Aging, Neuromuscular Decline, and the Change in Physiological and Behavioral Complexity of Upper-Limb Movement Dynamics

S. Morrison; K. M. Newell

doi:10.1155/2012/891218

Aging, Neuromuscular Decline, and the Change in Physiological and Behavioral Complexity of Upper-Limb Movement Dynamics

Morrison, S.;Newell, K. M. 2012-08-01 00:00:00 Hindawi Publishing Corporation Journal of Aging Research Volume 2012, Article ID 891218, 14 pages doi:10.1155/2012/891218 Review Article Aging, Neuromuscular Decline, and the Change in Physiological and Behavioral Complexity of Upper-Limb Movement Dynamics 1 2 S. Morrison and K. M. Newell School of Physical Therapy, Old Dominion University, Norfolk, VA 23529, USA Department of Kinesiology, Pennsylvania State University, State College, PA 16801, USA Correspondence should be addressed to S. Morrison, smorriso@odu.edu Received 16 March 2012; Revised 20 June 2012; Accepted 21 June 2012 Academic Editor: Wojtek Chodzko-Zajko Copyright © 2012 S. Morrison and K. M. Newell. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Aging is characterized by a general decline in physiological and behavioral function that has been widely interpreted within the context of the loss of complexity hypothesis. In this paper, we examine the relation between aging, neuromuscular function and physiological-behavioral complexity in the arm-hand eﬀector system, speciﬁcally with reference to physiological tremor and isometric force production. Experimental ﬁndings reveal that the adaptive behavioral consequences of the aging-related functional decline in neurophysiological processes are less pronounced in simple motor tasks which provides support for the proposition that the motor output is inﬂuenced by both extrinsic (e.g., task related) and intrinsic (e.g., coordination, weakness) factors. Moreover, the aging-related change in complexity can be bidirectional (increase or decrease) according to the inﬂuence of task constraints on the adaptation required of the intrinsic properties of the eﬀector system. 1. Introduction understanding of the direct eﬀect of aging very diﬃcult. In the last decade, the functional deﬁcits in aging have been A hallmark feature of aging and the onset of disease is investigated in the context of changes in the complexity and a general decline in physiological function and behavioral variability of the output of physiological system(s) [6, 12, 17, capacity [1]. This decline can be manifested in diﬀerent levels 18]. Speciﬁcally, the eﬀects of aging are viewed to result in a and functions of the biological system, including skeletal deﬁcit in physiological function that arises from a progressive muscle [2–4], cardiovascular processes [5, 6], central nervous “loss of complexity” of the physiological system. This deﬁcit system activity [7–9], and respiratory function [10], leading is postulated to arise from a decrease in the functioning to detriments in the behavioral capacity of activities of daily number of components or elements of a given system and/or living, including increased tremor, loss of balance control, a decrease in the interaction/coupling between components and a decline in walking ability [5, 6, 11–13]. Understanding [6, 12, 19]. the potential reason(s) for decline in function is a challenging There is not a single deﬁnition of a complex system undertaking, however, as there are numerous variables that but there is considerable agreement on the properties of can, either singularly or in combination, aﬀect physiological complex systems that include (a) many degrees of freedom function in the aging adult. For example, factors related to and interconnections between them and (b) the exhibition (but not limited to) biological, behavioral, socioeconomic, of spontaneous self-organization that is adaptive, nonlinear, nutritional, and/or lifestyle/career choices can all impact and dynamic in that it evolves in time, and where order evolves and dissolves without a controller [6, 12, 17, 20]. This on the general process of aging and have implications for theoretical backdrop has led to the experimental emphasis on physiological function [14–16]. the time- and frequency-domain structure of variability as The broad range of variables which can negatively opposed to the traditional approach of only considering the aﬀect function in the older adult makes a comprehensive 2 Journal of Aging Research dispersion properties of variables through the assumptions on the neuromuscular function of the arm-hand eﬀector about central tendency properties of distributions. Central complex given that, for any individual, an optimal degree of hand control is required to perform everyday ﬁne motor to this approach has been the use of nonlinear measures of physiological and behavioral time series [20–22]. These skills involving precision, grasping, and/or manipulating tools have revealed changes in complexity with healthy aging small objects [45]. One factor that can negatively impact general hand function is the degree of tremulous oscillations and/or age-related diseases like essential tremor, type 2 diabetes, and Parkinson’s disease [23–29]. observed during ﬁne motor tasks involving a degree of precision or force control. While these tremors are usually of small amplitude in young adults so that they rarely impact on hand control, these oscillations tend to increase with aging 2. Measuring Physiological Complexity and can severely inﬂuence the performance of ﬁne motor Given the inherent complexity of many physiological out- skills in older persons [46–50]. Here, we provide an overview puts, there has been a concerted eﬀort to develop appropriate of the major aging-related changes in physiological tremor nonlinear tools that can quantify the speciﬁc signal of interest and isometric force production. [30, 31]. To this end, a variety of measures have been developed and utilized to assess the dynamic properties of speciﬁc physiological signals. While a complete review of the 3. Functional and Structural Adaptations in diﬀering assessment tools is beyond the scope of this paper, Skeletal Muscle with Aging there are certain tools that have been commonly used to assess time series related to physiological processes (a more It is widely held that aging is associated with a general decline comprehensive review of the various measures, their use and in skeletal muscle function [3, 4, 51, 52]. One consequence of limitations, is provided by Stergiou and Decker [31, 32] this decline is that older people lose the capacity to generate and Bravi et al. [30]). A few of the analyses used include task-relevant and/or precise levels of muscle force in the time-frequency analysis, wavelet analysis, recurrence plots, context of action. This decline has been attributed to a loss poincare plots, measures of signal entropy (e.g., approximate of overall muscle function [4, 53] and has been associated entropy (ApEn), sample entropy (SampEn), and multiscale with changes in a number of mechanisms involving those entropy (MSE)), correlation dimension, detrended ﬂuctua- intrinsic to the muscle and through its neural interface. The tion analysis (DFA), and Lyapunov exponent [9, 32–43]. speciﬁc muscle changes found in the elderly include increases Each analytic technique has been designed to assess in average muscle force [54, 55], increased motor unit (MU) diﬀerent aspects of the signal and, in many cases, produces ﬁring rate variability [56], modulation of MU ﬁring rate a single outcome measure of the attractor dynamics [18, 30]. [57, 58], altered synchrony between MU recruitment and One advantage of using such measures to assess complexity MU ﬁring rate [51], and reduced sensitivity [59]. Structural is that they are typically dimensionless to the scale of changes in the muscle properties associated with aging systems and deﬁne conditions for dynamic similarities [44]. include a loss (atrophy) of fast twitch motor units and/or This allows for the comparison of signal complexity arising switch to slow twitch units (referred to as MU remodeling), from diﬀerent physiological systems and processes. However, altered MU size, and/or a decline in the number of alpha the reliance on any one measure can potentially give a motor neurons within the spinal cord [3, 51, 52, 56, 57, 60]. misleading representation of physiological complexity [19]. Consequences of these changes include an overall decrease in Therefore, it is recommended that the measurement of muscle cross-sectional area, a reduction in muscle mass, and physiological complexity be based on multiple measures of a decline in strength [4, 16, 61, 62]. system dynamics to increase the sensitivity of complexity Generally, the term sarcopenia has been used to describe assessment under both healthy and pathological conditions the loss of muscle mass and low muscle function (strength [18, 19, 30]. Despite the range of selected measures that or performance) associated with aging [63–65]. However, can be used to capture the dynamics of a given signal given the diverse range of age-related changes that occur and their limitations, as is highlighted in Figure 1,itis in muscle, which can span basic structural changes to clear that changes in the dynamics of signals are more functional changes impacting on the overall “muscle quality,” readily distinguished using nonlinear measures of pattern it has been proposed that the term dynapenia be used to complexity than the standard dispersion measures (SD, CV) denote those alterations in contractile properties and/or of a variable. neuromuscular function while sarcopenia be used to describe While there is growing evidence to support the view any age-related loss of muscle mass [15, 16, 66]. It has been that aging can be characterized by a general loss of physi- proposed that such a distinction would provide a framework ological and behavioral complexity, there are ﬁndings that for independently assessing those age-related factors which challenge the universal nature of the direction of change aﬀect muscle mass separately from those variables which in complexity with aging. The focus of this paper is to impact on neuromuscular function [15]. evaluate recent experimental ﬁndings as to the eﬀect aging The consequences of these age-related changes in func- has on neuromuscular function and its relation to changes tion and mass are that the capacity of skeletal muscle to in physiological and behavioral complexity. While examples produce force is compromised in the older adult [4, 62, for the eﬀects of aging on complexity will be provided for 67]. Indeed, the muscle responses of older adults are often anumberofdiﬀerent movement forms, the emphasis is characterized by prolonged contraction time, an increase Journal of Aging Research 3 Spatiotemporal features of gait Physiological tremor (Stride-to-stride variability) 2 −2 1.5 SD = 0.014 ms SD = 0.021 s 1.4 ApEn = 1.69 ApEn = 1.31 1.3 1.2 1.1 −1 −2 0.9 0123456789 10 0 100 200 300 400 500 600 700 800 900 1000 Time (s) Number of strides Parkinsonian tremor Postural (COP) motion during standing −2 SD = 0.83 ms SD = 1.1 mm 2 ApEn = 0.81 ApEn = 0.47 1 2 0 0 −1 −2 −2 −4 −3 −6 0123456789 10 0123456789 10 Time (s) Time (s) Alternating ﬁnger ﬂexion-extension Head acceleration during walking −2 SD = 1.7 ms −2 SD = 0.28 ms ApEn = 0.34 1.5 ApEn = 0.14 0.5 −4 −0.5 −8 0123456789 10 02468 10 Time (s) Time (s) Figure 1: Examples of various physiological signals related to tremor, postural motion, and gait. For each example, an index of the variation in regards to amplitude (SD) and for changes in the variation over the time course of the signal (using approximate entropy (ApEn) analysis) is shown. As this ﬁgure illustrates, the more semirhythmical and repeatable signals (e.g., head acceleration, ﬁnger motion) were characterized by lower ApEn values, which implies increased regularity (decreased complexity) of the movement signal. Furthermore, the signals that appear more noiselike and irregular (e.g., physiological tremor, stride-to-stride variability) have higher ApEn values implying greater complexity. In contrast, a standard measure of variation (SD) provides little distinction between signals, illustrating that such assessments of variability, by themselves, may be less useful in determining the inherent variability across diﬀerent movement signals. in the level of muscle activity for a given level of force 4. Physiological Tremor with Aging production, a decrease in the steadiness at which force can Physiological tremor is an intrinsic feature of the neuro- be produced, and a decline in overall muscle force producing muscular system reﬂecting the combined output of multi- capacity [4, 53, 57, 62, 68, 69]. It is clear that there are many ple oscillatory sources, including the mechanical resonant types of change that can occur with the normal aging process properties of the speciﬁc limb segment, cardiac mechan- and that ultimately aﬀect muscle function. ics, peripheral neural mechanisms (that include contribu- While aging has been associated with a number of tions from stretch reﬂexes), and central neural processes changes at the muscle level, the impact that these changes [45, 77]. As highlighted in Figure 2, the neural component have on overall movement performance is less well under- of a typical tremor signal has most power between 8– stood. Here we will focus on the relation between aging, 12 Hz and represents input from the basal ganglia, inferior neuromuscular function, and physiological-behavioral com- olive, deep cerebellar nuclei, thalamus, and, at the spinal plexity in the arm-hand eﬀector unit. Aging is associated cord, alpha motor neurons [45, 78]. One motor symptom with a general decline in hand function [46, 47, 70] and there linked with aging is an increase in the amplitude of the have been numerous investigations of the eﬀect of aging on 8–12 Hz component of physiological tremor, a behavioral physiological tremor [49, 50, 71, 72] and isometric force pro- consequence that can have negative implications for the duction [47, 57, 69]. This paper will address these changes ability of an individual to perform everyday ﬁne motor skills. in physiological tremor and isometric force control within This increase in tremor amplitude is believed to primarily the context of the loss of complexity hypothesis [6, 12, 19], derive from altered central neural output and reﬂects the which holds that the process of healthy aging is reﬂected by a more general decline in the functional capacity of the aging loss of complexity of the respective physiological system. This neuromuscular system [24, 48–50, 71, 72, 79]. hypothesis is, in part, derived from the broader construct of Given that physiological tremor is, in part, derived from dynamical disease [73, 74]and adynamical systemsapproach neuromuscular mechanisms, it is important to isolate the to aging [75, 76], in which physiological systems change due basis of any age-related changes and how they ﬁt within to aberrations in the temporal organization of the evolving the more general context of our understanding of muscle dynamics. adaptations with aging. In particular, it is important to Acceleration Acceleration Acceleration −2 (m.s ) −2 −2 (m.s ) (m.s ) Acceleration Stride time (s) AP COP (mm) −2 (m.s ) 4 Journal of Aging Research Finger only extended 1.5 Elderly 0.5 ApEn (young): 1.73 −0.5 0.8 −1 ApEn (elderly): 1.71 −1.5 0.6 1.5 Young 0.4 0.5 0.2 −0.5 −1 −1.5 0 5 10 15 20 25 30 Upper limb extended Frequency (Hz) 1.5 Elderly 0.5 ApEn (young): 1.68 0.8 ApEn (elderly): 1.51 −0.5 0.6 −1 −1.5 0.4 1.5 Young 0.2 0.5 −0.5 0 5 10 15 20 25 30 −1 Frequency (Hz) −1.5 0 5 10 15 20 25 30 Elderly Time (s) Young (a) (b) Figure 2: Representative postural acceleration (tremor) traces and power spectral proﬁles from the index ﬁnger of a healthy young and an elderly subject. Traces for each person are shown for conditions where (a) only the ﬁnger was extended (the rest of the upper limb was externally supported) and (b) when the entire upper arm was unsupported. Tremor traces were obtained from a single trial for the index ﬁnger of each individual. Measures of the degree of regularity (ApEn) of each tremor signal are also shown for each condition. For this analysis, higher values reﬂect greater complexity within the tremor time series. This example highlights that the age-related diﬀerences in ﬁnger tremor were only present under conditions where the entire arm was held against gravity. determine whether the increases in tremor amplitude are due older [41]). An alternative reason for the lack of aging-related to a speciﬁc decline in aspects of neuromuscular function change in tremor amplitude may be due to the conditions or associated with aging or to a diminished ability of the older tasks under which physiological tremor is assessed [81]. neuromuscular system to adapt to more challenging and/or In the majority of studies of age-tremor eﬀects, the physically demanding task demands. Furthermore, while a common practice has been to limit the assessment of these long standing view is that tremor tends to increase with oscillations to the tremor within a single (usually the ﬁnger) aging [49, 71, 72], this position has not been universally segment [41, 50, 79, 82]. In this situation, the more proximal supported by contemporary experimental research [48, 50]. segments are supported externally and do not contribute to For example, several studies have observed no age-related the oscillations seen distally. This experimental approach has increase in tremor amplitude and only subtle changes in the been employed in an eﬀort to tease out and isolate the spe- frequency of the 8–12 Hz neural tremor peak [41, 50, 80]. ciﬁc age-related adaptations in muscle physiology since the The signiﬁcance of these ﬁndings cannot be understated, action is restricted to a single segment, joint, and/or muscle because if the established changes in muscle physiology with group. However, while this approach allows a more direct aging do not translate to increases in physiological tremor, evaluation of the responses of an individual muscle, it has then the reasons for this dissociation remain to be fully been argued that this protocol is somewhat artiﬁcial, since elucidated. One suggestion as to why these studies have not there are few (if any) instances during everyday tasks where reported aging-related increase in physiological tremor is persons are required to perform a functional, goal-directed that the changes may only be detectable in the oldest-old action involving a single muscle and/or segment. Conversely, members of the population (e.g., for persons aged 80 years or under more real world conditions where individuals need −2 −2 −2 −2 Finger tremor (m·s ) Finger tremor (m·s ) Finger tremor (m·s ) Finger tremor (m·s ) −2 2 −2 2 Power (m·s ) Power (m·s ) Journal of Aging Research 5 to maintain the postural position of the entire limb, tremor oscillations (and hence the greatest potential for actually is rarely localized to a single segment. Consequently, while being able to reduce tremor) under conditions where the single joint movements provide insight as to the intrinsic entire arm must be coordinated and controlled, and not function of a speciﬁc, isolated muscle, it remains an open just the oscillations in a single distal segment. However, question as to what these ﬁndings reveal about the challenges optimal performance for task of this nature is not simply the aging neuromuscular system faces when performing the result of increasing muscle activity. Previous research has everyday actions involving multiple limb segments. demonstrated that when subjects actively cocontracted the An alternative experimental approach has been to exam- muscles of the arm to stiﬀen the arm, the degree of tremor ine postural tremor when the entire upper arm is unsup- at the ﬁnger increased signiﬁcantly [91]. Consequently, ported. This protocol provides a more realistic evaluation individuals need to ﬁnd a balance between required levels of of the tremor responses apparent in the performance of muscle activity to hold the limb against gravity while also everyday actions and insight into diﬀerences due to aging be able to achieve a necessary degree of control to ensure or disease [24, 83–86]. Tasks of this nature are inherently limb oscillations are kept to a minimum. It is likely that more challenging as there is now a more substantive strength a combination of a loss of muscle function and control requirement (e.g., to sustain limb position against gravity) (dynapenia) and muscle strength (sacropenia) in older adults and the need to adaptively compensate for the tremor in contributes signiﬁcantly to their increased tremor responses. multiple segments so they do not all sequentially magnify The age-related adaptive changes in the tremor tasks the oscillations at the more distal segments [72, 87]. Given show that the aging neuromuscular system is less able to that these tasks place increased demands for control on the adapt to the constraints of performing more challenging neuromotor system, it has been suggested that examining and/or physically demanding everyday tasks. Under these tremor from diﬀerent segments when the entire arm is situations, the capacity of the older person is stressed more unsupported may prove to be useful in discerning between and so the eﬀects of the changes at the individual muscle level neurologically healthy and clinical populations [83, 84, 86]. areaggregatedinsomeway thatisreﬂectedbyanincreasein Indeed, when this approach has been adopted, very clear physiological tremor. In comparison to single-joint tremor and notable diﬀerences in tremor are found as a function actions, older participants ﬁnd multiple segment tremor of normal aging [24, 72], Parkinson’s disease [27, 85, 86, tasks more demanding and so the increased tremor reﬂects 88, 89], and multiple sclerosis [83]. The typical pattern of the greater demands of holding the entire limb unsupported. results for this type of approach, as shown in Figures 2 Furthermore, the selective changes in EMG activity and and 3, is that older persons tend to exhibit greater hand the 8–12 Hz neural component of tremor for this type of and ﬁnger tremor coupled with increased muscle activity action support the position that increased neuromuscular in the forearm extensors when required to hold the entire drive generated in response to the more challenging task arm against gravity, compared to the EMG/tremor responses conditions is a contributing factor to revealing the aging- when only the ﬁnger is extended (the other segments were related increases in oscillatory outputs [51, 58]. supported externally). For the healthy elderly individuals, where tremor increases were reported, these were limited to the more distal segments only (e.g., the hand and ﬁnger), 5. Aging Changes in Physiological with no notable changes in the tremor from the forearm or Complexity of Tremor upper arm [24, 72]. Further, the age-related increases appear to be exacerbated when the older person performs the task in In addition to the challenges about the theoretical relevance a standing position compared to sitting [24], which supports of examining tremor in single joint versus multiple joint the view that relatively simple postural adjustments can also postural tasks, there is still, as noted previously, ambiguity inﬂuence tremor dynamics [87]. In both situations, however, as to whether tremor variability actually increases with the the tremor increase is primarily restricted to the neural 8– process of aging. In an eﬀort to provide greater insight as 12 Hz component and related muscle activity, indicating to the eﬀects of aging and/or disease on physiological and that changes in the output of those central neural processes behavioral processes, there has been an evaluation of the underlying tremor genesis were responsible for the aging- spatial/temporal pattern of the given tremor signal using related diﬀerences. measures of complexity [6, 12, 17]. These contrasting ﬁndings on single versus multiple This experimental approach to aging is based on the segment tremor invite the question as to the relative diﬃculty proposition that there is a deﬁcit in physiological function of movements performed about a single joint/segment. For that results from a progressive loss of complexity (i.e., comparison, the amplitude of physiological tremor observed dynamic variability) of the physiological system. This deﬁcit from the ﬁnger under single segment conditions has been has been phrased “loss of complexity” and is postulated to reported to be within the range of 1–3 mm [90], whereas, for arise from the general decrease in the number of elements of tasks requiring individuals to hold their entire arm up against a given system and/or decrease in the interaction/coupling gravity, oscillations of the order of 10–20 mm have been between control processes [6, 12, 19]. Given the complex reported for the index ﬁnger [24, 72]. If one considers the nature of the oscillatory output that is physiological tremor, task goal during these actions was to minimize limb postural it is natural that the theoretical perspective of complexity has motion (tremor), there is a higher degree of diﬃculty in been drawn on to examine the questions of the dynamics of controlling the muscles about an entire limb to minimize aging and disease with associated measures that are beyond 6 Journal of Aging Research Single joint action 0.1 0.02 0.08 0.015 0.06 0.01 0.04 0.005 0.02 Young Elderly 0 20406080 Multiple joint action 0.025 0.12 0.1 0.02 0.08 0.015 0.06 0.01 0.04 0.005 0.02 020 40 60 80 Young Elderly Frequency (Hz) Right arm Elderly Left arm Young (a) (b) Figure 3: Overall changes in mean RMS EMG activity from the extensor muscles of the forearm and examples of the power spectral proﬁles for a healthy young and elderly individual. Traces for each person are shown for conditions where only the ﬁnger was extended (the rest of the upper limb was externally supported) and when the entire upper arm was unsupported. As with Figure 2, any age-related diﬀerences in muscle activity were only seen under physically demanding task conditions. the standard dispersion indices of variability (e.g., standard greater repeatability or higher regularity in the time series. deviation). For example, using approximate entropy (ApEn) measures, Central to this approach has been the use of dynam- Sturman and associates [41] reported that there was an ical nonlinear measures of a physiological and behavioral increase in the time-dependent structure of physiological time series [20–22]. These tools have revealed changes in tremor with advanced age, despite there being no diﬀerences complexity with healthy aging and/or age-related diseases in tremor amplitude between the respective age groups. including essential tremor and Parkinson’s disease [23–27, Other studies have reported similar age-related diﬀerences 85]. One of the more commonly used measures has been in physiological tremor using the same analyses [24, 72, 81]. approximate entropy (ApEn), which has also been employed Interestingly, Hong et al. [81]conducted astudy to examine to assess complexity changes for a variety of physiological whether there were any age-related diﬀerences for tremor related signals including hormone secretion, isometric force in the frontal and transverse planes of motion. While no outputs, muscle activity, heart rate, postural motion, and gait aging-related eﬀects were observed for tremor in the vertical [37–40, 92, 93]. ApEn measures the probability that runs direction, changes in the tremor ApEn values for motion in of patterns that are close for m observations remain close the mediolateral axis between the young and older adults on the next (m + 1) incremental comparisons. This analysis were reported. produces a single value (range of 0–2) with higher values Together, these results support the view that aging and reﬂecting greater irregularity while lower values represent a disease can be reﬂected by a change in the time-dependent Mean extensor (ED) activity (mV) Mean extensor (ED) activity (mV) EMG power (mV) EMG power (mV) Journal of Aging Research 7 pattern or structure of the speciﬁc tremor signal output. This of freedom of the system. As we note later, a good example result, combined with the lack of any age diﬀerences in signal of this bi-directional hypothesis is in isometric force control regularity during the ﬁnger only conditions (see Figure 2), [94] where aging leads to a loss of complexity in the control is consistent with the proposition that the neuromuscular of a constant force level (where better performance is realized system of older individuals is typically not challenged enough by increasing the functional degrees of freedom) and an under the single segment condition to necessarily reveal increment in complexity in a sine wave force tacking (where any appreciable change in the system dynamics. The added better performance is realized by reducing the degrees of strength and coordination demands placed on the older freedom of the intrinsic dynamics). In this framework, the individual of having to hold their upper arm against gravity aging eﬀectismoregenerally alossofadaptationofthe and minimize tremor support the general premise of the loss functional degrees of freedom rather than universally loss of of complexity hypothesis. complexity. While it has been proposed that the general aging process is accompanied by a decrease in physiological complexity [6, 6. Isometric Force Production with Aging 12], it is important to note that, with regard to physiological tremor, the results of previous studies do not universally In grasping actions, individuals need to produce a certain support this perspective since there appears to be no consis- degree of isometric force in order to hold and/or manipulate tent diﬀerence in the structure of tremor signal under single agiven object [95, 96]. When producing this action, one segment conditions. The fact that several studies have either consequence is the production of small ﬂuctuations in the reported no change or a decline in physiological complexity force output, that have been referred to as reﬂecting force for tremor signal dynamics in older people lends support to steadiness or isometric force tremor [68, 97]. Healthy older the proposition that the hypothesis of a unidirectional nature individuals, in comparison to young adults, often exhibit of the loss of complexity hypotheses is too narrow [18]. A reduced control in force production, as quantiﬁed by an contrasting perspective is that there can be an increase or increase in these ﬂuctuations [59, 98, 99]. Interestingly, this decrease in a given signal’s pattern over time depending on age-related decline in force producing capacity has typically the interaction between components of the biological system been interpreted to reﬂect changes in motor unit (MU) and the inherent task dynamics [18]. control and sensorimotor function rather than in terms There is empirical evidence to support the position that of more macrothe constraintssuchasmusclestrength the aging-related changes in signal complexity can be bi- per se. The consequence of these changes is that elderly directional. In a recent study [85], it was reported that adults exhibit greater targeting error and isometric force the physiological tremor of older persons with Parkinson’s variability. As illustrated in Figure 4, both of these features disease (PD) exhibited a loss of complexity compared to the of variability tend to be more pronounced when producing lower maximum voluntary contraction (MVC) forces in healthy individuals of a similar age. However, the whole body comparison to higher maximal forces [57, 68, 100–102] motion (COP) of these same PD individuals was charac- and during force tracking tasks where a sinusoidal target is terized by an increase in signal complexity when compared displayed in comparison to a constant force target [103]. to the healthy elderly. This reciprocal pattern of change in Given the prevailing view that overall muscle strength these oscillatory signals within the same subjects supports declines with aging [3, 4, 13, 67], the ﬁnding that it is more the bi-directional perspective on changes in complexity diﬃcult to produce accurate levels of force output at lower with aging. Similarly, Hong et al. [81] reported that the MVC levels seems somewhat counterintuitive. If a decline in only signiﬁcant aging-related change in ﬁnger tremor was force producing capacity was to be the principal mitigating for side-to-side motion, while tremor in the vertical plane factor in the loss of muscle function in the older adult, then exhibited no diﬀerence between young, old (60–65 yrs), it would be predicted that producing higher forces would be and older-old (70–75 yrs) individuals. It would seem that a more diﬃcult. What these studies demonstrate is that any strong contributor to the observed age diﬀerences in signal age-related changes in movement ability are not merely the complexity is the older individual’s need to increase their product of alteration within the older muscle itself. Indeed, neuromuscular output so as to realize the speciﬁc demands similar to the ﬁndings shown previously for physiological of the task being performed [17]. tremor tasks, it would appear that the eﬀects of aging are The bi-directional hypothesis for the change of com- ampliﬁed under more challenging actions (e.g., sinusoidal plexity in the movement dynamics with aging is based on versus constant force production). the framework that the conﬂuence of organismic, envi- However, one important distinction can be made regard- ronmental, and task constraints channels the coordination ing the age-related changes in both physiological and and control of the system degrees of freedom [17, 18, 94]. isometric tremor. For physiological tremor, the argument In this view, the aging and loss of complexity eﬀect will often made is that the increased tremor amplitude reported hold when an increase in the dimension of behavior is where the entire arm is held against gravity primarily reﬂects required from the intrinsic dynamics to realize the task the diminished strength of the older person. However, the demands. And the bi-directional eﬀect of an increment same argument cannot be made for isometric force tremor, in complexity will be prevalent when the conﬂuence of since here the greatest diﬀerence is in performing tasks of constraints channels a reduction in the functional degrees lower force levels. Under isometric conditions, the suggested 8 Journal of Aging Research Sinusoidal force production Young Elderly 40% MVC ApEn = 0.33 ApEn = 0.37 20% MVC 4 4 ApEn = 0.35 ApEn = 0.44 3 3 2 2 1 1 0 2 4 6 8 10 12 14 16 18 20 0 2 4 6 8 10 12 14 16 18 20 Time (s) Time (s) (a) Constant force production Young Elderly 40% MVC 8 8 6 6 4 4 2 2 ApEn = 0.41 ApEn = 0.37 0 0 2 4 6 8 10 12 14 16 18 20 22 0 2 4 6 8 101214161820 Time (s) Time (s) 20% MVC 3 3 2.5 2.5 2 2 1.5 1.5 1 1 ApEn = 0.36 ApEn = 0.43 0.5 0.5 0 0 2 4 6 8 10 12 14 16 18 20 22 0 2 4 6 8 101214161820 Time (s) Time (s) Total force Target force (b) Figure 4: Representative examples of isometric force production trace (40% and 20% MVC) for a single young and older person. Examples are shown as individuals tracked a sinusoidal and constant target force. All traces were attained from a single subject during a single trial within each condition. Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Journal of Aging Research 9 reason(s) for the age-related diﬀerences in performance at in part be explained by the loss of complexity hypothesis lower force levels typically draws on the manner in which [6, 12, 19]. While the force signal for the older adult typically the neuromuscular system modulates MU recruitment and exhibits increased complexity under more challenging task ﬁring rate(s) in order to accurately grade force output [51, conditions, this pattern is not consistently prevalent across 94, 104]. Within this context, it would appear that the age- less challenging force levels or when diﬀerent eﬀectors are related variation in isometric force production dynamics utilized to perform the task [57, 69, 105, 107]. This invites the is driven more by task-speciﬁc control and coordination interpretation that any age diﬀerences in complexity of the constraints rather than the ability to produce (and sustain) signal output are more a function of the interaction between high absolute force levels [69]. extrinsic (task) and intrinsic (sacropenia, dynapenia) factors Further support for the notion that chronological age per rather than biological age being the single driving factor. se does not always drive the changes seen in force production Consequently, the pattern of changes in the biological signal comes from a study by Sosnoﬀ and Newell [105]. They are not consistent with the view that aging is reﬂected by reported that when diﬀerences in the maximal voluntary an overall loss of complexity [18]. Rather, the dynamics in contraction (MVC) force of young and older individuals the isometric force task reﬂect the conﬂuence of constraints were controlled for, there was no performance diﬀerence in including those of the aging individual, the task constraints, terms of the isometric force variability between age groups. and those of the environment. From these ﬁndings it was argued that chronological age is not, by itself, a suﬃcient indicator of the decline in isometric 8. Summary force control, but rather that the relative degree of weakness, irrespective of age, is a more appropriate biological index. With aging, there is a general decline in the physiological This result is of some importance since it would indicate function that is often manifested by speciﬁc changes in the that any age-related declines in isometric force control functional and structural properties of skeletal muscle [2– maybe more a function of inactivity, and so is modiﬁable 4, 51]. This decline in functional capacity of a given system by training, rather than simply the inevitable process of has been increasingly viewed within the context of the loss of decline associated with chronological aging. Indeed, sub- complexity hypothesis [6, 12]. While these changes alter the sequent studies have demonstrated that improvements in capacity of the individual muscle to respond, it is not clear isometric force control can be elicited with speciﬁc exercise to what degree these changes have a universal impact on an interventions [55, 106]. individual’s behavioral movement performance in physical activity. In the current paper, we examined the relation 7. Aging and Complexity in Isometric between aging, neuromuscular function, and physiological- Force Control behavioral complexity, speciﬁcally with reference to physi- As with the assessment of physiological tremor, additional ological tremor and isometric force production. These two insight as the any age-related changes in force production motor outputs were selected since they both derive primarily has been reported when measures of complexity have been from neuromuscular mechanisms, and the ability to control applied to the time series. In addition to the straightforward and minimize these oscillatory outputs is essential for the assessments of changes in force variability or targeting error, performance of many activities of daily living (ADL’s) which many studies have reported that the age-related diﬀerences contain a ﬁne motor skill component. The examination in force control extend to diﬀerences in the frequency of age-related changes in these motor processes would proﬁle of their force output, the pattern of regularity (based therefore provide greater understanding of the relation upon changes in ApEn and SampEn), and, where multiple between muscle adaptations and chronological age. A central digits are employed, changes in the coupling relations point to emerge is that there is no single pattern to the between these eﬀectors [100, 101, 103, 105, 107, 108]. When changes seen in physiological and isometric force tremor reviewing the resultant force signals, it is interesting to in older adults. Rather, it would appear that the speciﬁc compare the age-related diﬀerences in signal complexity alterations in the given motor outputs reﬂect a myriad of for isometric actions with the responses generated for extrinsic (task related) and intrinsic (muscle weakness, loss physiological tremor tasks. As shown in Figure 5, the force of coordination) constraints that are unlikely to be all the response from older adults is highlighted by an increase direct result of the process of aging. Consequently, it is in complexity (increased ApEn) in comparison to younger argued that any amplitude or structural changes observed individuals when performing more challenging isometric in physiological and force tremor amplitude reﬂect the task (e.g., 20% MVC, sinusoidal tracking). However, during diminished ability of the older neuromuscular system to more demanding postural tremor tasks (e.g., whole arm adapt to diﬀering task demands. extended, see Figure 2), the tremor output from the older Finally, the ﬁndings of this body of research do not adult was characterized by a decline in complexity (lower universally support the unidirectional interpretation that ApEn). aging is associated with a loss of physiological and behavioral It would appear that, as with the discussion of the complexity. Instead, the variable pattern of change in eﬀect of aging on physiological tremor, the changes in the complexity observed across both physiological and isometric isometric force producing ability of older person can only tremor forms in older adults supports the broader view 10 Journal of Aging Research Isometric force tremor 20% MVC, sinusoidal 20% MVC, constant 0.8 0.8 0.6 0.6 0.4 0.4 0.2 0.2 0 0 Young Elderly Young Elderly (a) Physiological tremor Multiple segment Single segment 1.8 1.8 1.6 1.6 1.4 1.4 1.2 1.2 Young Elderly Young Elderly Right ﬁnger Right ﬁnger Left ﬁnger Left ﬁnger (b) Figure 5: Age-related diﬀerences in approximate entropy (ApEn) measures for isometric force (a) and postural tremor (b) tasks. Changes in ApEn across the young and older individuals are shown for both the multiple segment and single-segment tremor tasks. In addition, the age-related diﬀerences during two isometric actions (20% MVC performed under sinusoidal tracking and constant force conditions) are also shown. This ﬁgure illustrates that the tremor signal tends to be less complex (lower ApEn) during multiple-segment tremor tasks and the 20% MVC constant force producing actions. However, for the 20% MVC sinusoidal funder isometric force task, the resultant signal for the older adults is more complex (higher ApEn) in comparison to the younger adults. Error bars represent one standard error of the mean. Mean ApEn Mean ApEn Mean ApEn Mean ApEn Journal of Aging Research 11 that age-related changes in physiological complexity are bi- Clinical Nutrition and Metabolic Care, vol. 13, no. 3, pp. 271– 276, 2010. directional, depending to a large degree on the constraints [16] D. J. Clark and R. A. Fielding, “Neuromuscular contributions to action. 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Publisher: Hindawi Publishing Corporation
Copyright: Copyright © 2012 S. Morrison and K. M. Newell. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
ISSN: 2090-2204
eISSN: 2090-2212
DOI: 10.1155/2012/891218
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Abstract

Hindawi Publishing Corporation Journal of Aging Research Volume 2012, Article ID 891218, 14 pages doi:10.1155/2012/891218 Review Article Aging, Neuromuscular Decline, and the Change in Physiological and Behavioral Complexity of Upper-Limb Movement Dynamics 1 2 S. Morrison and K. M. Newell School of Physical Therapy, Old Dominion University, Norfolk, VA 23529, USA Department of Kinesiology, Pennsylvania State University, State College, PA 16801, USA Correspondence should be addressed to S. Morrison, smorriso@odu.edu Received 16 March 2012; Revised 20 June 2012; Accepted 21 June 2012 Academic Editor: Wojtek Chodzko-Zajko Copyright © 2012 S. Morrison and K. M. Newell. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Aging is characterized by a general decline in physiological and behavioral function that has been widely interpreted within the context of the loss of complexity hypothesis. In this paper, we examine the relation between aging, neuromuscular function and physiological-behavioral complexity in the arm-hand eﬀector system, speciﬁcally with reference to physiological tremor and isometric force production. Experimental ﬁndings reveal that the adaptive behavioral consequences of the aging-related functional decline in neurophysiological processes are less pronounced in simple motor tasks which provides support for the proposition that the motor output is inﬂuenced by both extrinsic (e.g., task related) and intrinsic (e.g., coordination, weakness) factors. Moreover, the aging-related change in complexity can be bidirectional (increase or decrease) according to the inﬂuence of task constraints on the adaptation required of the intrinsic properties of the eﬀector system. 1. Introduction understanding of the direct eﬀect of aging very diﬃcult. In the last decade, the functional deﬁcits in aging have been A hallmark feature of aging and the onset of disease is investigated in the context of changes in the complexity and a general decline in physiological function and behavioral variability of the output of physiological system(s) [6, 12, 17, capacity [1]. This decline can be manifested in diﬀerent levels 18]. Speciﬁcally, the eﬀects of aging are viewed to result in a and functions of the biological system, including skeletal deﬁcit in physiological function that arises from a progressive muscle [2–4], cardiovascular processes [5, 6], central nervous “loss of complexity” of the physiological system. This deﬁcit system activity [7–9], and respiratory function [10], leading is postulated to arise from a decrease in the functioning to detriments in the behavioral capacity of activities of daily number of components or elements of a given system and/or living, including increased tremor, loss of balance control, a decrease in the interaction/coupling between components and a decline in walking ability [5, 6, 11–13]. Understanding [6, 12, 19]. the potential reason(s) for decline in function is a challenging There is not a single deﬁnition of a complex system undertaking, however, as there are numerous variables that but there is considerable agreement on the properties of can, either singularly or in combination, aﬀect physiological complex systems that include (a) many degrees of freedom function in the aging adult. For example, factors related to and interconnections between them and (b) the exhibition (but not limited to) biological, behavioral, socioeconomic, of spontaneous self-organization that is adaptive, nonlinear, nutritional, and/or lifestyle/career choices can all impact and dynamic in that it evolves in time, and where order evolves and dissolves without a controller [6, 12, 17, 20]. This on the general process of aging and have implications for theoretical backdrop has led to the experimental emphasis on physiological function [14–16]. the time- and frequency-domain structure of variability as The broad range of variables which can negatively opposed to the traditional approach of only considering the aﬀect function in the older adult makes a comprehensive 2 Journal of Aging Research dispersion properties of variables through the assumptions on the neuromuscular function of the arm-hand eﬀector about central tendency properties of distributions. Central complex given that, for any individual, an optimal degree of hand control is required to perform everyday ﬁne motor to this approach has been the use of nonlinear measures of physiological and behavioral time series [20–22]. These skills involving precision, grasping, and/or manipulating tools have revealed changes in complexity with healthy aging small objects [45]. One factor that can negatively impact general hand function is the degree of tremulous oscillations and/or age-related diseases like essential tremor, type 2 diabetes, and Parkinson’s disease [23–29]. observed during ﬁne motor tasks involving a degree of precision or force control. While these tremors are usually of small amplitude in young adults so that they rarely impact on hand control, these oscillations tend to increase with aging 2. Measuring Physiological Complexity and can severely inﬂuence the performance of ﬁne motor Given the inherent complexity of many physiological out- skills in older persons [46–50]. Here, we provide an overview puts, there has been a concerted eﬀort to develop appropriate of the major aging-related changes in physiological tremor nonlinear tools that can quantify the speciﬁc signal of interest and isometric force production. [30, 31]. To this end, a variety of measures have been developed and utilized to assess the dynamic properties of speciﬁc physiological signals. While a complete review of the 3. Functional and Structural Adaptations in diﬀering assessment tools is beyond the scope of this paper, Skeletal Muscle with Aging there are certain tools that have been commonly used to assess time series related to physiological processes (a more It is widely held that aging is associated with a general decline comprehensive review of the various measures, their use and in skeletal muscle function [3, 4, 51, 52]. One consequence of limitations, is provided by Stergiou and Decker [31, 32] this decline is that older people lose the capacity to generate and Bravi et al. [30]). A few of the analyses used include task-relevant and/or precise levels of muscle force in the time-frequency analysis, wavelet analysis, recurrence plots, context of action. This decline has been attributed to a loss poincare plots, measures of signal entropy (e.g., approximate of overall muscle function [4, 53] and has been associated entropy (ApEn), sample entropy (SampEn), and multiscale with changes in a number of mechanisms involving those entropy (MSE)), correlation dimension, detrended ﬂuctua- intrinsic to the muscle and through its neural interface. The tion analysis (DFA), and Lyapunov exponent [9, 32–43]. speciﬁc muscle changes found in the elderly include increases Each analytic technique has been designed to assess in average muscle force [54, 55], increased motor unit (MU) diﬀerent aspects of the signal and, in many cases, produces ﬁring rate variability [56], modulation of MU ﬁring rate a single outcome measure of the attractor dynamics [18, 30]. [57, 58], altered synchrony between MU recruitment and One advantage of using such measures to assess complexity MU ﬁring rate [51], and reduced sensitivity [59]. Structural is that they are typically dimensionless to the scale of changes in the muscle properties associated with aging systems and deﬁne conditions for dynamic similarities [44]. include a loss (atrophy) of fast twitch motor units and/or This allows for the comparison of signal complexity arising switch to slow twitch units (referred to as MU remodeling), from diﬀerent physiological systems and processes. However, altered MU size, and/or a decline in the number of alpha the reliance on any one measure can potentially give a motor neurons within the spinal cord [3, 51, 52, 56, 57, 60]. misleading representation of physiological complexity [19]. Consequences of these changes include an overall decrease in Therefore, it is recommended that the measurement of muscle cross-sectional area, a reduction in muscle mass, and physiological complexity be based on multiple measures of a decline in strength [4, 16, 61, 62]. system dynamics to increase the sensitivity of complexity Generally, the term sarcopenia has been used to describe assessment under both healthy and pathological conditions the loss of muscle mass and low muscle function (strength [18, 19, 30]. Despite the range of selected measures that or performance) associated with aging [63–65]. However, can be used to capture the dynamics of a given signal given the diverse range of age-related changes that occur and their limitations, as is highlighted in Figure 1,itis in muscle, which can span basic structural changes to clear that changes in the dynamics of signals are more functional changes impacting on the overall “muscle quality,” readily distinguished using nonlinear measures of pattern it has been proposed that the term dynapenia be used to complexity than the standard dispersion measures (SD, CV) denote those alterations in contractile properties and/or of a variable. neuromuscular function while sarcopenia be used to describe While there is growing evidence to support the view any age-related loss of muscle mass [15, 16, 66]. It has been that aging can be characterized by a general loss of physi- proposed that such a distinction would provide a framework ological and behavioral complexity, there are ﬁndings that for independently assessing those age-related factors which challenge the universal nature of the direction of change aﬀect muscle mass separately from those variables which in complexity with aging. The focus of this paper is to impact on neuromuscular function [15]. evaluate recent experimental ﬁndings as to the eﬀect aging The consequences of these age-related changes in func- has on neuromuscular function and its relation to changes tion and mass are that the capacity of skeletal muscle to in physiological and behavioral complexity. While examples produce force is compromised in the older adult [4, 62, for the eﬀects of aging on complexity will be provided for 67]. Indeed, the muscle responses of older adults are often anumberofdiﬀerent movement forms, the emphasis is characterized by prolonged contraction time, an increase Journal of Aging Research 3 Spatiotemporal features of gait Physiological tremor (Stride-to-stride variability) 2 −2 1.5 SD = 0.014 ms SD = 0.021 s 1.4 ApEn = 1.69 ApEn = 1.31 1.3 1.2 1.1 −1 −2 0.9 0123456789 10 0 100 200 300 400 500 600 700 800 900 1000 Time (s) Number of strides Parkinsonian tremor Postural (COP) motion during standing −2 SD = 0.83 ms SD = 1.1 mm 2 ApEn = 0.81 ApEn = 0.47 1 2 0 0 −1 −2 −2 −4 −3 −6 0123456789 10 0123456789 10 Time (s) Time (s) Alternating ﬁnger ﬂexion-extension Head acceleration during walking −2 SD = 1.7 ms −2 SD = 0.28 ms ApEn = 0.34 1.5 ApEn = 0.14 0.5 −4 −0.5 −8 0123456789 10 02468 10 Time (s) Time (s) Figure 1: Examples of various physiological signals related to tremor, postural motion, and gait. For each example, an index of the variation in regards to amplitude (SD) and for changes in the variation over the time course of the signal (using approximate entropy (ApEn) analysis) is shown. As this ﬁgure illustrates, the more semirhythmical and repeatable signals (e.g., head acceleration, ﬁnger motion) were characterized by lower ApEn values, which implies increased regularity (decreased complexity) of the movement signal. Furthermore, the signals that appear more noiselike and irregular (e.g., physiological tremor, stride-to-stride variability) have higher ApEn values implying greater complexity. In contrast, a standard measure of variation (SD) provides little distinction between signals, illustrating that such assessments of variability, by themselves, may be less useful in determining the inherent variability across diﬀerent movement signals. in the level of muscle activity for a given level of force 4. Physiological Tremor with Aging production, a decrease in the steadiness at which force can Physiological tremor is an intrinsic feature of the neuro- be produced, and a decline in overall muscle force producing muscular system reﬂecting the combined output of multi- capacity [4, 53, 57, 62, 68, 69]. It is clear that there are many ple oscillatory sources, including the mechanical resonant types of change that can occur with the normal aging process properties of the speciﬁc limb segment, cardiac mechan- and that ultimately aﬀect muscle function. ics, peripheral neural mechanisms (that include contribu- While aging has been associated with a number of tions from stretch reﬂexes), and central neural processes changes at the muscle level, the impact that these changes [45, 77]. As highlighted in Figure 2, the neural component have on overall movement performance is less well under- of a typical tremor signal has most power between 8– stood. Here we will focus on the relation between aging, 12 Hz and represents input from the basal ganglia, inferior neuromuscular function, and physiological-behavioral com- olive, deep cerebellar nuclei, thalamus, and, at the spinal plexity in the arm-hand eﬀector unit. Aging is associated cord, alpha motor neurons [45, 78]. One motor symptom with a general decline in hand function [46, 47, 70] and there linked with aging is an increase in the amplitude of the have been numerous investigations of the eﬀect of aging on 8–12 Hz component of physiological tremor, a behavioral physiological tremor [49, 50, 71, 72] and isometric force pro- consequence that can have negative implications for the duction [47, 57, 69]. This paper will address these changes ability of an individual to perform everyday ﬁne motor skills. in physiological tremor and isometric force control within This increase in tremor amplitude is believed to primarily the context of the loss of complexity hypothesis [6, 12, 19], derive from altered central neural output and reﬂects the which holds that the process of healthy aging is reﬂected by a more general decline in the functional capacity of the aging loss of complexity of the respective physiological system. This neuromuscular system [24, 48–50, 71, 72, 79]. hypothesis is, in part, derived from the broader construct of Given that physiological tremor is, in part, derived from dynamical disease [73, 74]and adynamical systemsapproach neuromuscular mechanisms, it is important to isolate the to aging [75, 76], in which physiological systems change due basis of any age-related changes and how they ﬁt within to aberrations in the temporal organization of the evolving the more general context of our understanding of muscle dynamics. adaptations with aging. In particular, it is important to Acceleration Acceleration Acceleration −2 (m.s ) −2 −2 (m.s ) (m.s ) Acceleration Stride time (s) AP COP (mm) −2 (m.s ) 4 Journal of Aging Research Finger only extended 1.5 Elderly 0.5 ApEn (young): 1.73 −0.5 0.8 −1 ApEn (elderly): 1.71 −1.5 0.6 1.5 Young 0.4 0.5 0.2 −0.5 −1 −1.5 0 5 10 15 20 25 30 Upper limb extended Frequency (Hz) 1.5 Elderly 0.5 ApEn (young): 1.68 0.8 ApEn (elderly): 1.51 −0.5 0.6 −1 −1.5 0.4 1.5 Young 0.2 0.5 −0.5 0 5 10 15 20 25 30 −1 Frequency (Hz) −1.5 0 5 10 15 20 25 30 Elderly Time (s) Young (a) (b) Figure 2: Representative postural acceleration (tremor) traces and power spectral proﬁles from the index ﬁnger of a healthy young and an elderly subject. Traces for each person are shown for conditions where (a) only the ﬁnger was extended (the rest of the upper limb was externally supported) and (b) when the entire upper arm was unsupported. Tremor traces were obtained from a single trial for the index ﬁnger of each individual. Measures of the degree of regularity (ApEn) of each tremor signal are also shown for each condition. For this analysis, higher values reﬂect greater complexity within the tremor time series. This example highlights that the age-related diﬀerences in ﬁnger tremor were only present under conditions where the entire arm was held against gravity. determine whether the increases in tremor amplitude are due older [41]). An alternative reason for the lack of aging-related to a speciﬁc decline in aspects of neuromuscular function change in tremor amplitude may be due to the conditions or associated with aging or to a diminished ability of the older tasks under which physiological tremor is assessed [81]. neuromuscular system to adapt to more challenging and/or In the majority of studies of age-tremor eﬀects, the physically demanding task demands. Furthermore, while a common practice has been to limit the assessment of these long standing view is that tremor tends to increase with oscillations to the tremor within a single (usually the ﬁnger) aging [49, 71, 72], this position has not been universally segment [41, 50, 79, 82]. In this situation, the more proximal supported by contemporary experimental research [48, 50]. segments are supported externally and do not contribute to For example, several studies have observed no age-related the oscillations seen distally. This experimental approach has increase in tremor amplitude and only subtle changes in the been employed in an eﬀort to tease out and isolate the spe- frequency of the 8–12 Hz neural tremor peak [41, 50, 80]. ciﬁc age-related adaptations in muscle physiology since the The signiﬁcance of these ﬁndings cannot be understated, action is restricted to a single segment, joint, and/or muscle because if the established changes in muscle physiology with group. However, while this approach allows a more direct aging do not translate to increases in physiological tremor, evaluation of the responses of an individual muscle, it has then the reasons for this dissociation remain to be fully been argued that this protocol is somewhat artiﬁcial, since elucidated. One suggestion as to why these studies have not there are few (if any) instances during everyday tasks where reported aging-related increase in physiological tremor is persons are required to perform a functional, goal-directed that the changes may only be detectable in the oldest-old action involving a single muscle and/or segment. Conversely, members of the population (e.g., for persons aged 80 years or under more real world conditions where individuals need −2 −2 −2 −2 Finger tremor (m·s ) Finger tremor (m·s ) Finger tremor (m·s ) Finger tremor (m·s ) −2 2 −2 2 Power (m·s ) Power (m·s ) Journal of Aging Research 5 to maintain the postural position of the entire limb, tremor oscillations (and hence the greatest potential for actually is rarely localized to a single segment. Consequently, while being able to reduce tremor) under conditions where the single joint movements provide insight as to the intrinsic entire arm must be coordinated and controlled, and not function of a speciﬁc, isolated muscle, it remains an open just the oscillations in a single distal segment. However, question as to what these ﬁndings reveal about the challenges optimal performance for task of this nature is not simply the aging neuromuscular system faces when performing the result of increasing muscle activity. Previous research has everyday actions involving multiple limb segments. demonstrated that when subjects actively cocontracted the An alternative experimental approach has been to exam- muscles of the arm to stiﬀen the arm, the degree of tremor ine postural tremor when the entire upper arm is unsup- at the ﬁnger increased signiﬁcantly [91]. Consequently, ported. This protocol provides a more realistic evaluation individuals need to ﬁnd a balance between required levels of of the tremor responses apparent in the performance of muscle activity to hold the limb against gravity while also everyday actions and insight into diﬀerences due to aging be able to achieve a necessary degree of control to ensure or disease [24, 83–86]. Tasks of this nature are inherently limb oscillations are kept to a minimum. It is likely that more challenging as there is now a more substantive strength a combination of a loss of muscle function and control requirement (e.g., to sustain limb position against gravity) (dynapenia) and muscle strength (sacropenia) in older adults and the need to adaptively compensate for the tremor in contributes signiﬁcantly to their increased tremor responses. multiple segments so they do not all sequentially magnify The age-related adaptive changes in the tremor tasks the oscillations at the more distal segments [72, 87]. Given show that the aging neuromuscular system is less able to that these tasks place increased demands for control on the adapt to the constraints of performing more challenging neuromotor system, it has been suggested that examining and/or physically demanding everyday tasks. Under these tremor from diﬀerent segments when the entire arm is situations, the capacity of the older person is stressed more unsupported may prove to be useful in discerning between and so the eﬀects of the changes at the individual muscle level neurologically healthy and clinical populations [83, 84, 86]. areaggregatedinsomeway thatisreﬂectedbyanincreasein Indeed, when this approach has been adopted, very clear physiological tremor. In comparison to single-joint tremor and notable diﬀerences in tremor are found as a function actions, older participants ﬁnd multiple segment tremor of normal aging [24, 72], Parkinson’s disease [27, 85, 86, tasks more demanding and so the increased tremor reﬂects 88, 89], and multiple sclerosis [83]. The typical pattern of the greater demands of holding the entire limb unsupported. results for this type of approach, as shown in Figures 2 Furthermore, the selective changes in EMG activity and and 3, is that older persons tend to exhibit greater hand the 8–12 Hz neural component of tremor for this type of and ﬁnger tremor coupled with increased muscle activity action support the position that increased neuromuscular in the forearm extensors when required to hold the entire drive generated in response to the more challenging task arm against gravity, compared to the EMG/tremor responses conditions is a contributing factor to revealing the aging- when only the ﬁnger is extended (the other segments were related increases in oscillatory outputs [51, 58]. supported externally). For the healthy elderly individuals, where tremor increases were reported, these were limited to the more distal segments only (e.g., the hand and ﬁnger), 5. Aging Changes in Physiological with no notable changes in the tremor from the forearm or Complexity of Tremor upper arm [24, 72]. Further, the age-related increases appear to be exacerbated when the older person performs the task in In addition to the challenges about the theoretical relevance a standing position compared to sitting [24], which supports of examining tremor in single joint versus multiple joint the view that relatively simple postural adjustments can also postural tasks, there is still, as noted previously, ambiguity inﬂuence tremor dynamics [87]. In both situations, however, as to whether tremor variability actually increases with the the tremor increase is primarily restricted to the neural 8– process of aging. In an eﬀort to provide greater insight as 12 Hz component and related muscle activity, indicating to the eﬀects of aging and/or disease on physiological and that changes in the output of those central neural processes behavioral processes, there has been an evaluation of the underlying tremor genesis were responsible for the aging- spatial/temporal pattern of the given tremor signal using related diﬀerences. measures of complexity [6, 12, 17]. These contrasting ﬁndings on single versus multiple This experimental approach to aging is based on the segment tremor invite the question as to the relative diﬃculty proposition that there is a deﬁcit in physiological function of movements performed about a single joint/segment. For that results from a progressive loss of complexity (i.e., comparison, the amplitude of physiological tremor observed dynamic variability) of the physiological system. This deﬁcit from the ﬁnger under single segment conditions has been has been phrased “loss of complexity” and is postulated to reported to be within the range of 1–3 mm [90], whereas, for arise from the general decrease in the number of elements of tasks requiring individuals to hold their entire arm up against a given system and/or decrease in the interaction/coupling gravity, oscillations of the order of 10–20 mm have been between control processes [6, 12, 19]. Given the complex reported for the index ﬁnger [24, 72]. If one considers the nature of the oscillatory output that is physiological tremor, task goal during these actions was to minimize limb postural it is natural that the theoretical perspective of complexity has motion (tremor), there is a higher degree of diﬃculty in been drawn on to examine the questions of the dynamics of controlling the muscles about an entire limb to minimize aging and disease with associated measures that are beyond 6 Journal of Aging Research Single joint action 0.1 0.02 0.08 0.015 0.06 0.01 0.04 0.005 0.02 Young Elderly 0 20406080 Multiple joint action 0.025 0.12 0.1 0.02 0.08 0.015 0.06 0.01 0.04 0.005 0.02 020 40 60 80 Young Elderly Frequency (Hz) Right arm Elderly Left arm Young (a) (b) Figure 3: Overall changes in mean RMS EMG activity from the extensor muscles of the forearm and examples of the power spectral proﬁles for a healthy young and elderly individual. Traces for each person are shown for conditions where only the ﬁnger was extended (the rest of the upper limb was externally supported) and when the entire upper arm was unsupported. As with Figure 2, any age-related diﬀerences in muscle activity were only seen under physically demanding task conditions. the standard dispersion indices of variability (e.g., standard greater repeatability or higher regularity in the time series. deviation). For example, using approximate entropy (ApEn) measures, Central to this approach has been the use of dynam- Sturman and associates [41] reported that there was an ical nonlinear measures of a physiological and behavioral increase in the time-dependent structure of physiological time series [20–22]. These tools have revealed changes in tremor with advanced age, despite there being no diﬀerences complexity with healthy aging and/or age-related diseases in tremor amplitude between the respective age groups. including essential tremor and Parkinson’s disease [23–27, Other studies have reported similar age-related diﬀerences 85]. One of the more commonly used measures has been in physiological tremor using the same analyses [24, 72, 81]. approximate entropy (ApEn), which has also been employed Interestingly, Hong et al. [81]conducted astudy to examine to assess complexity changes for a variety of physiological whether there were any age-related diﬀerences for tremor related signals including hormone secretion, isometric force in the frontal and transverse planes of motion. While no outputs, muscle activity, heart rate, postural motion, and gait aging-related eﬀects were observed for tremor in the vertical [37–40, 92, 93]. ApEn measures the probability that runs direction, changes in the tremor ApEn values for motion in of patterns that are close for m observations remain close the mediolateral axis between the young and older adults on the next (m + 1) incremental comparisons. This analysis were reported. produces a single value (range of 0–2) with higher values Together, these results support the view that aging and reﬂecting greater irregularity while lower values represent a disease can be reﬂected by a change in the time-dependent Mean extensor (ED) activity (mV) Mean extensor (ED) activity (mV) EMG power (mV) EMG power (mV) Journal of Aging Research 7 pattern or structure of the speciﬁc tremor signal output. This of freedom of the system. As we note later, a good example result, combined with the lack of any age diﬀerences in signal of this bi-directional hypothesis is in isometric force control regularity during the ﬁnger only conditions (see Figure 2), [94] where aging leads to a loss of complexity in the control is consistent with the proposition that the neuromuscular of a constant force level (where better performance is realized system of older individuals is typically not challenged enough by increasing the functional degrees of freedom) and an under the single segment condition to necessarily reveal increment in complexity in a sine wave force tacking (where any appreciable change in the system dynamics. The added better performance is realized by reducing the degrees of strength and coordination demands placed on the older freedom of the intrinsic dynamics). In this framework, the individual of having to hold their upper arm against gravity aging eﬀectismoregenerally alossofadaptationofthe and minimize tremor support the general premise of the loss functional degrees of freedom rather than universally loss of of complexity hypothesis. complexity. While it has been proposed that the general aging process is accompanied by a decrease in physiological complexity [6, 6. Isometric Force Production with Aging 12], it is important to note that, with regard to physiological tremor, the results of previous studies do not universally In grasping actions, individuals need to produce a certain support this perspective since there appears to be no consis- degree of isometric force in order to hold and/or manipulate tent diﬀerence in the structure of tremor signal under single agiven object [95, 96]. When producing this action, one segment conditions. The fact that several studies have either consequence is the production of small ﬂuctuations in the reported no change or a decline in physiological complexity force output, that have been referred to as reﬂecting force for tremor signal dynamics in older people lends support to steadiness or isometric force tremor [68, 97]. Healthy older the proposition that the hypothesis of a unidirectional nature individuals, in comparison to young adults, often exhibit of the loss of complexity hypotheses is too narrow [18]. A reduced control in force production, as quantiﬁed by an contrasting perspective is that there can be an increase or increase in these ﬂuctuations [59, 98, 99]. Interestingly, this decrease in a given signal’s pattern over time depending on age-related decline in force producing capacity has typically the interaction between components of the biological system been interpreted to reﬂect changes in motor unit (MU) and the inherent task dynamics [18]. control and sensorimotor function rather than in terms There is empirical evidence to support the position that of more macrothe constraintssuchasmusclestrength the aging-related changes in signal complexity can be bi- per se. The consequence of these changes is that elderly directional. In a recent study [85], it was reported that adults exhibit greater targeting error and isometric force the physiological tremor of older persons with Parkinson’s variability. As illustrated in Figure 4, both of these features disease (PD) exhibited a loss of complexity compared to the of variability tend to be more pronounced when producing lower maximum voluntary contraction (MVC) forces in healthy individuals of a similar age. However, the whole body comparison to higher maximal forces [57, 68, 100–102] motion (COP) of these same PD individuals was charac- and during force tracking tasks where a sinusoidal target is terized by an increase in signal complexity when compared displayed in comparison to a constant force target [103]. to the healthy elderly. This reciprocal pattern of change in Given the prevailing view that overall muscle strength these oscillatory signals within the same subjects supports declines with aging [3, 4, 13, 67], the ﬁnding that it is more the bi-directional perspective on changes in complexity diﬃcult to produce accurate levels of force output at lower with aging. Similarly, Hong et al. [81] reported that the MVC levels seems somewhat counterintuitive. If a decline in only signiﬁcant aging-related change in ﬁnger tremor was force producing capacity was to be the principal mitigating for side-to-side motion, while tremor in the vertical plane factor in the loss of muscle function in the older adult, then exhibited no diﬀerence between young, old (60–65 yrs), it would be predicted that producing higher forces would be and older-old (70–75 yrs) individuals. It would seem that a more diﬃcult. What these studies demonstrate is that any strong contributor to the observed age diﬀerences in signal age-related changes in movement ability are not merely the complexity is the older individual’s need to increase their product of alteration within the older muscle itself. Indeed, neuromuscular output so as to realize the speciﬁc demands similar to the ﬁndings shown previously for physiological of the task being performed [17]. tremor tasks, it would appear that the eﬀects of aging are The bi-directional hypothesis for the change of com- ampliﬁed under more challenging actions (e.g., sinusoidal plexity in the movement dynamics with aging is based on versus constant force production). the framework that the conﬂuence of organismic, envi- However, one important distinction can be made regard- ronmental, and task constraints channels the coordination ing the age-related changes in both physiological and and control of the system degrees of freedom [17, 18, 94]. isometric tremor. For physiological tremor, the argument In this view, the aging and loss of complexity eﬀect will often made is that the increased tremor amplitude reported hold when an increase in the dimension of behavior is where the entire arm is held against gravity primarily reﬂects required from the intrinsic dynamics to realize the task the diminished strength of the older person. However, the demands. And the bi-directional eﬀect of an increment same argument cannot be made for isometric force tremor, in complexity will be prevalent when the conﬂuence of since here the greatest diﬀerence is in performing tasks of constraints channels a reduction in the functional degrees lower force levels. Under isometric conditions, the suggested 8 Journal of Aging Research Sinusoidal force production Young Elderly 40% MVC ApEn = 0.33 ApEn = 0.37 20% MVC 4 4 ApEn = 0.35 ApEn = 0.44 3 3 2 2 1 1 0 2 4 6 8 10 12 14 16 18 20 0 2 4 6 8 10 12 14 16 18 20 Time (s) Time (s) (a) Constant force production Young Elderly 40% MVC 8 8 6 6 4 4 2 2 ApEn = 0.41 ApEn = 0.37 0 0 2 4 6 8 10 12 14 16 18 20 22 0 2 4 6 8 101214161820 Time (s) Time (s) 20% MVC 3 3 2.5 2.5 2 2 1.5 1.5 1 1 ApEn = 0.36 ApEn = 0.43 0.5 0.5 0 0 2 4 6 8 10 12 14 16 18 20 22 0 2 4 6 8 101214161820 Time (s) Time (s) Total force Target force (b) Figure 4: Representative examples of isometric force production trace (40% and 20% MVC) for a single young and older person. Examples are shown as individuals tracked a sinusoidal and constant target force. All traces were attained from a single subject during a single trial within each condition. Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Isometric force (N) Journal of Aging Research 9 reason(s) for the age-related diﬀerences in performance at in part be explained by the loss of complexity hypothesis lower force levels typically draws on the manner in which [6, 12, 19]. While the force signal for the older adult typically the neuromuscular system modulates MU recruitment and exhibits increased complexity under more challenging task ﬁring rate(s) in order to accurately grade force output [51, conditions, this pattern is not consistently prevalent across 94, 104]. Within this context, it would appear that the age- less challenging force levels or when diﬀerent eﬀectors are related variation in isometric force production dynamics utilized to perform the task [57, 69, 105, 107]. This invites the is driven more by task-speciﬁc control and coordination interpretation that any age diﬀerences in complexity of the constraints rather than the ability to produce (and sustain) signal output are more a function of the interaction between high absolute force levels [69]. extrinsic (task) and intrinsic (sacropenia, dynapenia) factors Further support for the notion that chronological age per rather than biological age being the single driving factor. se does not always drive the changes seen in force production Consequently, the pattern of changes in the biological signal comes from a study by Sosnoﬀ and Newell [105]. They are not consistent with the view that aging is reﬂected by reported that when diﬀerences in the maximal voluntary an overall loss of complexity [18]. Rather, the dynamics in contraction (MVC) force of young and older individuals the isometric force task reﬂect the conﬂuence of constraints were controlled for, there was no performance diﬀerence in including those of the aging individual, the task constraints, terms of the isometric force variability between age groups. and those of the environment. From these ﬁndings it was argued that chronological age is not, by itself, a suﬃcient indicator of the decline in isometric 8. Summary force control, but rather that the relative degree of weakness, irrespective of age, is a more appropriate biological index. With aging, there is a general decline in the physiological This result is of some importance since it would indicate function that is often manifested by speciﬁc changes in the that any age-related declines in isometric force control functional and structural properties of skeletal muscle [2– maybe more a function of inactivity, and so is modiﬁable 4, 51]. This decline in functional capacity of a given system by training, rather than simply the inevitable process of has been increasingly viewed within the context of the loss of decline associated with chronological aging. Indeed, sub- complexity hypothesis [6, 12]. While these changes alter the sequent studies have demonstrated that improvements in capacity of the individual muscle to respond, it is not clear isometric force control can be elicited with speciﬁc exercise to what degree these changes have a universal impact on an interventions [55, 106]. individual’s behavioral movement performance in physical activity. In the current paper, we examined the relation 7. Aging and Complexity in Isometric between aging, neuromuscular function, and physiological- Force Control behavioral complexity, speciﬁcally with reference to physi- As with the assessment of physiological tremor, additional ological tremor and isometric force production. These two insight as the any age-related changes in force production motor outputs were selected since they both derive primarily has been reported when measures of complexity have been from neuromuscular mechanisms, and the ability to control applied to the time series. In addition to the straightforward and minimize these oscillatory outputs is essential for the assessments of changes in force variability or targeting error, performance of many activities of daily living (ADL’s) which many studies have reported that the age-related diﬀerences contain a ﬁne motor skill component. The examination in force control extend to diﬀerences in the frequency of age-related changes in these motor processes would proﬁle of their force output, the pattern of regularity (based therefore provide greater understanding of the relation upon changes in ApEn and SampEn), and, where multiple between muscle adaptations and chronological age. A central digits are employed, changes in the coupling relations point to emerge is that there is no single pattern to the between these eﬀectors [100, 101, 103, 105, 107, 108]. When changes seen in physiological and isometric force tremor reviewing the resultant force signals, it is interesting to in older adults. Rather, it would appear that the speciﬁc compare the age-related diﬀerences in signal complexity alterations in the given motor outputs reﬂect a myriad of for isometric actions with the responses generated for extrinsic (task related) and intrinsic (muscle weakness, loss physiological tremor tasks. As shown in Figure 5, the force of coordination) constraints that are unlikely to be all the response from older adults is highlighted by an increase direct result of the process of aging. Consequently, it is in complexity (increased ApEn) in comparison to younger argued that any amplitude or structural changes observed individuals when performing more challenging isometric in physiological and force tremor amplitude reﬂect the task (e.g., 20% MVC, sinusoidal tracking). However, during diminished ability of the older neuromuscular system to more demanding postural tremor tasks (e.g., whole arm adapt to diﬀering task demands. extended, see Figure 2), the tremor output from the older Finally, the ﬁndings of this body of research do not adult was characterized by a decline in complexity (lower universally support the unidirectional interpretation that ApEn). aging is associated with a loss of physiological and behavioral It would appear that, as with the discussion of the complexity. Instead, the variable pattern of change in eﬀect of aging on physiological tremor, the changes in the complexity observed across both physiological and isometric isometric force producing ability of older person can only tremor forms in older adults supports the broader view 10 Journal of Aging Research Isometric force tremor 20% MVC, sinusoidal 20% MVC, constant 0.8 0.8 0.6 0.6 0.4 0.4 0.2 0.2 0 0 Young Elderly Young Elderly (a) Physiological tremor Multiple segment Single segment 1.8 1.8 1.6 1.6 1.4 1.4 1.2 1.2 Young Elderly Young Elderly Right ﬁnger Right ﬁnger Left ﬁnger Left ﬁnger (b) Figure 5: Age-related diﬀerences in approximate entropy (ApEn) measures for isometric force (a) and postural tremor (b) tasks. Changes in ApEn across the young and older individuals are shown for both the multiple segment and single-segment tremor tasks. In addition, the age-related diﬀerences during two isometric actions (20% MVC performed under sinusoidal tracking and constant force conditions) are also shown. This ﬁgure illustrates that the tremor signal tends to be less complex (lower ApEn) during multiple-segment tremor tasks and the 20% MVC constant force producing actions. However, for the 20% MVC sinusoidal funder isometric force task, the resultant signal for the older adults is more complex (higher ApEn) in comparison to the younger adults. Error bars represent one standard error of the mean. Mean ApEn Mean ApEn Mean ApEn Mean ApEn Journal of Aging Research 11 that age-related changes in physiological complexity are bi- Clinical Nutrition and Metabolic Care, vol. 13, no. 3, pp. 271– 276, 2010. directional, depending to a large degree on the constraints [16] D. J. Clark and R. A. Fielding, “Neuromuscular contributions to action. 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Aging, Neuromuscular Decline, and the Change in Physiological and Behavioral Complexity of Upper-Limb Movement Dynamics

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Aging, Neuromuscular Decline, and the Change in Physiological and Behavioral Complexity of Upper-Limb Movement Dynamics

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