The effects of self-involvement on attention, arousal, and facial expression during social interaction with virtual others: a psychophysiological study

Social neuroscience has shed light on the underpinnings of understanding other minds. The current study investigated the effect of self-involvement during social interaction on attention, arousal, and facial expression. Specifically, we sought to disentangle the effect of being personally addressed from the effect of decoding the meaning of another person's facial expression. To this end, eye movements, pupil size, and facial electromyographic (EMG) activity were recorded while participants observed virtual characters gazing at them or looking at someone else. In dynamic animations, the virtual characters then displayed either socially relevant facial expressions (similar to those used in everyday life situations to establish interpersonal contact) or arbitrary facial movements. The results show that attention allocation, as assessed by eye-tracking measurements, was specifically related to self-involvement regardless of the social meaning being conveyed. Arousal, as measured by pupil size, was primarily related to perceiving the virtual character's gender. In contrast, facial EMG activity was determined by the perception of socially relevant facial expressions irrespective of whom these were directed towards.     

Being with virtual others: studying social cognition in temporal lobe epilepsy

Social cognitive neuroscience has highlighted the importance of frontotemporal neurocircuitry for social cognition. Temporal lobe epilepsy (TLE) impacts these brain areas and their functional connections and might therefore specifically affect social perceptual and cognitive skills. In the study described here, an established paradigm was used to evaluate the social cognitive skills of female patients with left TLE. Study participants were shown dynamic animations in which virtual characters either looked at the human observer directly or looked away toward someone else, thus manipulating self-involvement. The virtual characters then exhibited different facial expressions that were either socially relevant or arbitrary. Participants were asked to rate the communicative intentions of the virtual character. Patients' ratings of communicative intent appeared to be linked to their own self-involvement in the interaction, whereas healthy volunteers' ratings of facial expressions were independent of self-involvement. Potential mechanisms for the observed differences are discussed.     

Anticipating control over aversive stimuli is mediated by the medial prefrontal cortex: An fMRI study with healthy adults

The anticipation of control over aversive events in life is relevant for our mental health. Insights on the underlying neural mechanisms remain limited. We developed a new functional magnetic resonance imaging (fMRI) task that uses auditory stimuli to explore the neural correlates of (1) the anticipation of control over aversion and (2) the processing of aversion. In a sample of 25 healthy adults, we observed increased neural activation in the medial prefrontal cortex (ventromedial prefrontal cortex and rostral anterior cingulate cortex), other brain areas relevant for reward anticipation (ventral striatum, brainstem [ventral tegmental area], midcingulate cortex), and the posterior cingulate cortex when they anticipated control over aversion compared with anticipating no control (1). The processing of aversive sounds compared to neutral sounds (2) was associated with increased neural activation in the bilateral posterior insula. Our findings provide evidence for the important role of medial prefrontal regions in control anticipation and highlight the relevance of conceiving the neural mechanisms involved within a reward‐based framework.     

Loss of dopamine terminals in the medial prefrontal cortex increased the ratio of DOPAC to DA in tissue of the nucleus accumbens shell: role of stress

We examined whether dopamine depletion in the medial prefrontal cortex of the rat differentially affects basal and evoked dopamine and 3,4-dihydroxyphenylacetic acid (DOPAC) content in the subareas of the neostriatum and nucleus accumbens. Loss of ≈80% of tissue dopamine content in the medial prefrontal cortex did not significantly alter basal tissue concentrations of dopamine or DOPAC or the DOPAC : dopamine ratio in either the nucleus accumbens core or shell or the medial or lateral neostriatum. However, tail pressure stress significantly increased the DOPAC : dopamine ratio in the nucleus accumbens shell of lesioned rats. Because dorsal and ventral areas of the medial prefrontal cortex preferentially innervate the core and shell, respectively, we sought to determine whether the selective effect of lesions on dopamine terminals in the shell of the nucleus accumbens are paralleled by greater dopamine loss in the ventral medial prefrontal cortex. 6-Hydroxydopamine decreased tissue concentrations of dopamine in both the dorsal (−74%) and ventral medial prefrontal cortex (−68%). In lesioned rats, few tyrosine hydroxylase-immunoreactive fibers remained in the dorsal medial prefrontal cortex whereas a dense innervation remained in the ventralmost area. The present data suggest that the influence of mesocortical dopamine neurons on the dopamine projection to the nucleus accumbens shell is expressed only under conditions of stress. Furthermore, lesion-induced alterations in dopamine neurons projecting to the nucleus accumbens shell are not due to a more extensive loss of dopamine terminals in the ventral than in the dorsal medial prefrontal cortex.     

Adolescent gain in positive valence of a socially relevant stimulus: engagement of the mesocorticolimbic reward circuitry

A successful transition from childhood to adulthood requires adolescent maturation of social information processing. The neurobiological underpinnings of this maturational process remain elusive. This research employed the male Syrian hamster as a tractable animal model for investigating the neural circuitry involved in this critical transition. In this species, adult and juvenile males display different behavioral and neural responses to vaginal secretions, which contain pheromones essential for expression of sexual behavior in adulthood. These studies tested the hypothesis that vaginal secretions acquire positive valence over adolescent development via remodeling of neural circuits underlying sexual reward. Sexually naïve adult, but not juvenile, hamsters showed a conditioned place preference for vaginal secretions. Differences in behavioral response to vaginal secretions between juveniles and adults correlated with a difference in the vaginal secretion‐induced neural activation pattern in mesocorticolimbic reward circuitry. Fos immunoreactivity increased in response to vaginal secretions in the medial amygdala and ventral tegmental dopaminergic cells of both juvenile and adult males. However, only in adults was there a Fos response to vaginal secretions in non‐dopaminergic cells in interfascicular ventral tegmental area, nucleus accumbens core and infralimbic medial prefrontal cortex. These results demonstrate that a socially relevant chemosensory stimulus acquires the status of an unconditioned reward during adolescence, and that this adolescent gain in social reward is correlated with experience‐independent engagement of specific cell groups in reward circuitry.     

What's in a smile? Neural correlates of facial embodiment during social interaction

Abstract

Previous investigations have shown that the perception of socially relevant facial expressions, indicating someone else's intention to communicate (e.g., smiling), correlate with increased activity in zygomaticus major muscle regardless of whether the facial expressions seen are directed towards the human observer or toward someone else (Mojzisch et al., 2006). These spontaneous, involuntary reactions have been described as facial mimicry and seem to be of considerable importance for successful interpersonal communication. We investigated whether specific neural substrates underlie these responses by performing a finite impulse response (FIR) analysis of an experiment using functional magnetic resonance imaging (fMRI) to investigate the perception of socially relevant facial expressions (Schilbach et al., 2006). This analysis demonstrates that differential neural activity can be detected relative to the FIR time window in which facial mimicry occurs. The neural network found includes but extends beyond classical motor regions (face motor area) recruiting brain regions known to be involved in social cognition. This network is proposed to subserve the integration of emotional and action-related processes as part of a pre-reflective, embodied reaction to the perception of socially relevant facial expressions as well as a reflective representation of self and other.     

Contextual modulation of amygdala responsivity to surprised faces

We recently demonstrated a functional relationship between fMRI responses within the amygdala and the medial prefrontal cortex based upon whether subjects interpreted surprised facial expressions positively or negatively. In the present fMRI study, we sought to assess amygdala-medial prefrontal cortex responsivity when the interpretations of surprised faces were determined by contextual experimental stimuli, rather than subjective judgment. Subjects passively viewed individual presentations of surprised faces preceded by either a negatively or positively valenced contextual sentence (e. g., She just found $500 vs. She just lost $500). Negative and positive sentences were carefully matched in terms of length, situations described, and arousal level. Negatively cued surprised faces produced greater ventral amygdala activation compared to positively cued surprised faces. Responses to negative versus positive sentences were greater within the ventrolateral prefrontal cortex, whereas responses to positive versus negative sentences were greater within the ventromedial prefrontal cortex. The present study demonstrates that amygdala response to surprised facial expressions can be modulated by negatively versus positively valenced verbal contextual information. Connectivity analyses identified candidate cortical-subcortical systems subserving this modulation.     

What's in a smile? Neural correlates of facial embodiment during social interaction

Previous investigations have shown that the perception of socially relevant facial expressions, indicating someone else's intention to communicate (e.g., smiling), correlate with increased activity in zygomaticus major muscle regardless of whether the facial expressions seen are directed towards the human observer or toward someone else (Mojzisch et al., 2006). These spontaneous, involuntary reactions have been described as facial mimicry and seem to be of considerable importance for successful interpersonal communication. We investigated whether specific neural substrates underlie these responses by performing a finite impulse response (FIR) analysis of an experiment using functional magnetic resonance imaging (fMRI) to investigate the perception of socially relevant facial expressions (Schilbach et al., 2006). This analysis demonstrates that differential neural activity can be detected relative to the FIR time window in which facial mimicry occurs. The neural network found includes but extends beyond classical motor regions (face motor area) recruiting brain regions known to be involved in social cognition. This network is proposed to subserve the integration of emotional and action-related processes as part of a pre-reflective, embodied reaction to the perception of socially relevant facial expressions as well as a reflective representation of self and other.     

Age‐related changes in amygdala–frontal connectivity during emotional face processing from childhood into young adulthood

The ability to process and respond to emotional facial expressions is a critical skill for healthy social and emotional development. There has been growing interest in understanding the neural circuitry underlying development of emotional processing, with previous research implicating functional connectivity between amygdala and frontal regions. However, existing work has focused on threatening emotional faces, raising questions regarding the extent to which these developmental patterns are specific to threat or to emotional face processing more broadly. In the current study, we examined age‐related changes in brain activity and amygdala functional connectivity during an fMRI emotional face matching task (including angry, fearful, and happy faces) in 61 healthy subjects aged 7–25 years. We found age‐related decreases in ventral medial prefrontal cortex activity in response to happy faces but not to angry or fearful faces, and an age‐related change (shifting from positive to negative correlation) in amygdala–anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC) functional connectivity to all emotional faces. Specifically, positive correlations between amygdala and ACC/mPFC in children changed to negative correlations in adults, which may suggest early emergence of bottom‐up amygdala excitatory signaling to ACC/mPFC in children and later development of top‐down inhibitory control of ACC/mPFC over amygdala in adults. Age‐related changes in amygdala–ACC/mPFC connectivity did not vary for processing of different facial emotions, suggesting changes in amygdala–ACC/mPFC connectivity may underlie development of broad emotional processing, rather than threat‐specific processing. Hum Brain Mapp 37:1684–1695, 2016. © 2016 Wiley Periodicals, Inc .     

Functional disconnections in the direct and indirect amygdala pathways for fear processing in schizophrenia

BACKGROUND: Schizophrenia patients show reduced neural activity, relative to controls, in the amygdala and its projection to the medial prefrontal cortex (MPFC) in response to fear perception. In this study we tested the hypothesis that schizophrenia is characterized by abnormal functional connectivity in the amygdala network underlying fear perception. METHODS: Functional MRI images were acquired from 14 schizophrenia patients and 14 matched healthy control subjects during an emotion perception task, in which fearful and neutral facial expression stimuli were presented pseudorandomly under nonconscious (using masking) and conscious conditions. Both subtraction and functional connectivity analyses were undertaken using a region of interest approach. RESULTS: In response to fearful facial expressions, schizophrenia patients displayed reduced amygdala activity, compared to controls, in both the conscious and nonconscious conditions. The amygdala displayed a reversal of the normal pattern of connectivity with the brainstem, visual cortex, and also with the dorsal and ventral divisions of the MPFC in the schizophrenia patients. CONCLUSIONS: The presence of functional disconnections in amygdala pathways suggests that schizophrenia patients have a failure in coordinating their automatic orienting to salient signals and the associated prefrontal monitoring of these signals.     

Neural correlates of anticipation and processing of performance feedback in social anxiety

Fear of negative evaluation, such as negative social performance feedback, is the core symptom of social anxiety. The present study investigated the neural correlates of anticipation and perception of social performance feedback in social anxiety. High (HSA) and low (LSA) socially anxious individuals were asked to give a speech on a personally relevant topic and received standardized but appropriate expert performance feedback in a succeeding experimental session in which neural activity was measured during anticipation and presentation of negative and positive performance feedback concerning the speech performance, or a neutral feedback‐unrelated control condition. HSA compared to LSA subjects reported greater anxiety during anticipation of negative feedback. Functional magnetic resonance imaging results showed deactivation of medial prefrontal brain areas during anticipation of negative feedback relative to the control and the positive condition, and medial prefrontal and insular hyperactivation during presentation of negative as well as positive feedback in HSA compared to LSA subjects. The results indicate distinct processes underlying feedback processing during anticipation and presentation of feedback in HSA as compared to LSA individuals. In line with the role of the medial prefrontal cortex in self‐referential information processing and the insula in interoception, social anxiety seems to be associated with lower self‐monitoring during feedback anticipation, and an increased self‐focus and interoception during feedback presentation, regardless of feedback valence. Hum Brain Mapp 35:6023–6031, 2014. © 2014 Wiley Periodicals, Inc.     

Impairment of social perception associated with lesions of the prefrontal cortex

OBJECTIVE: Behavioral and social impairments have been frequently reported after damage to the prefrontal cortex in humans. This study evaluated social perception in patients with prefrontal cortex lesions and compared their performance on a social perception task with that of healthy volunteers. METHOD: Thirty-three patients with prefrontal cortex lesions and 31 healthy volunteers were tested with the Interpersonal Perception Task. In this task, subjects viewed videotaped social interactions and relied primarily on nonverbal cues to make interpersonal judgments, such as determining the degree of intimacy between two persons depicted in the videotaped scene. Patients with prefrontal cortex lesions were classified according to lesion involvement of specific regions, including the orbitofrontal cortex, dorsolateral prefrontal cortex, and anterior cingulate cortex. RESULTS: Relative to the comparison subjects, patients whose lesions involved the orbitofrontal cortex demonstrated impaired social perception. Contrary to predictions, patients with lesions in the dorsolateral prefrontal cortex also showed deficits in using social cues to make interpersonal judgments. All patients, particularly those with lesions in the dorsolateral prefrontal cortex, showed poorer insight into their deficits, relative to healthy volunteers. CONCLUSIONS: These findings of deficits in social perception after damage to the orbitofrontal cortex extend previous clinical and experimental evidence of damage-related impairment in other aspects of social cognition, such as the ability to accurately evaluate emotional facial expressions. In addition, the results suggest that the dorsolateral prefrontal cortex is recruited when inferences about social interactions are made on the basis of nonverbal information.     

Neurodevelopmental changes across adolescence in viewing and labeling dynamic peer emotions

Adolescence is a sensitive period of social-affective development, characterized by biological, neurological, and social changes. The field currently conceptualizes these changes in terms of an imbalance between systems supporting reactivity and regulation, specifically nonlinear changes in reactivity networks and linear changes in regulatory networks. Previous research suggests that the labeling or reappraisal of emotion increases activity in lateral prefrontal cortex (LPFC), and decreases activity in amygdala relative to passive viewing of affective stimuli. However, past work in this area has relied heavily on paradigms using static, adult faces, as well as explicit regulation. In the current study, we assessed cross-sectional trends in neural responses to viewing and labeling dynamic peer emotional expressions in adolescent girls 10–23 years old. Our dynamic adolescent stimuli set reliably and robustly recruited key brain regions involved in emotion reactivity (medial orbital frontal cortex/ventral medial prefrontal cortex; MOFC/vMPFC, bilateral amygdala) and regulation (bilateral dorsal and ventral LPFC). However, contrary to the age-trends predicted by the dominant models in studies of risk/reward, the LPFC showed a nonlinear age trend across adolescence to labeling dynamic peer faces, whereas the MOFC/vMPFC showed a linear decrease with age to viewing dynamic peer faces. There were no significant age trends observed in the amygdala.     

Visual and spatial working memory: from boxes to networks

It is shown that visuo-spatial working memory is better characterized as processes operating on sensory information (visual appearance) and on spatial location (environmental coordinates) in a distributed network than as unitary slave system. Results from passive (short-term) and active memory tasks (imagery) disclose the properties (capacity, content) and the components of this network. The prefrontal cortex is a control structure (dorsal prefers active, ventral passive tasks) and it contributes to spatial memory by a prospective spatial code (eye movements). Visual appearance (including dynamic aspects) is represented as features and object files (bound features) within content-specific areas in the ventral occipital cortex. Spatial coordinates are represented in the parietal cortex (modality-unspecific), when used in spatio-temporal tasks (Corsi) they are closely related to attention. Imagery of objects activates occipito-temporal structures, spatial transformations and mental rotation the parietal cortex (specifically the intraparietal sulcus). Perception, working memory, and imagery use the same neural network. Differences between the tasks are explained by different demands and states of the neural network, and differences in the configuration of the anterior–posterior neural circuits.     

A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder

BACKGROUND: Previous functional neuroimaging studies have demonstrated exaggerated amygdala responses and diminished medial prefrontal cortex responses during the symptomatic state in posttraumatic stress disorder (PTSD). OBJECTIVES: To determine whether these abnormalities also occur in response to overtly presented affective stimuli unrelated to trauma; to examine the functional relationship between the amygdala and medial prefrontal cortex and their relationship to PTSD symptom severity in response to these stimuli; and to determine whether responsivity of these regions habituates normally across repeated stimulus presentations in PTSD. DESIGN: Case-control study. SETTING: Academic medical center. PARTICIPANTS: Volunteer sample of 13 men with PTSD (PTSD group) and 13 trauma-exposed men without PTSD (control group). MAIN OUTCOME MEASURES: We used functional magnetic resonance imaging (fMRI) to study blood oxygenation level-dependent signal during the presentation of emotional facial expressions. RESULTS: The PTSD group exhibited exaggerated amygdala responses and diminished medial prefrontal cortex responses to fearful vs happy facial expressions. In addition, in the PTSD group, blood oxygenation level-dependent signal changes in the amygdala were negatively correlated with signal changes in the medial prefrontal cortex, and symptom severity was negatively related to blood oxygenation level-dependent signal changes in the medial prefrontal cortex. Finally, relative to the control group, the PTSD group tended to exhibit diminished habituation of fearful vs happy responses in the right amygdala across functional runs, although this effect did not exceed our a priori statistical threshold. CONCLUSIONS: These results provide evidence for exaggerated amygdala responsivity, diminished medial prefrontal cortex responsivity, and a reciprocal relationship between these 2 regions during passive viewing of overtly presented affective stimuli unrelated to trauma in PTSD.     

Functional abnormalities of the default network during self- and other-reflection in autism

Recent studies of autism have identified functional abnormalities of the default network during a passive resting state. Since the default network is also typically engaged during social, emotional and introspective processing, dysfunction of this network may underlie some of the difficulties individuals with autism exhibit in these broad domains. In the present experiment, we attempted to further delineate the nature of default network abnormality in autism using experimentally constrained social and introspective tasks. Thirteen autism and 12 control participants were scanned while making true/false judgments for various statements about themselves (SELF condition) or a close other person (OTHER), and pertaining to either psychological personality traits (INTERNAL) or observable characteristics and behaviors (EXTERNAL). In the ventral medial prefrontal cortex/ventral anterior cingulate cortex, activity was reduced in the autism group across all judgment conditions and also during a resting condition, suggestive of task-independent dysfunction of this region. In other default network regions, overall levels of activity were not different between groups. Furthermore, in several of these regions, we found group by condition interactions only for INTERNAL/EXTERNAL judgments, and not SELF/OTHER judgments, suggestive of task-specific dysfunction. Overall, these results provide a more detailed view of default network functionality and abnormality in autism.     

Imitating expressions: emotion-specific neural substrates in facial mimicry

Intentionally adopting a discrete emotional facial expressioncan modulate the subjective feelings corresponding to that emotion;however, the underlying neural mechanism is poorly understood.We therefore used functional brain imaging (functional magneticresonance imaging) to examine brain activity during intentionalmimicry of emotional and non-emotional facial expressions andrelate regional responses to the magnitude of expression-inducedfacial movement. Eighteen healthy subjects were scanned whileimitating video clips depicting three emotional (sad, angry,happy), and two ‘ingestive’ (chewing and licking)facial expressions. Simultaneously, facial movement was monitoredfrom displacement of fiducial markers (highly reflective dots)on each subject's face. Imitating emotional expressions enhancedactivity within right inferior prefrontal cortex. This patternwas absent during passive viewing conditions. Moreover, themagnitude of facial movement during emotion-imitation predictedresponses within right insula and motor/premotor cortices. Enhancedactivity in ventromedial prefrontal cortex and frontal polewas observed during imitation of anger, in ventromedial prefrontaland rostral anterior cingulate during imitation of sadness andin striatal, amygdala and occipitotemporal during imitationof happiness. Our findings suggest a central role for rightinferior frontal gyrus in the intentional imitation of emotionalexpressions. Further, by entering metrics for facial muscularchange into analysis of brain imaging data, we highlight sharedand discrete neural substrates supporting affective, actionand social consequences of somatomotor emotional expression.     

The face of rejection: rejection sensitivity moderates dorsal anterior cingulate activity to disapproving facial expressions

Previous research has examined neural responses to threatening facial expressions such as those displaying anger, fear, and disgust. Here, we examined neural responses to a different type of threatening facial expression that primarily signifies a threat to social connection, namely a "disapproving" facial expression. We hypothesized that neural responses to disapproving facial expressions would be moderated by individual differences in rejection sensitivity. Using functional magnetic resonance imaging (fMRI), we scanned participants while they viewed brief video clips of facial expressions depicting disapproval, anger, and disgust. As expected, all three expressions yielded bilateral amygdala activation relative to a resting baseline. Additionally, individuals who scored higher on a measure of rejection sensitivity exhibited greater dorsal anterior cingulate cortex activity in response to disapproving facial expressions, but not in response to anger or disgust facial expressions. Results suggest that, at the neural level, individuals high in rejection sensitivity may be more sensitive to facial expressions signaling potential rejection, but not to threatening facial expressions in general. Results also suggest that disapproving facial expressions convey a distinct type of threat and should be considered in future studies of socially threatening facial expressions.