How reward modulates mimicry: EMG evidence of greater automatic facial mimicry of more rewarding faces

Spontaneous mimicry is a marker of empathy. Conditions characterized by reduced spontaneous mimicry (e.g., autism) also display deficits in sensitivity to social rewards. We tested if spontaneous mimicry of socially rewarding stimuli (happy faces) depends on the reward value of stimuli in 32 typical participants. An evaluative conditioning paradigm was used to associate different reward values with neutral target faces. Subsequently, electromyographic activity over the Zygomaticus Major was measured whilst participants watched video clips of the faces making happy expressions. Higher Zygomaticus Major activity was found in response to happy faces conditioned with high reward versus low reward. Moreover, autistic traits in the general population modulated the extent of spontaneous mimicry of happy faces. This suggests a link between reward and spontaneous mimicry and provides a possible underlying mechanism for the reduced response to social rewards seen in autism.

Fetal programming effects of testosterone on the reward system and behavioral approach tendencies in humans

BACKGROUND: Sex differences are present in many neuropsychiatric conditions that affect emotion and approach-avoidance behavior. One potential mechanism underlying such observations is testosterone in early development. Although much is known about the effects of testosterone in adolescence and adulthood, little is known in humans about how testosterone in fetal development influences later neural sensitivity to valenced facial cues and approach-avoidance behavioral tendencies. METHODS: With functional magnetic resonance imaging we scanned 25 8-11-year-old children while viewing happy, fear, neutral, or scrambled faces. Fetal testosterone (FT) was measured via amniotic fluid sampled between 13 and 20 weeks gestation. Behavioral approach-avoidance tendencies were measured via parental report on the Sensitivity to Punishment and Sensitivity to Rewards questionnaire. RESULTS: Increasing FT predicted enhanced selectivity for positive compared with negatively valenced facial cues in reward-related regions such as caudate, putamen, and nucleus accumbens but not the amygdala. Statistical mediation analyses showed that increasing FT predicts increased behavioral approach tendencies by biasing caudate, putamen, and nucleus accumbens but not amygdala to be more responsive to positive compared with negatively valenced cues. In contrast, FT was not predictive of behavioral avoidance tendencies, either through direct or neurally mediated paths. CONCLUSIONS: This work suggests that testosterone in humans acts as a fetal programming mechanism on the reward system and influences behavioral approach tendencies later in life. As a mechanism influencing atypical development, FT might be important across a range of neuropsychiatric conditions that asymmetrically affect the sexes, the reward system, emotion processing, and approach behavior.

Empathy and emotion recognition in people with autism, first-degree relatives, and controls

Empathy is the lens through which we view others' emotion expressions, and respond to them. In this study, empathy and facial emotion recognition were investigated in adults with autism spectrum conditions (ASC; N=314), parents of a child with ASC (N=297) and IQ-matched controls (N=184). Participants completed a self-report measure of empathy (the Empathy Quotient [EQ]) and a modified version of the Karolinska Directed Emotional Faces Task (KDEF) using an online test interface. Results showed that mean scores on the EQ were significantly lower in fathers (p<0.05) but not mothers (p>0.05) of children with ASC compared to controls, whilst both males and females with ASC obtained significantly lower EQ scores (p<0.001) than controls. On the KDEF, statistical analyses revealed poorer overall performance by adults with ASC (p<0.001) compared to the control group. When the 6 distinct basic emotions were analysed separately, the ASC group showed impaired performance across five out of six expressions (happy, sad, angry, afraid and disgusted). Parents of a child with ASC were not significantly worse than controls at recognising any of the basic emotions, after controlling for age and non-verbal IQ (all p>0.05). Finally, results indicated significant differences between males and females with ASC for emotion recognition performance (p<0.05) but not for self-reported empathy (p>0.05). These findings suggest that self-reported empathy deficits in fathers of autistic probands are part of the 'broader autism phenotype'. This study also reports new findings of sex differences amongst people with ASC in emotion recognition, as well as replicating previous work demonstrating empathy difficulties in adults with ASC. The use of empathy measures as quantitative endophenotypes for ASC is discussed.

Psychophysics of emotion: the QUEST for emotional attention

To investigate the mechanisms involved in automatic processing of facial expressions, we used the QUEST procedure to measure the display durations needed to make a gender decision on emotional faces portraying fearful, happy, or neutral facial expressions. In line with predictions of appraisal theories of emotion, our results showed greater processing priority of emotional stimuli regardless of their valence. Whereas all experimental conditions led to an averaged threshold of about 50 ms, fearful and happy facial expressions led to significantly less variability in the responses than neutral faces. Results suggest that attention may have been automatically drawn by the emotion portrayed by face targets, yielding more informative perceptions and less variable responses. The temporal resolution of the perceptual system (expressed by the thresholds) and the processing priority of the stimuli (expressed by the variability in the responses) may influence subjective and objective measures of awareness, respectively.

Beta event-related desynchronization as an index of individual differences in processing human facial expression: further investigations of autistic traits in typically developing adults

The human mirror neuron system (hMNS) has been associated with various forms of social cognition and affective processing including vicarious experience. It has also been proposed that a faulty hMNS may underlie some of the deficits seen in the autism spectrum disorders (ASDs). In the present study we set out to investigate whether emotional facial expressions could modulate a putative EEG index of hMNS activation (mu suppression) and if so, would this differ according to the individual level of autistic traits [high versus low Autism Spectrum Quotient (AQ) score]. Participants were presented with 3 s films of actors opening and closing their hands (classic hMNS mu-suppression protocol) while simultaneously wearing happy, angry, or neutral expressions. Mu-suppression was measured in the alpha and low beta bands. The low AQ group displayed greater low beta event-related desynchronization (ERD) to both angry and neutral expressions. The high AQ group displayed greater low beta ERD to angry than to happy expressions. There was also significantly more low beta ERD to happy faces for the low than for the high AQ group. In conclusion, an interesting interaction between AQ group and emotional expression revealed that hMNS activation can be modulated by emotional facial expressions and that this is differentiated according to individual differences in the level of autistic traits. The EEG index of hMNS activation (mu suppression) seems to be a sensitive measure of the variability in facial processing in typically developing individuals with high and low self-reported traits of autism.

Searching for happiness across cultures

Three experiments examined the cultural relativity of emotion recognition using the visual search task. Caucasian-English and Japanese participants were required to search for an angry or happy discrepant face target against an array of competing distractor faces. Both cultural groups performed the task with displays that consisted of Caucasian and Japanese faces in order to investigate the effects of racial congruence on emotion detection performance. Under high perceptual load conditions, both cultural groups detected the happy face more efficiently than the angry face. When perceptual load was reduced such that target detection could be achieved by feature-matching, the English group continued to show a happiness advantage in search performance that was more strongly pronounced for other race faces. Japanese participants showed search time equivalence for happy and angry targets. Experiment 3 encouraged participants to adopt a perceptual based strategy for target detection by removing the term 'emotion' from the instructions. Whilst this manipulation did not alter the happiness advantage displayed by our English group, it reinstated it for our Japanese group, who showed a detection advantage for happiness only for other race faces. The results demonstrate cultural and linguistic modifiers on the perceptual saliency of the emotional signal and provide new converging evidence from cognitive psychology for the interactionist perspective on emotional expression recognition.

Autistic traits modulate frontostriatal connectivity during processing of rewarding faces

Deficits in facial mimicry have been widely reported in autism. Some studies have suggested that these deficits are restricted to spontaneous mimicry and do not extend to volitional mimicry. We bridge these apparently inconsistent observations, by testing the impact of reward value on neural indices of mimicry, and how autistic traits modulate this impact. Neutral faces were conditioned with high and low reward. Subsequently, functional connectivity between the ventral striatum (VS) and inferior frontal gyrus (IFG) was measured whilst neurotypical adults (n = 30) watched happy expressions made by these conditioned faces. We found greater VS-IFG connectivity in response to high-reward vs. low-reward happy faces. This difference was negatively proportional to autistic traits, suggesting that reduced spontaneous mimicry of social stimuli seen in autism, maybe related to a failure in the modulation of the mirror system by the reward system rather than a circumscribed deficit in the mirror system.

Neural responses to emotional faces in women recovered from anorexia nervosa

Impairments in emotional processing have been associated with anorexia nervosa. However, it is unknown whether neural and behavioural differences in the processing of emotional stimuli persist following recovery. The aim of this study was to investigate the neural processing of emotional faces in individuals recovered from anorexia nervosa compared with healthy controls. Thirty-two participants (16 recovered anorexia nervosa, 16 healthy controls) underwent a functional magnetic resonance imaging (fMRI) scan. Participants viewed fearful and happy emotional faces and indicated the gender of the face presented. Whole brain analysis revealed no significant differences between the groups to the contrasts of fear versus happy and vice versa. Region of interest analysis demonstrated no significant differences in the neural response to happy or fearful stimuli between the groups in the amygdala or fusiform gyrus. These results suggest that processing of emotional faces may not be aberrant after recovery from anorexia nervosa.

NK1 receptor antagonism and the neural processing of emotional information in healthy volunteers

The neuropeptide substance P and its receptor NK1 have been implicated in emotion, anxiety and stress in preclinical studies. However, the role of NK1 receptors in human brain function is less clear and there have been inconsistent reports of the value of NK1 receptor antagonists in the treatment of clinical depression. The present study therefore aimed to investigate effects of NK1 antagonism on the neural processing of emotional information in healthy volunteers. Twenty-four participants were randomized to receive a single dose of aprepitant (125 mg) or placebo. Approximately 4 h later, neural responses during facial expression processing and an emotional counting Stroop word task were assessed using fMRI. Mood and subjective experience were also measured using self-report scales. As expected a single dose of aprepitant did not affect mood and subjective state in the healthy volunteers. However, NK1 antagonism increased responses specifically during the presentation of happy facial expressions in both the rostral anterior cingulate and the right amygdala. In the emotional counting Stroop task the aprepitant group had increased activation in both the medial orbitofrontal cortex and the precuneus cortex to positive vs. neutral words. These results suggest consistent effects of NK1 antagonism on neural responses to positive affective information in two different paradigms. Such findings confirm animal studies which support a role for NK1 receptors in emotion. Such an approach may be useful in understanding the effects of novel drug treatments prior to full-scale clinical trials.

Rerum cognoscere causas: part II - opportunities generated by the agency/structure debate and suggestions for clarifying the social theoretic position of system dynamics

This is the second half of a two-part paper dealing with the social theoretic assumptions underlying system dynamics. In the first half it was concluded that analysing system dynamics using traditional, paradigm-based social theories is highly problematic. An innovative and potentially fruitful resolution is now proposed to these problems. In the first section it is argued that in order to find an appropriate social theoretic home for system dynamics it is necessary to look to a key exchange in contemporary social science: the agency/structure debate. This debate aims to move beyond both the theories based only on the actions of individual human agents, and those theories that emphasise only structural influences. Emerging from this debate are various theories that instead aim to unite the human agent view of the social realm with views that concentrate solely on system structure. It is argued that system dynamics is best viewed as being implicitly grounded in such theories. The main conclusion is therefore that system dynamics can contribute to an important part of social thinking by providing a formal approach for explicating social mechanisms. This conclusion is of general significance for system dynamics. However, the over-arching aim of the two-part paper is to increase the understanding of system dynamics in related disciplines. Four suggestions are therefore offered for how the system dynamics method might be extended further into the social sciences. It is argued that, presented in the right way, the formal yet contingent feedback causality thinking of system dynamics should diffuse widely in the social sciences and make a distinctive and important contribution to them. Felix qui potuit rerum cognoscere causas Happy is he who comes to know the causes of things Virgil - Georgics, Book II, line 490. 29 BCE

The influence of anxiety on the initial selection of emotional faces presented in binocular rivalry

Neurocognitive theories of anxiety predict that threat-related information can be evaluated before attentional selection, and can influence behaviour differentially in high anxious compared to low anxious individuals. We investigate this further by presenting emotional and neutral faces in an adapted binocular rivalry paradigm. We show that the initial selection of emotional faces presented in binocular rivalry is highly influenced by self-reported state and trait anxiety-level. Heightened anxiety was correlated with increased perception of angry and fearful faces, and decreased perception of happy expressions. These results are consistent with recent evidence of involuntary selection of threat in anxiety.

The plasticity of the mirror system: how reward learning modulates cortical motor simulation of others

Cortical motor simulation supports the understanding of others' actions and intentions. This mechanism is thought to rely on the mirror neuron system (MNS), a brain network that is active both during action execution and observation. Indirect evidence suggests that alpha/beta suppression, an electroencephalographic (EEG) index of MNS activity, is modulated by reward. In this study we aimed to test the plasticity of the MNS by directly investigating the link between alpha/beta suppression and reward. 40 individuals from a general population sample took part in an evaluative conditioning experiment, where different neutral faces were associated with high or low reward values. In the test phase, EEG was recorded while participants viewed videoclips of happy expressions made by the conditioned faces. Alpha/beta suppression (identified using event-related desynchronisation of specific independent components) in response to rewarding faces was found to be greater than for non-rewarding faces. This result provides a mechanistic insight into the plasticity of the MNS and, more generally, into the role of reward in modulating physiological responses linked to empathy.

Latent learning in end stage renal disease (ESRD)

Cognitive functions such as attention and memory are known to be impaired in End Stage Renal Disease (ESRD), but the sites of the neural changes underlying these impairments are uncertain. Patients and controls took part in a latent learning task, which had previously shown a dissociation between patients with Parkinson’s disease and those with medial temporal damage. ESRD patients (n=24) and age and education-matched controls (n=24) were randomly assigned to either an exposed or unexposed condition. In Phase 1 of the task, participants learned that a cue (word) on the back of a schematic head predicted that the subsequently seen face would be smiling. For the exposed (but not unexposed) condition, an additional (irrelevant) colour cue was shown during presentation. In Phase 2, a different association, between colour and facial expression, was learned. Instructions were the same for each phase: participants had to predict whether the subsequently viewed face was going to be happy or sad. No difference in error rate between the groups was found in Phase 1, suggesting that patients and controls learned at a similar rate. However, in Phase 2, a significant interaction was found between group and condition, with exposed controls performing significantly worse than unexposed (therefore demonstrating learned irrelevance). In contrast, exposed patients made a similar number of errors to unexposed in Phase 2. The pattern of results in ESRD was different from that previously found in Parkinson’s disease, suggesting a different neural origin.

Aberrant brain responses to emotionally valent words is normalised after cognitive behavioural therapy in female depressed adolescents

AbstractBackground Depression in adolescence is debilitating with high recurrence in adulthood, yet its pathophysiological mechanism remains enigmatic. To examine the interaction between emotion, cognition and treatment, functional brain responses to sad and happy distractors in an affective go/no-go task were explored before and after Cognitive Behavioural Therapy (CBT) in depressed female adolescents, and healthy participants. Methods Eighty-two Depressed and 24 healthy female adolescents, aged 12 to 17 years, performed a functional magnetic resonance imaging (fMRI) affective go/no-go task at baseline. Participants were instructed to withhold their responses upon seeing happy or sad words. Among these participants, 13 patients had CBT over approximately 30 weeks. These participants and 20 matched controls then repeated the task. Results At baseline, increased activation in response to happy relative to neutral distractors was observed in the orbitofrontal cortex in depressed patients which was normalized after CBT. No significant group differences were found behaviourally or in brain activation in response to sad distractors. Improvements in symptoms (mean: 9.31, 95% CI: 5.35-13.27) were related at trend-level to activation changes in orbitofrontal cortex. Limitations In the follow-up section, a limited number of post-CBT patients were recruited. Conclusions To our knowledge, this is the first fMRI study addressing the effect of CBT in adolescent depression. Although a bias toward negative information is widely accepted as a hallmark of depression, aberrant brain hyperactivity to positive distractors was found and normalised after CBT. Research, assessment and treatment focused on positive stimuli could be a future consideration. Moreover, a pathophysiological mechanism distinct from adult depression may be suggested and awaits further exploration.

Spontaneous facial mimicry is modulated by joint attention and autistic traits

Joint attention (JA) and spontaneous facial mimicry (SFM) are fundamental processes in social interactions, and they are closely related to empathic abilities. When tested independently, both of these processes have been usually observed to be atypical in individuals with autism spectrum conditions (ASC). However, it is not known how these processes interact with each other in relation to autistic traits. This study addresses this question by testing the impact of JA on SFM of happy faces using a truly interactive paradigm. Sixty-two neurotypical participants engaged in gaze-based social interaction with an anthropomorphic, gaze-contingent virtual agent. The agent either established JA by initiating eye contact or looked away, before looking at an object and expressing happiness or disgust. Eye tracking was used to make the agent's gaze behavior and facial actions contingent to the participants' gaze. SFM of happy expressions was measured by Electromyography (EMG) recording over the Zygomaticus Major muscle. Results showed that JA augments SFM in individuals with low compared with high autistic traits. These findings are in line with reports of reduced impact of JA on action imitation in individuals with ASC. Moreover, they suggest that investigating atypical interactions between empathic processes, instead of testing these processes individually, might be crucial to understanding the nature of social deficits in autism