 58. Takeuchi, H.; Taki, Y.; Nouchi, R.; Sekiguchi, A.; Hashizume, H.; Sassa, Y.; Kotozaki, Y.; Miyauchi, C.M.; Yokoyama, R.; Iizuka, K.; et al. Association between resting-state functional connectivity and empathizing/systemizing. Neuroimage 2014, 99, 312–322. [CrossRef] 59. Cox, C.L.; Uddin, L.Q.; Di Martino, A.; Castellanos, F.X.; Milham, M.P.; Kelly, C. The balance between feeling and knowing: Affective and cognitive empathy are reflected in the brain’s intrinsic functional dynamics. Soc. Cogn. Affect. Neurosci. 2011, 7, 727–737. [CrossRef] [PubMed] 60. Romero-Martínez, Á.; Lila, M.; Martínez, M.; Pedrón-Rico, V.; Moya-Albiol, L. Improvements in empathy and cognitive flexibility after court-mandated intervention program in intimate partner violence perpetrators: The role of alcohol abuse. Int. J. Environ. Res. Public Health 2016, 13, 394. [CrossRef] © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).

Journal

Behavioral SciencesMultidisciplinary Digital Publishing Institute

Published: Jan 15, 2019

There are no references for this article.