Neuroscience Letters 396 (2006) 192–196

Emotion and movement: Activation of defensive circuitry alters the magnitude of a sustained muscle contraction Stephen A. Coombes ∗ , James H. Cauraugh, Christopher M. Janelle University of Florida, USA Received 9 September 2005; received in revised form 30 October 2005; accepted 23 November 2005

Abstract Understanding the emotion–movement relationship is crucial to the development of motor theory and movement rehabilitation recommendations for a wide range of diseases and injuries that involve motor impairment. Behaviorally, when movements are executed following exposure to emotional stimuli, evidence suggests that active defensive circuitry results in faster but more variable voluntary movements. However, each of the existing protocols has involved movement execution following the offset of anxiety or emotion eliciting stimuli. The specific aim of this study, therefore, was to determine whether the continued exposure to emotional stimuli would alter the magnitude and variability of a sustained motor contraction. During the presentation of pleasant, unpleasant, neutral, and blank images, participants (N = 45) were instructed to respond to the onset of an auditory stimulus by initiating and then sustaining a maximal bimanual isometric contraction of the wrist and finger extensor muscles against two independent load cells (left/right limb). Corroborating previous evidence and supporting hypothesis 1, findings indicated that exposure to unpleasant images lead to an increase in mean force production. Variability of movement, however, did not vary as a function of affective context. These findings indicate that continued exposure to unpleasant stimuli magnifies the force production of a sustained voluntary movement, without sacrificing the variability of that contraction. Mechanism driven open and closed loop explanations are offered for these phenomena, implications are addressed, and future directions are discussed. © 2005 Elsevier Ireland Ltd. All rights reserved. Keywords: Emotion; Force; Sustained muscle contraction

The necessity to understand the impact of emotion on motor control has recently been recognized by researchers emanating from a broad range of scientific domains. In the mainstream affective sciences, the neural correlates of fear- and reward-related systems continue to receive substantial empirical attention given their primitive origin, evolutionary significance, behavioral impact, and acute involvement in the development and perpetuation of affective disorders (i.e., anxiety, phobia) [12,6,15]. Likewise, motor control researchers remain diligent in their quest to determine the cortical and subcortical structures that independently or collectively execute, inhibit, and control movement [10]. Clearly, these efforts continue to be crucial to the development of motor theory and movement rehabilitation recommendations for a wide range of diseases and

∗ Corresponding author at: University of Florida, Department of Applied Physiology and Kinesiology, P.O. Box 118205, 100 FLG, Gainesville, FL 32611, USA. Tel.: +1 352 392 0584x1378; fax: +1 352 392 0316. E-mail address: [email protected] (S.A. Coombes).

0304-3940/$ – see front matter © 2005 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2005.11.048

injuries that involve motor impairment (i.e., stroke, Parkinson’s disease). The recent convergence of these and related disciplines has resulted in novel approaches to understanding the neural circuitry that regulates movement, emotion, and their interaction [7,11,4]. Based on extensive psychophysiological data, coupled with acknowledgement of the amygdala as central to emotional processing, the biphasic theory of emotion [13] posits that the broad array of emotions experienced and displayed by human beings can be organized according to their valence (i.e., appetitive or defensive) and intensity (i.e., arousal level). When engaged, each system (appetitive, defensive) impacts the functioning brain, priming physiological adaptation and specific representations, associations, and action programs that correspond to the environmental context that has elicited the given emotion. In short, a primary function of emotion is the preparation for action [20]. To date, however, although active defensive circuitry has been associated with faster voluntary movements [3,5,16], and greater movement error [5,18], each of the existing protocols has either required direction specific movements [3,16] and/or has

S.A. Coombes et al. / Neuroscience Letters 396 (2006) 192–196

involved movement execution following the offset of anxiety or emotion eliciting stimuli [3,5,16,18]. Simulating approach and avoidance behaviors via lever pushing and pulling protocols has provided considerable insight into emotion-modulated movement. Founded in the premise that the perception of aversive stimuli is associated with rapid muscle extension, whereas the perception of appetitive stimuli is associated with muscle flexion [1], Chen and Bargh reported that participants pushed a lever faster following exposure to negative words and pulled faster to positive words [3]. However, although Marsh et al. similarly demonstrated that pushing movements are accelerated when participants are exposed to images depicting anger, the authors also reported faster pulling movements coinciding with the perception of fear in others [16]. Consequently, the issue of whether or not unpleasant aversive stimuli exclusively prime extension related avoidance movements remains a prominent topic in the emotion–movement literature. The nature of the task, the context, and the emotion eliciting stimuli all appear to mediate the characteristics of the subsequent movement. In the present study, given that our goal was to determine the impact of emotion on the maintenance of a sustained contraction, we sought to neutralize the impact of movement direction by using an extension task, which required upwards movement rather than movements toward or away from the participant. In consequence, although predictive hypotheses can be garnered from these studies; the continued impact of emotion on the magnitude and variability of a sustained directionally nonspecific motor contraction remains unknown. The execution of movement typically coincides with, rather than follows, exposure to emotional stimuli. Further, given that emotions impact varying physiological systems in functionally and temporally different ways, the question remains, how does an ongoing affective context alter the magnitude and variability of sustained force production? Consequently, we sought to determine the specific impact of exposure to affective images on the human motor system. We predicted that relative to exposure to pleasant, neutral, and blank images, exposure to unpleasant images and the consequential activation of defensive circuitry would modulate the activated motor system such that sustained force production would be amplified (increased mean force) but more variable (increased coefficient of variation). Forty-five undergraduate students (females = 26; males = 19; age range = 18–29 years, M = 21.00 years, S.D. = 2.15) from the University of Florida participated in this study for extra course credit. Three subjects were excluded from the analysis due to technical issues. Participants reported no hearing loss or central nervous system disorders that would affect movement. Written informed consent was obtained from all participants prior to beginning the study. Participants viewed six digitized photographs selected from the International Affective Picture System (IAPS; NIMH Center for the Study of Emotion and Attention, 2005) representing three affective categories (IAPS image numbers and descriptions: pleasant, erotic couples: 4660, 4680; unpleasant, attack 6313, disfigured child, 3170; neutral, human face, 2210, wicker basket 7010). Images were selected according to affective normative ratings [14] to ensure that pleasant and unpleasant images

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were similarly arousing, and that each were significantly more arousing than neutral images (P = 6.3; U = 7.0; N = 2.66). For valence, each category significantly differed from each other (P = 7.3; U = 1.12; N = 4.66). In addition, two blank black images were presented to provide a control condition. All pictures were visible for 13 s. Stimulus presentation order was randomized and counterbalanced to control for the potential variability due to fatigue. While viewing each picture, participants were required to respond to an acoustic stimulus by initiating and then maintaining a sustained isometric bimanual contraction of the wrist and finger extensor muscles against two independent load cells. Acoustic stimuli were randomly presented binaurally through a set of calibrated headphones (Radio Shack digital sound level meter: 33-2055, Fort Worth, TX) 2–4 s following picture onset. To index force generation during each sustained isometric wrist extension, two 34.1 kg load cells embedded in cushioned platforms, were altered in height to accommodate each limb (see Fig. 1). Force data were amplified by 5 K and collected at 1000 Hz via Biopac software (3.7.3, Biopac Systems Inc., Goleta, CA, USA). Trial onset and offset, and visual and auditory stimulus presentation were controlled via a custom Labview program (7.1; National Instruments, Austin, TX). The customwritten program simultaneously sent a 5-V digital marker into the physiological trace to indicate picture onset and acoustic stimulus onset. Each separate 17 s trial (2 s baseline; 13 s picture presentation; 2 s buffer) was streamed to disk for offline analyses. After all questions had been answered, participants were seated in a comfortable chair positioned 1.0 m from an 18 in. LCD presentation screen. Next, the force platforms were calibrated. Following calibration, participants were familiarized with the protocol via a two trial practice session (unique neu-

Fig. 1. Experimental set up. Top: postures of arms, forearms, and shoulders before and during the bimanual task. Bottom left: posture of hands relative to load cells during movement preparation and ITI. Bottom right: posture of hands relative to load cells during movement execution.

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tral images). Participants were instructed to (1) “look at each picture for the entire time it is on the screen”, (2) “consider picture onset as a cue to get ready to make the required wrist and finger extension”, and (3) “respond to any acoustic stimuli by initiating and then sustaining a maximal bimanual isometric contraction of the wrist and finger extensor muscles for the entire time the picture is on the screen” (see Fig. 1). At picture offset, participants were instructed to relax, but to continue viewing the blank screen as the next image would appear after a short break (intertrial intervals were randomly altered to between 20 and 30 s). At the conclusion of all trials, limbs were removed from the customized force platform and the participants were debriefed. Two dependent variable scores were calculated for each trial: mean force generation, and coefficient of variation (CV) (standard deviation/mean force). CV scores were calculated and analyzed to ensure that variability was normalized to the magnitude of the corresponding absolute force value. For each trial for each limb, a semi-automated custom Labview analysis program superimposed force data over the digital trigger signal. Visible on a computer monitor, the program automatically identified and then inserted a cursor at the location of peak force. From peak force onset, four consecutive 2 s windows were parsed from the trial. Baseline corrected mean force and CV scores were calculated for each of the four time windows. Baseline scores were calculated from the 1.5 s period immediately preceding image onset. To establish whether affective context altered a sustained motor contraction, mean force and CV were each analyzed in 4 (valence: pleasant, unpleasant, neutral, blank) × 2 (limb: dominant, non-dominant) × 4 (time: windows 1, 2, 3, 4) ANOVA with repeated measures on all three factors. For F-ratios involving valence and/or time, if the sphericity assumption was violated, then Geisser–Greenhouse degrees of freedom corrections were applied. Follow-up analyses were conducted using simple effects tests and Tukey’s HSD procedure for significant interactions and main effects, respectively. For all analyses, the probability value was set at p < .05. Strong effects of Valence were evidenced for mean force (see Fig. 2). Specifically, when sustained contractions were executed during exposure to unpleasant images, relative to all other conditions, mean force was significantly elevated (F(1.79, 57.40) = 4.46, p = .02). On the contrary, analyses of CV scores evidenced that variability of force production was similar across all valence categories (F(3, 96) = 2.11, p < .11) (see Fig. 3). Analyses of Time indicated that across consecutive time segments, participants displayed a progressive attenuation of mean force production (F(1.17, 38.27) = 31.91, p < .001) and variability of force production (F(1.35, 36.33) = 53.90, p < .001). As illustrated in Fig. 2, mean force production was largest during the first 2 s window and then significantly decreased in each proceeding 2 s window. CV followed a similar pattern (see Fig. 3), with variability being greatest during time segment 1 and smallest during segment 4, relative to all other segments. Segments 2 and 3 were indistinguishable from each other (see Table 1 for all mean scores and S.E. for mean force and CV). This progressive attenuation of force production is displayed in exemplar

Fig. 2. Mean force averaged across limb: main effects of valence and time segment. When exposed to unpleasant images (i.e., activation of defensive circuitry) relative to all other valence conditions, participants produced greater mean force across all time segments. Further, mean force within all time segments were all significantly different from each other, evidencing a progressive decrease in mean force across time.

raw force traces in Fig. 4. The analyses failed to identify main effects for limb. The purpose of this experiment was to determine whether activation of defensive circuitry altered the magnitude and variability of force production during a sustained voluntary contraction of the wrist and finger extensors. In line with our prediction, activation of defensive circuitry increased mean force production during the entire sustained wrist and finger contraction. Contrary to our hypothesis, however, variability scores appeared to be independent of the magnitude of mean force production and remained similar across the four levels of valence. Coupled with the notion that emotions are a product of evolution that provide organisms with an increased chance of

Fig. 3. Variability averaged across limb: coefficient of variation (CV) scores evidenced that maintenance of force production was similar across all valence categories. Stability of force production, however, did vary according to time segment. Compared to all other segments, variability was largest during time segment 1 and smallest during segment 4. Segments 2 and 3 were statistically indistinguishable.

S.A. Coombes et al. / Neuroscience Letters 396 (2006) 192–196 Table 1 Mean force and variability scores and there respective S.E. values Valence

Time

Mean force (kg)

Variability (CV)

M

S.E.

M

S.E.

Pleasant

1 2 3 4

2.42 2.00 1.90 1.84

0.30 0.27 0.27 0.27

16.61 6.10 6.44 6.33

1.58 0.57 0.82 1.18

Unpleasant

1 2 3 4

2.54 2.17 2.04 1.98

0.28 0.27 0.27 0.27

15.90 6.52 5.06 4.80

1.42 0.54 0.40 0.57

Neutral

1 2 3 4

2.26 1.88 1.81 1.69

0.27 0.25 0.25 0.24

17.26 6.30 6.53 5.46

1.78 0.46 0.73 0.56

Blank

1 2 3 4

2.39 1.89 1.80 1.73

0.28 0.23 0.24 0.23

18.25 7.15 6.94 5.50

1.99 0.74 0.97 0.55

Data are averaged across left and right limbs.

survival [19], and given that unpleasant and pleasant images were matched for arousal, we posit that organisms have evolved such that when confronted with unpleasant/threatening situations they implicitly execute sustained voluntary movements with greater force without sacrificing movement variability. The lack of variation in the maintenance of force production deviates from the work of Noteboom et al. who reported a decrease in pinch grip stability following a 10-min session during which electric shocks were both threatened and administered to the back of participants’ hands [18]. The intensity of the threatening context is one potential explanation for this incongruence. In addition, a target force was not required in the present study, removing a number of potentially interactive variables concerning feedback, accuracy, and perception-action coupling. Ensuring that entire task performance coincided with the continued exposure to emotional images removed the temporal issue

Fig. 4. Sample force traces over the whole collection period demonstrating the systematic decreases in force production during each 2-s time period. Example traces are displayed for one pleasant and one unpleasant condition for one subject (dominant limb).

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that is raised by the time frame within which emotions alter central and peripheral motor control systems. These data extend previous findings concerning the affective modulation of voluntary movements. That is, in addition to the direction, speed and accuracy of short duration ballistic movements, the force of sustained isometric contractions are also significantly altered by affective context [3,16,8]. The stability of force generation evidenced herein offers a second contribution to the literature. As such, these data offer further insight into the manner by which emotions alter basic motor function. As a result, the prediction that active defensive circuitry accentuates force production remains a viable postulate. Likewise, further investigation into the stability of affectively modulated movements is encouraged. Given the conclusive nature of our behavioral data we offer two mechanistic explanations to address how active defensive circuitry alters the execution of a sustained contraction. The first explanation assumes an open loop control system in which only a single motor program was projected to the periphery. According to this postulate, following affective modulation (potentially via amygdala and cortico-basal ganglia loops [9]), the program projected to the periphery was of a magnitude such that it could be consistently maintained (above other valence contexts) across the 8 s contraction. A second possibility implicates modulation of a closed loop circuit in which multiple motor cortex projections were sent to the peripheral motor system. In this scenario, even minor latencies between projections could have resulted in increased variability in the overt demonstration of sustained force production (as predicted). However, either the latencies between projections were insignificant, or, activation of defensive circuitry only interferes with overt movements when a target upon which to aim the movement is presented [5,18]. During sustained nonspecific contractions, therefore, affective modulation of this closed loop circuit was such that more forceful motor programs are created (potentially via BG modulation), projected, and executed in a stable fashion. Consequently, if magnified but stable force is a goal, then we posit that altering affective context is a viable manipulation to achieve this aim. The necessity of understanding how emotions alter the motor system is paramount given the extensive range of movements that humans strive to initiate, control, and inhibit. Taking into account the multitude of motor deficits associated with affective disorders and the array of movement disorders that manifest in movement error (Parkinsons [17]) and an inability to generate adequate stable force (stroke [2]) these data hold considerable promise. Further, the simplicity of the protocol implemented in this experiment lends itself well to contemporary imaging technologies. Along with consistent replication and extension of psychophysiological, neurological, and behavioral evidence, we are confident that this protocol and minor variations of it will permit future investigations that will allow strong inference concerning the central and peripheral circuitry involved in emotion modulated movements. Identifying the key structures involved in the emotion–movement relationship and the manner in which they yield overt motor actions remains a challenge for future researchers. To conclude, considerable steps need to be taken to ensure that a rapidly evolving knowledge

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