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Autistic Traits Moderate the Impact of Reward Learning on Social Behaviour

Autistic Traits Moderate the Impact of Reward Learning on Social Behaviour RESEARCH ARTICLE Autistic Traits Moderate the Impact of Reward Learning on Social Behaviour Maria Serena Panasiti, Ignazio Puzzo, and Bhismadev Chakrabarti A deficit in empathy has been suggested to underlie social behavioural atypicalities in autism. A parallel theoretical account proposes that reduced social motivation (i.e., low responsivity to social rewards) can account for the said atypicalities. Recent evidence suggests that autistic traits modulate the link between reward and proxy metrics related to empathy. Using an evaluative conditioning paradigm to associate high and low rewards with faces, a previous study has shown that individuals high in autistic traits show reduced spontaneous facial mimicry of faces associated with high vs. low reward. This observation raises the possibility that autistic traits modulate the magnitude of evaluative con- ditioning. To test this, we investigated (a) if autistic traits could modulate the ability to implicitly associate a reward value to a social stimulus (reward learning/conditioning, using the Implicit Association Task, IAT); (b) if the learned association could modulate participants’ prosocial behaviour (i.e., social reciprocity, measured using the cyberball task); (c) if the strength of this modulation was influenced by autistic traits. In 43 neurotypical participants, we found that autistic traits moderated the relationship of social reward learning on prosocial behaviour but not reward learning itself. This evidence suggests that while autistic traits do not directly influence social reward learning, they modulate the rela- V C tionship of social rewards with prosocial behaviour. Autism Res 2016, 9: 471–479. 2015 The Authors Autism Research published by Wiley Periodicals, Inc. on behalf of International Society for Autism Research Keywords: reward; autism; prosocial behaviour; empathy Introduction related to individual autistic traits, i.e., the higher the The social motivation hypothesis posits that atypical autistic traits, the lower the reward-driven enhance- social behaviour in autism spectrum condition (ASC) ment of spontaneous facial mimicry. In a similar could be caused by a failure to assign reward values to experiment using evaluative conditioning of hand social stimuli and interactions [Chevallier, Kohls, stimuli, individuals with high autistic traits were found Troiani, Brodkin, & Schultz, 2012; Dawson et al., 2004; to engage in less automatic mimicry for hands Dawson, Webb, & McPartland, 2005]. Several studies associated with high vs. low rewards [Haffey, Press, have reported an aberrant functioning of the brain’s O’Connell, & Chakrabarti, 2013]. Finally, autistic traits reward circuit in individuals with high autistic traits have been shown to modulate the connectivity and those with a clinical diagnosis of ASC. In some of between ventral striatum an inferior frontal gyrus in these experiments, a reduced response to social rewards response to high vs. low conditioned happy faces in comparison to nonsocial rewards was noted [Cox [Sims, Neufeld, Johnstone, & Chakrabarti, 2014]. To et al., 2015; Gossen et al., 2014; Schmitz et al., 2008; summarise, these studies have demonstrated how Scott-van Zeeland, Dapretto, Ghahremani, Poldrack, & autistic traits modulate a connection between the Bookheimer, 2010]. How such atypical ascription of reward value of social stimuli and the extent of reward value to social stimuli can lead to deficits in spontaneous/automatic mimicry they elicit. processes related to empathy has been demonstrated in However, a number of studies have also observed a series of recent studies. Sims, Van Reekum, Johnstone, atypical reward related response to nonsocial reward and Chakrabarti [2012] reported that spontaneous facial (i.e., money) as well in ASC [Dichter et al., 2012; Kohls mimicry towards happy faces was enhanced by reward et al., 2013]. Thus, it remains unclear whether the conditioning and that this enhancement was inversely observations reported above are due to impaired reward From the Centre for Integrative Neuroscience and Neurodynamics, School of Psychology & Clinical Language Sciences, University of Reading, Read- ing, United Kingdom (M.S.P., I.P., B.C.); Department of Psychology, Sapienza University of Rome, Rome, Italy (M.S.P.); IRCCS, Fondazione Santa Lucia, Rome, Italy (M.S.P.); Department of Psychology, University of Southampton, Southampton, United Kingdom (I.P.) This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Received April 07, 2015; accepted for publication July 11, 2015 Address for correspondence and reprints: Bhismadev Chakrabarti, Centre for Integrative Neuroscience and Neurodynamics, School of Psychology & Clinical Language Sciences, University of Reading, Reading RG6 6AL, United Kingdom. E-mail: b.chakrabarti@reading.ac.uk Published online 17 August 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1523 V 2015 The Authors Autism Research published by Wiley Periodicals, Inc. on behalf of International Society for Autism Research Autism Research 9: 471–479, 2016 471 INSAR learning itself, or to an impaired link between the Psychology and Clinical Language Sciences Research reward and empathy-related processes. Ethics Committee of the University of Reading. The purpose of this study was to disentangle these two possibilities. With this aim, we used an evaluative condi- Stimulus Materials tioning paradigm [adapted from Sims et al., 2012] to associate the faces of two actors with two different levels Stimuli in the conditioning phase consisted of static of reward. Subsequently, we tested whether this condi- images of four faces (two males, two females) with neu- tioning affected the participants’ prosocial behaviour tral expressions (Figure 1). All stimuli were selected during a virtual ball tossing game (Cyberball Task, CT, from the standardized Mindreading set [Baron-Cohen, [Williams, Cheung, & Choi, 2000]). The cyberball task Golan, Wheelwright, & Hill, 2004; available at www. has been used widely to measure social behaviour, pri- jkp.com/mindreading]. These stimuli show sufficient marily to test the impact of social exclusion. In this inter-rater reliability and external validity [Golan & study, we altered the paradigm to provide a proxy metric Baron-Cohen, 2006; Golan, Baron-Cohen, & Hill, for prosocial behaviour (for a similar but distinct altera- 2006], and have been used in previous research [Sims tion, see [Riem, Bakermans-Kranenburg, Huffmeijer, & et al., 2012, 2014]. van IJzendoorn, 2013]). Crucially, we used an Implicit Association Task (IAT) [Greenwald, Mcghee, Jordan, & Schwartz, 1998] to obtain a measure of the strength of Procedure conditioning. The IAT is typically used as a measure of automatically activated evaluations such as prejudices or Participants were seated in front of a computer screen stereotypes, but also as a measure of the association and introduced to the experimental procedure. After the between the conditioned and unconditioned stimuli conditioning phase participants performed the Cyberball after classical conditioning protocols [Baccus, Baldwin, & task and two versions of the IAT. The order of presenta- Packer, 2004; Dijksterhuis, 2004; Hughes et al., 2005; tion of the two versions of the IAT was counterbalanced Olson & Fazio, 2001]. We expected that the level of con- across participants. Importantly, the Cyberball task was ditioning (measured by the IAT) would predict the always administered directly after the conditioning strength of the prosocial behaviour in the CT. phase, in order to minimise extinction effects. Autistic traits are distributed continuously in the gen- Conditioning Phase eral population, where individuals with a clinical diag- nosis of ASC are more represented at the high end of An evaluative conditioning paradigm in the form of a the score distribution. The aetiology of autistic symp- card guessing game was used to associate faces with high toms has been shown to be comparable at extreme and low reward value (Figure 1). At the beginning of each ends of the score distribution [Robinson et al., 2011]. trial, participants were shown two cards, one face up and Specifically for this study, we predicted that autistic one face down. The task was to predict whether the face- traits might have a different influence on (a) the down card was of greater or smaller value than the first strength of conditioning (i.e., IAT) itself; and (b) the card by pressing one of two keys on a keyboard. Partici- extent to which the conditioning was translated into pants knew that correct/incorrect predictions were asso- prosocial behaviour. ciated with some monetary gain/loss (20 p). No money was won or lost if the cards were of equal value. After each response, an acoustic feedback indicating whether Participants participants had won, lost or drawn the round was deliv- ered for 1500 ms. The total amount of money won was Fifty adults (26 females) between 18 and 41 years of age shown after completion of the card game. In each trial, (M5 24.97; SD5 5.94) were recruited from the Univer- one of four emotionally neutral target faces was dis- sity of Reading campus area. All participants had played on the top part of the screen with the cards below. normal or corrected-to-normal vision and six were left- The reward value associated with each face was manipu- handed. None of the participants reported current neu- lated by adjusting the number of trials in which partici- rological or psychiatric disorders, or history of regular drug/substance use. A total of seven participants were pants won or lost money in the presence of this excluded from the analysis for: (a) technical problems particular face. In the Positive Conditioned (PosC) condi- tion, participants won 80% of the trials paired with the (n5 4); (b) being outliers for the implicit association associated face; in the Negative Conditioned (NegC) con- task (IAT) (n5 3). Thus, 43 participants were included in the analysis. All participants gave written informed dition, participants lost 80% of the trials in which the consent and were financially remunerated for their par- low rewarding face was presented. Two additional condi- ticipation. The study was approved by the School of tions in which participants won, lost or drawn the 33% 472 Panasiti et al./Reward, prosocial behaviour, and autistic traits INSAR Figure 1. Top panel: example of the four neutral faces that were associated with different reward values (80% win, 33% win, 33% loss, 80% loss) during the conditioning phase. The first face corresponds to the Positive Reward condition (PosC), and the fourth face to the Negative Reward condition (NegC). Bottom panel: example of two trials of the condition phase in which the participants had to predict whether the face down card would be of lower or higher value than the face up card. Following their key response, feedback was displayed. of the trials, were used to prevent participants from playing a computer-based ball tossing game with fic- detecting the underlying structure of the game. The tional characters. Participants were asked to click on the name of the player they wanted to throw the ball remaining trials in all conditions were “draw” trials (i.e., to and wait until the ball was tossed back to them. The the two cards were of the same value). The card game ball-tossing game lasted for 30 throws. The two fictional consisted of 120 randomized trials (30 trials per condi- characters were the PosC and NegC faces (Figure 2). In tion). The faces in the four conditions were counterbal- order to rule out the possibility that the Cyberball task anced across participants. To ensure that participants could itself influence the likeability of the faces, a recip- paid attention to the faces while playing the card game, rocation rate of 50% was programmed for each charac- they were told that during the test phase a simple mem- ter meaning that it was equally likely that each ory task involving these same faces would be performed. character would toss the ball to the experimental partic- ipant or the other character. Participants were Cyberball Game instructed not to pay attention to the tossing perform- After conditioning, participants were told that they ance but to try and mentally visualize the experience to needed to practise their mental visualization skills while their best ability (e.g., where were they playing? what Panasiti et al./Reward, prosocial behaviour, and autistic traits 473 INSAR Figure 2. Screenshot of a Cyberball game trial. Participants were presented with a cartoon at the bottom of the screen. Pictures of the two fictional characters are displayed next to their respective cartoons. Participants had to decide whether to throw the ball to the PosC or the NegC face by clicking on the correspondent name. lated with social preference and prosocial behaviour [Andari et al., 2010; Riem et al., 2013]. Conditioning-Implicit Association Task The cIAT was used to test whether participants implic- itly learned the association between wins and PosC face and between losses and NegC face. The cIAT consisted of a seven-block design [Nosek, Greenwald, & Banaji, 2005] involving five practice blocks and two test blocks. Participants were instructed to use a right (P) or left (Q) key to categorize possible pictures belonging to one of the four categories (i.e., wins, losses, PosC identity or NegC identity) that appeared in the centre of the screen. In three blocks or 20 trials each (1, 2 and 5) par- ticipants had to respond according to two categories: either PosC vs. NegC identity or wins vs. losses. In the remaining blocks participants had to sort the pictures into four categories. Specifically, in two blocks [i.e., the congruent blocks: 3 (20 trials) and 4 (40 trials) for ver- sion cIAT-A; 6 (20 trials) and 7 (40 trials) for version cIAT-B] participants had to use one key to identify pic- tures that belonged either to the PosC identity or wins and another key to identify pictures of either NegC identity or losses. In the other two blocks [i.e., the incongruent blocks: 6 (20 trials) and 7 (40 trials) for Figure 3. Correlation between RTs for the incongruent blocks version cIAT-A; 3 (20 trials) and 4 (40 trials) for version of the cIAT-A and the number of tosses directed towards the cIAT-B] participants had to use one key to identify pic- PosC face (r5 0.32, P5 0.041). The grey zone indicates 95% tures of PosC identity or losses and the other for NegC confidence intervals. identity or wins. Each participant was administered two versions of the cIAT, one in which the congruent blocks was the weather like?). The number of the throws to appeared before the incongruent (cIAT-A) and one with the PosC face and to the NegC face has been used as the opposite pattern (cIAT-B). The sequence of adminis- measures of induced prosocial behaviour. The perform- tration of the two versions was counterbalanced across ance on this task has already been shown to be corre- participants. 474 Panasiti et al./Reward, prosocial behaviour, and autistic traits INSAR Table 1. Means and Standard Errors for cIAT-A and cIAT-B Reaction Times Version Incongruent Congruent cIAT-A 747.93 (23.87) 626.24 (14.24) cIAT-B 648.01 (18.32) 660.01 (15.79) The stimuli consisted of the PosC and NegC pictures used during the conditioning paradigm, plus three pic- tures representing the concept of wins and three pic- tures representing the concept of loss (e.g., thumbs up and thumbs down, respectively). Trait Measures Participants filled the Autism Spectrum Quotient (AQ) score online after they took part in the study. Four par- ticipants did not complete the questionnaire, thus, they Figure 4. Autistic traits moderate the influence of condition- were excluded from the AQ analysis; thus the total ing (RTs for Incongruent trials of the cIAT-A) on prosocial number of participants for these analyses was 39. Scores behaviour (Tosses to PosC). The learned association is trans- on the AQ ranged between 5 and 31 (M5 20.02 ferred to a social preference only in individuals with low AQ. SD5 7.10). No participant scored above 32 on the full AQ, which has been found to be a reliable threshold with cIAT measure (Figure 3). Specifically, we found score for a potential clinical diagnosis of ASC. that slower RTs during the incongruent block of the cIAT-A (i.e., a stronger implicitly learned association between wins and PosC face), were associated with Results greater number of balls tossed to the PosC identity cIAT (r5 0.32, P5 0.041) (Figure 4). In order to control for the order of presentation, Influence of autistic traits on implicit learning reaction times (RTs) of the cIAT were submitted to a 2 3 2 3 2 analysis of variance (ANOVA) with Congru- To test whether autistic traits had an influence on ency (congruent vs. incongruent) and Version (cIAT-A implicit learning we used hierarchical mixed models. vs. cIAT-B) as within-subject factors and Order of Pre- Data analysis was performed using R [R Development sentation (A–B vs. B–A) as between-subject factor. This Core Team, 2013]. We performed a multilevel mixed ANOVA revealed a main effect of Congruency linear regression analysis (LMM or “mixed effects mod- F(1,41)5 18.59, P< 0.001 g 5 0.31 showing that RTs p els”; [Garson, 2013; Pinheiro & Bates, 2000], through for incongruent blocks were significantly higher than the package lme4 ver. 1.1-5 [Bates, Maechler, Bolker, & RTs for congruent blocks. The interaction between Walker, 2014]. Unlike traditional statistical methods, Congruency and Version showed to be significant LMM are suitable for analyzing hierarchical data struc- F(1,41)5 55.62, P< 0.001 g 5 0.57 revealing that p tures and accounting for the nonindependence of incongruent RTs were higher than congruent RTs only observations with correlated error by separately treating for the cIAT-A version (P< 0.001, Tukey’s corrected) the effects caused by the experimental manipulation (Table 1). The effect of the Order of presentation or its (fixed effects) and the ones that are not (random interactions were not significant (all Ps> 0.05). Thus, effects) [Pinheiro & Bates, 2000]. irrespective of the order of presentation (A–B vs. B–A), We considered the subject as a random factor (i.e., the cIAT-A version (where the congruent block was pre- the random intercept), and Congruency, AQ and Con- sented before the incongruent), was the only version gruency*AQ as fixed effects of our design. Only the that reflected the conditioning. Consequently, only the Congruency predictor showed to be significant cIAT-A version was used for the subsequent analysis. (P5 0.002, see Table 2). Cyberball Task and c-IAT Moderation Analysis There was no significant difference in the total number To test whether AQ traits could moderate the extent to of balls tossed to the PosC identity vs. the NegC iden- which the learned association of faces with rewards tity (t(42)5 0.87, P5 0.38). However, the number of (i.e., Incongruent RTs of cIAT-A) was transferred to pro- balls tossed to the PosC identity significantly correlated social behaviour (i.e., Tosses to PosC), moderated Panasiti et al./Reward, prosocial behaviour, and autistic traits 475 INSAR Table 2. cIAT Task Performance: Beta Values for the human hands [Haffey et al., 2013], cortical motor simu- Regression Model lation [Trilla Gros, Panasiti, & Chakrabarti, 2015] and frontostriatal connectivity [Sims et al., 2014]. Impor- Estimate SE t value P tantly, evaluative conditioning is thought to contribute Intercept 647.48 16.73 38.70 0.000 to several important phenomena in social psychology Congruency 47.91 16.08 2.97 0.002 like stigmatization, and ingroup favoritism effect AQ 21.20 2.26 20.53 0.594 Congruency*AQ 21.15 2.20 20.52 0.600 [Walther, Nagengast, & Trasselli, 2005] which respec- tively determine the way we categorize the social world and the way we favour some individuals (in-group multiple regression analysis was used. This analysis members) with respect to others (out-group members). allows to test if the effect of the independent variable Consistently, here we demonstrate that it also plays a (Conditioning: Incongruent RTs of cIAT-A) on the role in prosocial behaviour. dependent variable (Tosses to PosC) is moderated by a Second, while there was no evidence for any influ- moderator variable (AQ). The interaction is tested by ence of autistic traits on the reward learning perform- entering in the regression model the two predictor vari- ance, we found that autistic traits moderated the extent ables and the product of the two (the interaction term) to which reward learning for social stimuli was trans- [Aiken & West, 1991]. First of all, we checked for bivari- ferred to prosocial behaviour toward those faces. The ate outliers and no influential cases could be detected first of these results is consistent with previous reports in the analyses (all Cook’s distances< 1). that demonstrated comparable reward learning behav- The interaction term (AQ*Conditioning) was found iour in adults with and without Asperger Syndrome to be significant, showing that the extent to which the [Johnson, Yechiam, Murphy, Queller, & Stout, 2006] conditioning affected the dependent variable (the social and comparable fear learning in adolescents with ASC preference) was moderated by participants’ autistic [Bernier, Dawson, Panagiotides, & Webb, 2005]. In con- traits b520.0003, t522.14, P5 0.038. To further trast, there are reports suggesting impaired fear and understand this interaction we conducted a simple reward learning in ASC [Dawson, Meltzoff, Osterling, & slope analysis for high, average and low values of the Rinaldi, 1998; Dawson, Osterling, Rinaldi, Carver, & moderator. We found that when AQ traits were low McPartland, 2001; Solomon et al., 2014; Zalla, Sav, & there was a significant positive relationship between Leboyer, 2009]. The heterogeneity of the ASC samples level of conditioning and social preference, b5 0.0042, in terms of symptom severity, age, as well as the experi- 95% CI [0.0014, 0.0069], t5 3.06, P5 0.004; when the mental paradigms used in the studies above makes it AQ were on average or high the relationship failed to difficult to draw any generalized conclusion about learning in ASC. However, it has been suggested that reach the significance (respectively, b520.0020, 95% people with autism might have difficulties in reward CI [0.0000, 0.0039], t5 1.99, P5 0.053; b520.0002, learning when the reward feedback is not highly pre- 95% CI [20.0032, 20.0028], t520.16, P5 0.87). This dictable [Dawson et al., 2002]. Thus, it is possible that results show that only when AQ traits are low the the reinforcement scheduling (80%) we used was high learned conditioning is transferred to a social behaviour enough to allow the acquisition of the association irre- (Figure 4). spective of AQ traits. This possibility should be further Confounder Analysis explored in future studies. Crucially, we found that autistic traits moderated the To control for a possible confound due to the gender of extent to which the learnt reward value of the face participants, all analyses were rerun using gender as a translated to prosocial behaviour. Specifically, only par- covariate. All effects reported above remained unchanged. ticipants with low autistic traits showed to transform the learned association into prosocial behaviour. This Discussion result is in line with the previous findings that showed that autistic traits modulate frontostriatal connectivity The central aim of this study was to test if autistic traits [Sims et al., 2014], and mimicry [Sims et al., 2012] for influenced the extent of reward learning or/and the positive conditioned happy faces or human hands [Haf- extent to which the learned association translated into fey et al., 2013]. It should however be noted that the prosocial behaviour. We found three key results. First, samples for these studies, including the current one, are the strength of conditioning was correlated to the num- drawn largely from and around the university. Future ber of ball tosses directed to the PosC face. Evaluative studies should test the generalisability of these results conditioning has already been seen to influence differ- in general population samples with larger age ranges. ent proxy metrics related to empathy such as spontane- Interestingly, the effect of the evaluative condition- ous mimicry of happy faces [Sims et al., 2012], or ing paradigm was reflected in the cIAT-A, but not in 476 Panasiti et al./Reward, prosocial behaviour, and autistic traits INSAR the cIAT-B. It has already been documented [Greenwald [Haffey et al., 2013; Sims et al., 2012, 2014]. Two key et al., 1998; Nosek, Greenwald, & Banaji, 2005] that the insights emerge from this study that helps understand IAT version in which the congruent block is performed these previous results better. First, all the previous stud- before the incongruent (like the cIAT-A in our study) ies used a single measure to index both conditioning shows stronger effects than the other (the correspond- and social behaviour (e.g., mimicry). In this experi- ent to cIAT-B in our study). Consistent with this, a ment, we disentangle the two processes and test which functional magnetic resonance imaging (fMRI) study of these two processes is modulated by autistic traits. reported a stronger activation of the cingulate cortex in Second, we provided evidence that autistic traits moder- the congruent-before-incongruent version of the IAT ated the effect of reward conditioning not only on with respect to the incongruent-before-congruent one implicit measures like mimicry [as shown by Sims et al. [Chee, Sriram, Soon, & Lee, 2000] suggesting that the 2012], but also on more explicit prosocial behaviour as former version is the most sensitive to measure the measured with the cyberball task. That autistic traits implicit association. Notably, in our study the can influence the process of transferring an acquired congruent-before-incongruent (cIAT-A) version was reward value to prosocial behaviour is particularly rele- always more sensitive than the cIAT-B no matter which vant for current treatments (ABA, Applied Behaviour version was administrated first. Furthermore, the cIAT-B Analysis) and intervention programs for autism that use version did not show a significant advantage of the operant or classical conditioning principles to improve incongruent association with respect to the congruent social behaviour. Currently only a subset of patients one (i.e., faster reaction time for the incongruent than who undergo ABA therapy show a good outcome the congruent) but only a lack of difference in RTs [Howlin & Magiati, 2009; Matson & Smith, 2008], sug- between the two task conditions. These observations gesting that there are a large number of patients for are important to rule out the possibility of a confound whom a reward-conditioning based intervention does due to the order of presentation of the two versions of not necessarily lead to improvement of social skills. It is the cIAT task. Many studies have presented participants possible that deficits in this link between reward learn- with the IAT-A version only in order to make sure that ing and empathy-related behaviour can impact the gen- the individual variability in the performance was not eralization of the associations acquired during therapy driven by this congruent-before-incongruent effect to the everyday life. Future studies should test this [Asendorpf, Banse, & Mucke, 2002; Egloff & Schmukle, result directly in people with ASC and stratify sub- 2002; Perugini & Leone, 2009]. However, we chose to groups of patients who may/may not benefit from clas- administer both versions of the IAT to each of our par- sical conditioning based treatment regimes. ticipants, to check if the order of these tasks (cIAT-A and cIAT-B) had a significant effect on the observed Acknowledgments results. While we do not see any effect of order, we We are grateful to Prof. J. Douglas Saddy and all at the note that switching from the congruent to the incon- CINN for their input and support at all stages of this gruent association makes the task performance more study. MSP was supported by a fellowship from Sapi- difficult (i.e., the difference in reaction times between enza University of Rome. This work was supported by a congruent and incongruent trials is higher). This is not Medical Research Council UK New Investigator surprising, since the congruent trials are consistent Research Grant to BC (G1100359/1). with the direction of the original evaluative condition- ing effects of the card game. On the other hand, doing the incongruent trials first did not reverse the evalua- References tive conditioning effect, but made the difference in Aiken, L.S., & West, S.G. (1991). Multiple regression: testing reaction times between the two conditions statistically and interpreting interactions. Newbury Park, CA: Sage. insignificant. Since the aim of using the cIAT in this Andari, E., Duhamel, J., Zalla, T., Herbrecht, E., Leboyer, M., & study was to provide a proxy measure of the strength of Sirigu, A. (2010). Promoting social behavior with oxytocin conditioning, we used only the cIAT-A version, in light in high- functioning autism spectrum disorders. 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Cyberos- Scott-van Zeeland, A.A., Dapretto, M., Ghahremani, D.G., tracism: effects of being ignored over the Internet. Journal Poldrack, R.A., & Bookheimer, S.Y. (2010). Reward process- of Personality and Social Psychology, 79(5), 748–762. doi: ing in autism. Autism Research, 3(2), 53–67. doi:10.1002/ 10.1037//0022-3514.79.5.748 aur.122.Reward Zalla, T., Sav, A.-M., & Leboyer, M. (2009). Stimulus-reward Sims, T.B., Neufeld, J., Johnstone, T., & Chakrabarti, B. (2014). association and reversal learning in individuals with Autistic traits modulate frontostriatal connectivity during Asperger Syndrome. Research in Autism Spectrum Disor- processing of rewarding faces. Social Cognitive and Affec- ders, 3(4), 913–923. doi:10.1016/j.rasd.2009.03.004 Panasiti et al./Reward, prosocial behaviour, and autistic traits 479 INSAR http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Autism Research Wiley

Autistic Traits Moderate the Impact of Reward Learning on Social Behaviour

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Abstract

RESEARCH ARTICLE Autistic Traits Moderate the Impact of Reward Learning on Social Behaviour Maria Serena Panasiti, Ignazio Puzzo, and Bhismadev Chakrabarti A deficit in empathy has been suggested to underlie social behavioural atypicalities in autism. A parallel theoretical account proposes that reduced social motivation (i.e., low responsivity to social rewards) can account for the said atypicalities. Recent evidence suggests that autistic traits modulate the link between reward and proxy metrics related to empathy. Using an evaluative conditioning paradigm to associate high and low rewards with faces, a previous study has shown that individuals high in autistic traits show reduced spontaneous facial mimicry of faces associated with high vs. low reward. This observation raises the possibility that autistic traits modulate the magnitude of evaluative con- ditioning. To test this, we investigated (a) if autistic traits could modulate the ability to implicitly associate a reward value to a social stimulus (reward learning/conditioning, using the Implicit Association Task, IAT); (b) if the learned association could modulate participants’ prosocial behaviour (i.e., social reciprocity, measured using the cyberball task); (c) if the strength of this modulation was influenced by autistic traits. In 43 neurotypical participants, we found that autistic traits moderated the relationship of social reward learning on prosocial behaviour but not reward learning itself. This evidence suggests that while autistic traits do not directly influence social reward learning, they modulate the rela- V C tionship of social rewards with prosocial behaviour. Autism Res 2016, 9: 471–479. 2015 The Authors Autism Research published by Wiley Periodicals, Inc. on behalf of International Society for Autism Research Keywords: reward; autism; prosocial behaviour; empathy Introduction related to individual autistic traits, i.e., the higher the The social motivation hypothesis posits that atypical autistic traits, the lower the reward-driven enhance- social behaviour in autism spectrum condition (ASC) ment of spontaneous facial mimicry. In a similar could be caused by a failure to assign reward values to experiment using evaluative conditioning of hand social stimuli and interactions [Chevallier, Kohls, stimuli, individuals with high autistic traits were found Troiani, Brodkin, & Schultz, 2012; Dawson et al., 2004; to engage in less automatic mimicry for hands Dawson, Webb, & McPartland, 2005]. Several studies associated with high vs. low rewards [Haffey, Press, have reported an aberrant functioning of the brain’s O’Connell, & Chakrabarti, 2013]. Finally, autistic traits reward circuit in individuals with high autistic traits have been shown to modulate the connectivity and those with a clinical diagnosis of ASC. In some of between ventral striatum an inferior frontal gyrus in these experiments, a reduced response to social rewards response to high vs. low conditioned happy faces in comparison to nonsocial rewards was noted [Cox [Sims, Neufeld, Johnstone, & Chakrabarti, 2014]. To et al., 2015; Gossen et al., 2014; Schmitz et al., 2008; summarise, these studies have demonstrated how Scott-van Zeeland, Dapretto, Ghahremani, Poldrack, & autistic traits modulate a connection between the Bookheimer, 2010]. How such atypical ascription of reward value of social stimuli and the extent of reward value to social stimuli can lead to deficits in spontaneous/automatic mimicry they elicit. processes related to empathy has been demonstrated in However, a number of studies have also observed a series of recent studies. Sims, Van Reekum, Johnstone, atypical reward related response to nonsocial reward and Chakrabarti [2012] reported that spontaneous facial (i.e., money) as well in ASC [Dichter et al., 2012; Kohls mimicry towards happy faces was enhanced by reward et al., 2013]. Thus, it remains unclear whether the conditioning and that this enhancement was inversely observations reported above are due to impaired reward From the Centre for Integrative Neuroscience and Neurodynamics, School of Psychology & Clinical Language Sciences, University of Reading, Read- ing, United Kingdom (M.S.P., I.P., B.C.); Department of Psychology, Sapienza University of Rome, Rome, Italy (M.S.P.); IRCCS, Fondazione Santa Lucia, Rome, Italy (M.S.P.); Department of Psychology, University of Southampton, Southampton, United Kingdom (I.P.) This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Received April 07, 2015; accepted for publication July 11, 2015 Address for correspondence and reprints: Bhismadev Chakrabarti, Centre for Integrative Neuroscience and Neurodynamics, School of Psychology & Clinical Language Sciences, University of Reading, Reading RG6 6AL, United Kingdom. E-mail: b.chakrabarti@reading.ac.uk Published online 17 August 2015 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/aur.1523 V 2015 The Authors Autism Research published by Wiley Periodicals, Inc. on behalf of International Society for Autism Research Autism Research 9: 471–479, 2016 471 INSAR learning itself, or to an impaired link between the Psychology and Clinical Language Sciences Research reward and empathy-related processes. Ethics Committee of the University of Reading. The purpose of this study was to disentangle these two possibilities. With this aim, we used an evaluative condi- Stimulus Materials tioning paradigm [adapted from Sims et al., 2012] to associate the faces of two actors with two different levels Stimuli in the conditioning phase consisted of static of reward. Subsequently, we tested whether this condi- images of four faces (two males, two females) with neu- tioning affected the participants’ prosocial behaviour tral expressions (Figure 1). All stimuli were selected during a virtual ball tossing game (Cyberball Task, CT, from the standardized Mindreading set [Baron-Cohen, [Williams, Cheung, & Choi, 2000]). The cyberball task Golan, Wheelwright, & Hill, 2004; available at www. has been used widely to measure social behaviour, pri- jkp.com/mindreading]. These stimuli show sufficient marily to test the impact of social exclusion. In this inter-rater reliability and external validity [Golan & study, we altered the paradigm to provide a proxy metric Baron-Cohen, 2006; Golan, Baron-Cohen, & Hill, for prosocial behaviour (for a similar but distinct altera- 2006], and have been used in previous research [Sims tion, see [Riem, Bakermans-Kranenburg, Huffmeijer, & et al., 2012, 2014]. van IJzendoorn, 2013]). Crucially, we used an Implicit Association Task (IAT) [Greenwald, Mcghee, Jordan, & Schwartz, 1998] to obtain a measure of the strength of Procedure conditioning. The IAT is typically used as a measure of automatically activated evaluations such as prejudices or Participants were seated in front of a computer screen stereotypes, but also as a measure of the association and introduced to the experimental procedure. After the between the conditioned and unconditioned stimuli conditioning phase participants performed the Cyberball after classical conditioning protocols [Baccus, Baldwin, & task and two versions of the IAT. The order of presenta- Packer, 2004; Dijksterhuis, 2004; Hughes et al., 2005; tion of the two versions of the IAT was counterbalanced Olson & Fazio, 2001]. We expected that the level of con- across participants. Importantly, the Cyberball task was ditioning (measured by the IAT) would predict the always administered directly after the conditioning strength of the prosocial behaviour in the CT. phase, in order to minimise extinction effects. Autistic traits are distributed continuously in the gen- Conditioning Phase eral population, where individuals with a clinical diag- nosis of ASC are more represented at the high end of An evaluative conditioning paradigm in the form of a the score distribution. The aetiology of autistic symp- card guessing game was used to associate faces with high toms has been shown to be comparable at extreme and low reward value (Figure 1). At the beginning of each ends of the score distribution [Robinson et al., 2011]. trial, participants were shown two cards, one face up and Specifically for this study, we predicted that autistic one face down. The task was to predict whether the face- traits might have a different influence on (a) the down card was of greater or smaller value than the first strength of conditioning (i.e., IAT) itself; and (b) the card by pressing one of two keys on a keyboard. Partici- extent to which the conditioning was translated into pants knew that correct/incorrect predictions were asso- prosocial behaviour. ciated with some monetary gain/loss (20 p). No money was won or lost if the cards were of equal value. After each response, an acoustic feedback indicating whether Participants participants had won, lost or drawn the round was deliv- ered for 1500 ms. The total amount of money won was Fifty adults (26 females) between 18 and 41 years of age shown after completion of the card game. In each trial, (M5 24.97; SD5 5.94) were recruited from the Univer- one of four emotionally neutral target faces was dis- sity of Reading campus area. All participants had played on the top part of the screen with the cards below. normal or corrected-to-normal vision and six were left- The reward value associated with each face was manipu- handed. None of the participants reported current neu- lated by adjusting the number of trials in which partici- rological or psychiatric disorders, or history of regular drug/substance use. A total of seven participants were pants won or lost money in the presence of this excluded from the analysis for: (a) technical problems particular face. In the Positive Conditioned (PosC) condi- tion, participants won 80% of the trials paired with the (n5 4); (b) being outliers for the implicit association associated face; in the Negative Conditioned (NegC) con- task (IAT) (n5 3). Thus, 43 participants were included in the analysis. All participants gave written informed dition, participants lost 80% of the trials in which the consent and were financially remunerated for their par- low rewarding face was presented. Two additional condi- ticipation. The study was approved by the School of tions in which participants won, lost or drawn the 33% 472 Panasiti et al./Reward, prosocial behaviour, and autistic traits INSAR Figure 1. Top panel: example of the four neutral faces that were associated with different reward values (80% win, 33% win, 33% loss, 80% loss) during the conditioning phase. The first face corresponds to the Positive Reward condition (PosC), and the fourth face to the Negative Reward condition (NegC). Bottom panel: example of two trials of the condition phase in which the participants had to predict whether the face down card would be of lower or higher value than the face up card. Following their key response, feedback was displayed. of the trials, were used to prevent participants from playing a computer-based ball tossing game with fic- detecting the underlying structure of the game. The tional characters. Participants were asked to click on the name of the player they wanted to throw the ball remaining trials in all conditions were “draw” trials (i.e., to and wait until the ball was tossed back to them. The the two cards were of the same value). The card game ball-tossing game lasted for 30 throws. The two fictional consisted of 120 randomized trials (30 trials per condi- characters were the PosC and NegC faces (Figure 2). In tion). The faces in the four conditions were counterbal- order to rule out the possibility that the Cyberball task anced across participants. To ensure that participants could itself influence the likeability of the faces, a recip- paid attention to the faces while playing the card game, rocation rate of 50% was programmed for each charac- they were told that during the test phase a simple mem- ter meaning that it was equally likely that each ory task involving these same faces would be performed. character would toss the ball to the experimental partic- ipant or the other character. Participants were Cyberball Game instructed not to pay attention to the tossing perform- After conditioning, participants were told that they ance but to try and mentally visualize the experience to needed to practise their mental visualization skills while their best ability (e.g., where were they playing? what Panasiti et al./Reward, prosocial behaviour, and autistic traits 473 INSAR Figure 2. Screenshot of a Cyberball game trial. Participants were presented with a cartoon at the bottom of the screen. Pictures of the two fictional characters are displayed next to their respective cartoons. Participants had to decide whether to throw the ball to the PosC or the NegC face by clicking on the correspondent name. lated with social preference and prosocial behaviour [Andari et al., 2010; Riem et al., 2013]. Conditioning-Implicit Association Task The cIAT was used to test whether participants implic- itly learned the association between wins and PosC face and between losses and NegC face. The cIAT consisted of a seven-block design [Nosek, Greenwald, & Banaji, 2005] involving five practice blocks and two test blocks. Participants were instructed to use a right (P) or left (Q) key to categorize possible pictures belonging to one of the four categories (i.e., wins, losses, PosC identity or NegC identity) that appeared in the centre of the screen. In three blocks or 20 trials each (1, 2 and 5) par- ticipants had to respond according to two categories: either PosC vs. NegC identity or wins vs. losses. In the remaining blocks participants had to sort the pictures into four categories. Specifically, in two blocks [i.e., the congruent blocks: 3 (20 trials) and 4 (40 trials) for ver- sion cIAT-A; 6 (20 trials) and 7 (40 trials) for version cIAT-B] participants had to use one key to identify pic- tures that belonged either to the PosC identity or wins and another key to identify pictures of either NegC identity or losses. In the other two blocks [i.e., the incongruent blocks: 6 (20 trials) and 7 (40 trials) for Figure 3. Correlation between RTs for the incongruent blocks version cIAT-A; 3 (20 trials) and 4 (40 trials) for version of the cIAT-A and the number of tosses directed towards the cIAT-B] participants had to use one key to identify pic- PosC face (r5 0.32, P5 0.041). The grey zone indicates 95% tures of PosC identity or losses and the other for NegC confidence intervals. identity or wins. Each participant was administered two versions of the cIAT, one in which the congruent blocks was the weather like?). The number of the throws to appeared before the incongruent (cIAT-A) and one with the PosC face and to the NegC face has been used as the opposite pattern (cIAT-B). The sequence of adminis- measures of induced prosocial behaviour. The perform- tration of the two versions was counterbalanced across ance on this task has already been shown to be corre- participants. 474 Panasiti et al./Reward, prosocial behaviour, and autistic traits INSAR Table 1. Means and Standard Errors for cIAT-A and cIAT-B Reaction Times Version Incongruent Congruent cIAT-A 747.93 (23.87) 626.24 (14.24) cIAT-B 648.01 (18.32) 660.01 (15.79) The stimuli consisted of the PosC and NegC pictures used during the conditioning paradigm, plus three pic- tures representing the concept of wins and three pic- tures representing the concept of loss (e.g., thumbs up and thumbs down, respectively). Trait Measures Participants filled the Autism Spectrum Quotient (AQ) score online after they took part in the study. Four par- ticipants did not complete the questionnaire, thus, they Figure 4. Autistic traits moderate the influence of condition- were excluded from the AQ analysis; thus the total ing (RTs for Incongruent trials of the cIAT-A) on prosocial number of participants for these analyses was 39. Scores behaviour (Tosses to PosC). The learned association is trans- on the AQ ranged between 5 and 31 (M5 20.02 ferred to a social preference only in individuals with low AQ. SD5 7.10). No participant scored above 32 on the full AQ, which has been found to be a reliable threshold with cIAT measure (Figure 3). Specifically, we found score for a potential clinical diagnosis of ASC. that slower RTs during the incongruent block of the cIAT-A (i.e., a stronger implicitly learned association between wins and PosC face), were associated with Results greater number of balls tossed to the PosC identity cIAT (r5 0.32, P5 0.041) (Figure 4). In order to control for the order of presentation, Influence of autistic traits on implicit learning reaction times (RTs) of the cIAT were submitted to a 2 3 2 3 2 analysis of variance (ANOVA) with Congru- To test whether autistic traits had an influence on ency (congruent vs. incongruent) and Version (cIAT-A implicit learning we used hierarchical mixed models. vs. cIAT-B) as within-subject factors and Order of Pre- Data analysis was performed using R [R Development sentation (A–B vs. B–A) as between-subject factor. This Core Team, 2013]. We performed a multilevel mixed ANOVA revealed a main effect of Congruency linear regression analysis (LMM or “mixed effects mod- F(1,41)5 18.59, P< 0.001 g 5 0.31 showing that RTs p els”; [Garson, 2013; Pinheiro & Bates, 2000], through for incongruent blocks were significantly higher than the package lme4 ver. 1.1-5 [Bates, Maechler, Bolker, & RTs for congruent blocks. The interaction between Walker, 2014]. Unlike traditional statistical methods, Congruency and Version showed to be significant LMM are suitable for analyzing hierarchical data struc- F(1,41)5 55.62, P< 0.001 g 5 0.57 revealing that p tures and accounting for the nonindependence of incongruent RTs were higher than congruent RTs only observations with correlated error by separately treating for the cIAT-A version (P< 0.001, Tukey’s corrected) the effects caused by the experimental manipulation (Table 1). The effect of the Order of presentation or its (fixed effects) and the ones that are not (random interactions were not significant (all Ps> 0.05). Thus, effects) [Pinheiro & Bates, 2000]. irrespective of the order of presentation (A–B vs. B–A), We considered the subject as a random factor (i.e., the cIAT-A version (where the congruent block was pre- the random intercept), and Congruency, AQ and Con- sented before the incongruent), was the only version gruency*AQ as fixed effects of our design. Only the that reflected the conditioning. Consequently, only the Congruency predictor showed to be significant cIAT-A version was used for the subsequent analysis. (P5 0.002, see Table 2). Cyberball Task and c-IAT Moderation Analysis There was no significant difference in the total number To test whether AQ traits could moderate the extent to of balls tossed to the PosC identity vs. the NegC iden- which the learned association of faces with rewards tity (t(42)5 0.87, P5 0.38). However, the number of (i.e., Incongruent RTs of cIAT-A) was transferred to pro- balls tossed to the PosC identity significantly correlated social behaviour (i.e., Tosses to PosC), moderated Panasiti et al./Reward, prosocial behaviour, and autistic traits 475 INSAR Table 2. cIAT Task Performance: Beta Values for the human hands [Haffey et al., 2013], cortical motor simu- Regression Model lation [Trilla Gros, Panasiti, & Chakrabarti, 2015] and frontostriatal connectivity [Sims et al., 2014]. Impor- Estimate SE t value P tantly, evaluative conditioning is thought to contribute Intercept 647.48 16.73 38.70 0.000 to several important phenomena in social psychology Congruency 47.91 16.08 2.97 0.002 like stigmatization, and ingroup favoritism effect AQ 21.20 2.26 20.53 0.594 Congruency*AQ 21.15 2.20 20.52 0.600 [Walther, Nagengast, & Trasselli, 2005] which respec- tively determine the way we categorize the social world and the way we favour some individuals (in-group multiple regression analysis was used. This analysis members) with respect to others (out-group members). allows to test if the effect of the independent variable Consistently, here we demonstrate that it also plays a (Conditioning: Incongruent RTs of cIAT-A) on the role in prosocial behaviour. dependent variable (Tosses to PosC) is moderated by a Second, while there was no evidence for any influ- moderator variable (AQ). The interaction is tested by ence of autistic traits on the reward learning perform- entering in the regression model the two predictor vari- ance, we found that autistic traits moderated the extent ables and the product of the two (the interaction term) to which reward learning for social stimuli was trans- [Aiken & West, 1991]. First of all, we checked for bivari- ferred to prosocial behaviour toward those faces. The ate outliers and no influential cases could be detected first of these results is consistent with previous reports in the analyses (all Cook’s distances< 1). that demonstrated comparable reward learning behav- The interaction term (AQ*Conditioning) was found iour in adults with and without Asperger Syndrome to be significant, showing that the extent to which the [Johnson, Yechiam, Murphy, Queller, & Stout, 2006] conditioning affected the dependent variable (the social and comparable fear learning in adolescents with ASC preference) was moderated by participants’ autistic [Bernier, Dawson, Panagiotides, & Webb, 2005]. In con- traits b520.0003, t522.14, P5 0.038. To further trast, there are reports suggesting impaired fear and understand this interaction we conducted a simple reward learning in ASC [Dawson, Meltzoff, Osterling, & slope analysis for high, average and low values of the Rinaldi, 1998; Dawson, Osterling, Rinaldi, Carver, & moderator. We found that when AQ traits were low McPartland, 2001; Solomon et al., 2014; Zalla, Sav, & there was a significant positive relationship between Leboyer, 2009]. The heterogeneity of the ASC samples level of conditioning and social preference, b5 0.0042, in terms of symptom severity, age, as well as the experi- 95% CI [0.0014, 0.0069], t5 3.06, P5 0.004; when the mental paradigms used in the studies above makes it AQ were on average or high the relationship failed to difficult to draw any generalized conclusion about learning in ASC. However, it has been suggested that reach the significance (respectively, b520.0020, 95% people with autism might have difficulties in reward CI [0.0000, 0.0039], t5 1.99, P5 0.053; b520.0002, learning when the reward feedback is not highly pre- 95% CI [20.0032, 20.0028], t520.16, P5 0.87). This dictable [Dawson et al., 2002]. Thus, it is possible that results show that only when AQ traits are low the the reinforcement scheduling (80%) we used was high learned conditioning is transferred to a social behaviour enough to allow the acquisition of the association irre- (Figure 4). spective of AQ traits. This possibility should be further Confounder Analysis explored in future studies. Crucially, we found that autistic traits moderated the To control for a possible confound due to the gender of extent to which the learnt reward value of the face participants, all analyses were rerun using gender as a translated to prosocial behaviour. Specifically, only par- covariate. All effects reported above remained unchanged. ticipants with low autistic traits showed to transform the learned association into prosocial behaviour. This Discussion result is in line with the previous findings that showed that autistic traits modulate frontostriatal connectivity The central aim of this study was to test if autistic traits [Sims et al., 2014], and mimicry [Sims et al., 2012] for influenced the extent of reward learning or/and the positive conditioned happy faces or human hands [Haf- extent to which the learned association translated into fey et al., 2013]. It should however be noted that the prosocial behaviour. We found three key results. First, samples for these studies, including the current one, are the strength of conditioning was correlated to the num- drawn largely from and around the university. Future ber of ball tosses directed to the PosC face. Evaluative studies should test the generalisability of these results conditioning has already been seen to influence differ- in general population samples with larger age ranges. ent proxy metrics related to empathy such as spontane- Interestingly, the effect of the evaluative condition- ous mimicry of happy faces [Sims et al., 2012], or ing paradigm was reflected in the cIAT-A, but not in 476 Panasiti et al./Reward, prosocial behaviour, and autistic traits INSAR the cIAT-B. It has already been documented [Greenwald [Haffey et al., 2013; Sims et al., 2012, 2014]. Two key et al., 1998; Nosek, Greenwald, & Banaji, 2005] that the insights emerge from this study that helps understand IAT version in which the congruent block is performed these previous results better. First, all the previous stud- before the incongruent (like the cIAT-A in our study) ies used a single measure to index both conditioning shows stronger effects than the other (the correspond- and social behaviour (e.g., mimicry). In this experi- ent to cIAT-B in our study). Consistent with this, a ment, we disentangle the two processes and test which functional magnetic resonance imaging (fMRI) study of these two processes is modulated by autistic traits. reported a stronger activation of the cingulate cortex in Second, we provided evidence that autistic traits moder- the congruent-before-incongruent version of the IAT ated the effect of reward conditioning not only on with respect to the incongruent-before-congruent one implicit measures like mimicry [as shown by Sims et al. [Chee, Sriram, Soon, & Lee, 2000] suggesting that the 2012], but also on more explicit prosocial behaviour as former version is the most sensitive to measure the measured with the cyberball task. That autistic traits implicit association. Notably, in our study the can influence the process of transferring an acquired congruent-before-incongruent (cIAT-A) version was reward value to prosocial behaviour is particularly rele- always more sensitive than the cIAT-B no matter which vant for current treatments (ABA, Applied Behaviour version was administrated first. Furthermore, the cIAT-B Analysis) and intervention programs for autism that use version did not show a significant advantage of the operant or classical conditioning principles to improve incongruent association with respect to the congruent social behaviour. Currently only a subset of patients one (i.e., faster reaction time for the incongruent than who undergo ABA therapy show a good outcome the congruent) but only a lack of difference in RTs [Howlin & Magiati, 2009; Matson & Smith, 2008], sug- between the two task conditions. These observations gesting that there are a large number of patients for are important to rule out the possibility of a confound whom a reward-conditioning based intervention does due to the order of presentation of the two versions of not necessarily lead to improvement of social skills. It is the cIAT task. Many studies have presented participants possible that deficits in this link between reward learn- with the IAT-A version only in order to make sure that ing and empathy-related behaviour can impact the gen- the individual variability in the performance was not eralization of the associations acquired during therapy driven by this congruent-before-incongruent effect to the everyday life. Future studies should test this [Asendorpf, Banse, & Mucke, 2002; Egloff & Schmukle, result directly in people with ASC and stratify sub- 2002; Perugini & Leone, 2009]. However, we chose to groups of patients who may/may not benefit from clas- administer both versions of the IAT to each of our par- sical conditioning based treatment regimes. ticipants, to check if the order of these tasks (cIAT-A and cIAT-B) had a significant effect on the observed Acknowledgments results. While we do not see any effect of order, we We are grateful to Prof. J. Douglas Saddy and all at the note that switching from the congruent to the incon- CINN for their input and support at all stages of this gruent association makes the task performance more study. MSP was supported by a fellowship from Sapi- difficult (i.e., the difference in reaction times between enza University of Rome. This work was supported by a congruent and incongruent trials is higher). 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