Whose emotion is it? Perspective matters to understand brain-body interactions in emotions.

Feeling happy, or judging whether someone else is feeling happy are two distinct facets of emotions that nevertheless rely on similar physiological and neural activity. Differentiating between these two states, also called Self/Other distinction, is an essential aspect of empathy, but how exactly is it implemented? In non-emotional cognition, the transient neural response evoked at each heartbeat, or heartbeat evoked response (HER), indexes the self and signals Self/Other distinction. Here, using electroencephalography (n = 32), we probe whether HERs' role in Self/Other distinction extends also to emotion - a domain where brain-body interactions are particularly relevant. We asked participants to rate independently validated affective scenes, reporting either their own emotion (Self) or the emotion expressed by people in the scene (Other). During the visual cue indicating to adopt the Self or Other perspective, before the affective scene, HERs distinguished between the two conditions, in visual cortices as well as in the right frontal operculum. Physiological reactivity (facial electromyogram, skin conductance, heart rate) during affective scene co-varied as expected with valence and arousal ratings, but also with the Self- or Other- perspective adopted. Finally, HERs contributed to the subjective experience of valence in the Self condition, in addition to and independently from physiological reactivity. We thus show that HERs represent a trans-domain marker of Self/Other distinction, here specifically contributing to experienced valence. We propose that HERs represent a form of evidence related to the 'I' part of the judgement 'To which extent do I feel happy'. The 'I' related evidence would be combined with the affective evidence collected during affective scene presentation, accounting at least partly for the difference between feeling an emotion and identifying it in someone else.

Neural correlates of interoceptive accuracy: Beyond cardioception.

Interoceptive accuracy (IAc), the precision with which one assesses the signals arising from one's own body, is receiving increasing attention in the literature. IAc has mainly been approached as an individual trait and has been investigated through the cardiac modality using mostly non-ecological methods. Such studies consensually designate the anterior insular cortex as the main brain correlate of IAc. However, there is a lack of brain imaging studies investigating IAc in a broader and more ecological way. Here, we used a novel ecological task in which participants monitored their general bodily reactions to external events and investigated brain regions subtending intraindividual (i.e. trial-by-trial) variations of IAc. At each trial, participants had to rate the intensity of their bodily reactions to an emotional picture. We recorded participants' skin conductance response (SCR) to the picture as an indicator of actual physiological response intensity. We fitted a functional magnetic resonance imaging (fMRI) model using, as regressors, the SCR value, the rating and the product of the two (as a proxy of participants' IAc) obtained trial per trial. We observed that activity in the dorsomedial prefrontal cortex (dmPFC) increased when individuals' IAc decreased. This result reveals general mechanism of error processing in intraindividual variations of IAc, which are unspecific to interoception. Our result has a practical impact in the clinical domain. Namely, it supports the predictive coding framework whereby IAc deficits may reflect impairments in processing a mismatch between actual interoceptive signals and predictions.

Rapid approach-avoidance responses to emotional displays reflect value-based decisions: Neural evidence from an EEG study.

The ability to swiftly and accurately respond to others' non-verbal signals, such as their emotional expressions, constitutes one of the building blocks for social adaptation. It is debated whether rapid action tendencies to socio-emotional signals solely depend upon stimulus-evoked pre-decisional motor bias or can also engage goal-directed (decisional) processes that involve the arbitration between action alternatives. Here, we used drift diffusion models (DDMs) of choice and electroencephalography (EEG) to investigate the impact of threat-signaling individuals (angry or fearful) on spontaneous approach-avoidance decisions. Participants choose to avoid angry individuals more often than fearful ones and this effect was stronger for intense expressions. Diffusion models showed that this pattern of choice was accounted for by a process of value-based evidence accumulation, suggesting an active competition between action options. At the brain level, we found that EEG activity preceding movement initiation (200 ms) in a mid-frontal cluster of electrodes - sourced in the orbital and ventromedial frontal cortices - encoded value difference between chosen and unchosen options, thus predicting participant's choices on a trial-by-trial basis. Furthermore, value difference also modulated EEG signal during feedback about the decision. Altogether, the present findings convincingly support the underestimated influence of implicit goal-directed mechanisms in approach-avoidance responses to socio-emotional signals.

Minimal group membership biases early neural processing of emotional expressions.

Mere affiliation with a social group alters people's perception of other individuals. One suggested mechanism behind such influence is that group membership triggers divergent visual facial representations for in-group and out-group members, which could constrain face processing. Here, using electroencephalography (EEG) under functional magnetic resonance imagery (fMRI) during a group categorization task, we investigated the impact of mere affiliation to an arbitrary group on the processing of emotional faces. The results indicate that in- and out-group members trigger differential event-related potential activity, appearing 150 ms after presentation of group membership information, which correlated with medial prefrontal fMRI activity. Additionally, EEG activity in the earliest stages of face processing (30-100 ms after expression onset) dissociated unexpected group-related emotions (in-group anger and out-group joy) from expected ones and correlated with temporo-parietal junction fMRI activity. We discuss the possibility that such dissociation may result from top-down influences from divergent representations for in-group and out-group members. Taken together, the present results suggest that mere membership in an arbitrary group polarized expectations which constrain the first steps of face processing.

Selective attention effects on early integration of social signals: same timing, modulated neural sources.

Humans combine co-emitted social signals to predict other's immediate intentions and prepare an adapted response. However, little is known about whether attending to only one of co-emitted social signals impacts on its combination with other signals. Here, using electroencephalography, we address selective attention effects on early combination of social signals. We manipulated three visual cues: gaze direction, emotional expression, and pointing gesture, while participants performed either emotion or gaze direction judgments. Results showed that a temporal marker of social cues integration emerges 170ms after the stimulus onset, even if the integration of the three visual cues was not required to perform the task, as only one feature at a time was task relevant. Yet in addition to common temporal regions, the relative contribution of specific neural sources of this integration changed as a function of the attended feature: integration during emotion judgments was mainly implemented in classic limbic areas but in the dorsal pathway during gaze direction judgments. Together, these findings demonstrate that co-emitted social cues are integrated as long as they are relevant to the observer, even when they are irrelevant to the ongoing task.

A direct amygdala-motor pathway for emotional displays to influence action: A diffusion tensor imaging study.

An important evolutionary function of emotions is to prime individuals for action. Although functional neuroimaging has provided evidence for such a relationship, little is known about the anatomical substrates allowing the limbic system to influence cortical motor-related areas. Using diffusion-weighted magnetic resonance imaging and probabilistic tractography on a cohort of 40 participants, we provide evidence of a structural connection between the amygdala and motor-related areas (lateral and medial precentral, motor cingulate and primary motor cortices, and postcentral gyrus) in humans. We then compare this connection with the connections of the amygdala with emotion-related brain areas (superior temporal sulcus, fusiform gyrus, orbitofrontal cortex, and lateral inferior frontal gyrus) and determine which amygdala nuclei are at the origin of these projections. Beyond the well-known subcortical influences over automatic and stereotypical emotional behaviors, a direct amygdala-motor pathway might provide a mechanism by which the amygdala can influence more complex motor behaviors.

Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1).

Patients with striate cortex damage and clinical blindness retain the ability to process certain visual properties of stimuli that they are not aware of seeing. Here we investigated the neural correlates of residual visual perception for dynamic whole-body emotional actions. Angry and neutral emotional whole-body actions were presented in the intact and blind visual hemifield of a cortically blind patient with unilateral destruction of striate cortex. Comparisons of angry vs. neutral actions performed separately in the blind and intact visual hemifield showed in both cases increased activation in primary somatosensory, motor, and premotor cortices. Activations selective for intact hemifield presentation of angry compared with neutral actions were located subcortically in the right lateral geniculate nucleus and cortically in the superior temporal sulcus, prefrontal cortex, precuneus, and intraparietal sulcus. Activations specific for blind hemifield presentation of angry compared with neutral actions were found in the bilateral superior colliculus, pulvinar nucleus of the thalamus, amygdala, and right fusiform gyrus. Direct comparison of emotional modulation in the blind vs. intact visual hemifield revealed selective activity in the right superior colliculus and bilateral pulvinar for angry expressions, thereby showing a selective involvement of these subcortical structures in nonconscious visual emotion perception.

Spontaneous instrumental approach-avoidance learning in social contexts in autism.

BACKGROUND: Individuals with Autism Spectrum Condition (ASC) are characterized by atypicalities in social interactions, compared to Typically Developing individuals (TD). The social motivation theory posits that these difficulties stem from diminished anticipation, reception, and/or learning from social rewards. Although learning from socioemotional outcomes is core to the theory, studies to date have been sparse and inconsistent. This possibly arises from a combination of theoretical, methodological and sample-related issues. Here, we assessed participants' ability to develop a spontaneous preference for actions that lead to desirable socioemotional outcomes (approaching/avoiding of happy/angry individuals, respectively), in an ecologically valid social scenario. We expected that learning abilities would be impaired in ASC individuals, particularly in response to affiliative social feedback. METHOD: We ran an online social reinforcement learning task, on two large online cohorts with (n = 274) and without (n = 290) ASC, matched for gender, age and education. Participants had to indicate where they would sit in a waiting room. Each seat was associated with different probabilities of approaching/avoiding emotional individuals. Importantly, the task was implicit, as participants were not instructed to learn, and emotional expressions were never mentioned. We applied both categorical analyses contrasting the ASC and TD groups and dimensional factor analysis on affective questionnaires. RESULTS: Contrary to our hypothesis, participants showed spontaneous learning from socioemotional outcomes, regardless of their diagnostic group. Yet, when accounting for dimensional variations in autistic traits, as well as depression and anxiety, two main findings emerged among females who failed to develop explicit learning strategies: (1) autism severity in ASC correlated with reduced learning to approach happy individuals; (2) anxiety-depression severity across both ASC and TD participants correlated with reduced learning to approach/avoid happy/angry individuals, respectively. CONCLUSIONS: Implicit spontaneous learning from socioemotional outcomes is not generally impaired in autism but may be specifically associated with autism severity in females with ASC, when they do not have an explicit strategy for adapting to their social environment. Clinical diagnosis and intervention ought to take into account individual differences in their full complexity, including the presence of co-morbid anxiety and depression, when dealing with social atypicalities in autism.

Early binding of gaze, gesture, and emotion: neural time course and correlates.

Communicative intentions are transmitted by many perceptual cues, including gaze direction, body gesture, and facial expressions. However, little is known about how these visual social cues are integrated over time in the brain and, notably, whether this binding occurs in the emotional or the motor system. By coupling magnetic resonance and electroencephalography imaging in humans, we were able to show that, 200 ms after stimulus onset, the premotor cortex integrated gaze, gesture, and emotion displayed by a congener. At earlier stages, emotional content was processed independently in the amygdala (170 ms), whereas directional cues (gaze direction with pointing gesture) were combined at ∼190 ms in the parietal and supplementary motor cortices. These results demonstrate that the early binding of visual social signals displayed by an agent engaged the dorsal pathway and the premotor cortex, possibly to facilitate the preparation of an adaptive response to another person's immediate intention.

Threat prompts defensive brain responses independently of attentional control.

Negative emotional signals are known to influence task performance, but so far, investigations have focused on how emotion interacts with perceptual processes by mobilizing attentional resources. The attention-independent effects of negative emotional signals are less well understood. Here, we show that threat signals trigger defensive responses independently of what observers pay attention to. Participants were scanned using functional magnetic resonance imaging while watching short video clips of threatening actions and performed either color or emotion judgments. Seeing threatening actions interfered with performance in both tasks. Amygdala activation reflected both stimulus and task conditions. In contrast, threat stimuli prompted a constant activity in a network underlying reflexive defensive behavior (periaqueductal gray, hypothalamus, and premotor cortex). Threat stimuli also disrupted ongoing behavior and provoked motor conflict in prefrontal regions during both tasks. The present results are consistent with the view that emotions trigger adaptive action tendencies independently of task settings.

Social affordances: is the mirror neuron system involved?

We question the idea that the mirror neuron system is the substrate of social affordances perception, and we suggest that most of the activity seen in the parietal and premotor cortex of the human brain is independent of mirroring activity as characterized in macaques, but rather reflects a process of one's own action specification in response to social signals.

Power pose effects on approach and avoidance decisions in response to social threat.

Individuals' opportunities for action in threatening social contexts largely depend on their social power. While powerful individuals can afford to confront aggressors and dangers, powerless individuals need others' support and better avoid direct challenges. Here, we investigated if adopting expansive or contracted poses, which signal dominance and submission, impacts individuals' approach and avoidance decisions in response to social threat signals using a within-subject design. Overall, participants more often chose to avoid rather than to approach angry individuals, but showed no clear approach or avoidance preference for fearful individuals. Crucially, contracted poses considerably increased the tendency to avoid angry individuals, whereas expansive poses induced no substantial changes. This suggests that adopting power-related poses may impact action decisions in response to social threat signals. The present results emphasize the social function of power poses, but should be replicated before drawing strong conclusions.

Prioritization of danger-related social signals during threat-induced anxiety.

Under threat, the combinations of fearful display and gaze orientation emitted by others can provide crucial information about the presence and location of the danger, as well as whether other individuals are in distress and need help. While it has been shown that threat-induced anxiety facilitates the processing of fearful faces, the question remains as to whether the processing of one of the two combinations of fearful displays and gaze direction (signaling danger vs. need for help) is prioritized within a threatening environment. To address this question, we ran two experiments. In a first online experiment, we showed that fearful displays associated with averted and direct gaze are appraised as preferentially signaling danger and need for help, respectively. In a second experiment, participants performed a fear categorization task (neutral vs. fear faces), manipulating gaze direction and intensity levels of facial expressions, under two alternating contexts: one involving exposure to unpredictable distress screams (threat condition) and the other being a nonthreat control condition. In threat blocks, participants had a higher tendency to interpret averted faces as expressing fear. Drift-diffusion analyses revealed that this resulted from the combined increase in drift rate and threshold. Our findings showed that threat-induced anxiety leads to prioritized processing of averted over direct fearful facial displays, assigning processing priority to social signals that convey information about the presence and location of potential danger. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Depression and approach-avoidance decisions to emotional displays: The role of anhedonia.

Depression is linked to dysfunctional appetitive and aversive motivational systems and effort-based decision-making, yet whether such deficits extend to social decisions remains unclear. Participants (23 non-depressed, 48 depressed - 24 with a past history of suicide attempt) completed a social decision-making task consisting in freely choosing whether to approach or avoid individuals displaying happy or angry expressions. Occasionally, participants had to make a further effort (change button press) to obtain the desired outcome. All participants preferentially avoided anger on their first choice. Yet, depressed patients less often chose to approach happy individuals, as a function of anhedonia severity. Depressed patients were also less inclined than controls to change their response when the anticipated outcome of their first choice was undesirable (approach angry and avoid happy). Again, such effect correlated with anhedonia severity. Our results support that both altered valuation and willingness to exert effort impact approach-avoidance decisions in social contexts in depression. On this basis, we propose a new integrating framework for reconciling different hypotheses on the effect of depression and anhedonia on motivational responses to emotional stimuli.

Look at me, I'll remember you: the perception of self-relevant social cues enhances memory and right hippocampal activity.

Being looked at by a person enhances the subsequent memorability of her/his identity. Here, we tested the specificity of this effect and its underlying brain processes. We manipulated three social cues displayed by an agent: Gaze Direction (Direct/Averted), Emotional Expression (Anger/Neutral), and Pointing gesture (Presence/Absence). Our behavioral experiment showed that direct as compared with averted gaze perception enhanced subsequent retrieval of face identity. Similar effect of enhanced retrieval was found when pointing finger was absent as compared with present but not for anger as compared with neutral expression. The fMRI results revealed amygdala activity for both Anger and Direct gaze conditions, suggesting emotional arousal. Yet, the right hippocampus, known to play a role in self-relevant memory processes, was only revealed during direct gaze perception. Further investigations suggest that right hippocampal activity was maximal for the most self-relevant social event (i.e. actor expressing anger and pointing toward the participant with direct gaze). Altogether, our results suggest that the perception of self-relevant social cues such as direct gaze automatically prompts "self-relevant memory" processes.

Spontaneous instrumental avoidance learning in social contexts.

Adaptation to our social environment requires learning how to avoid potentially harmful situations, such as encounters with aggressive individuals. Threatening facial expressions can evoke automatic stimulus-driven reactions, but whether their aversive motivational value suffices to drive instrumental active avoidance remains unclear. When asked to freely choose between different action alternatives, participants spontaneously-without instruction or monetary reward-developed a preference for choices that maximized the probability of avoiding angry individuals (sitting away from them in a waiting room). Most participants showed clear behavioral signs of instrumental learning, even in the absence of an explicit avoidance strategy. Inter-individual variability in learning depended on participants' subjective evaluations and sensitivity to threat approach feedback. Counterfactual learning best accounted for avoidance behaviors, especially in participants who developed an explicit avoidance strategy. Our results demonstrate that implicit defensive behaviors in social contexts are likely the product of several learning processes, including instrumental learning.

Action co-representation under threat: A Social Simon study.

Several studies have shown that individuals automatically integrate the actions of other individuals into their own action plans, thus facilitating action coordination. What happens to this mechanism in situations of danger? This capacity could either be reduced, in order to allocate more cognitive resources for individualistic actions, or be maintained or enhanced to enable cooperation under threat. In order to determine the impact of the perception of danger on this capacity, two groups of participants carried out, in pairs, the Social Simon task, which provides a measure of co-representation. The task was performed during so-called 'threat blocks' (during which participants could be exposed at any time to an aversive stimulus) and so-called 'safety blocks' (during which no aversive stimulation could occur). In a first group of participants, both individuals were exposed at the same time to threat blocks. In a second group, only one of the two participants was exposed to them at a time. Our results indicate that co-representation, an important cognitive mechanism for cooperation, (i) is preserved in situations of danger; and (ii) may even be increased in participants who are confronted alone to threat but in the presence of a safe partner. Contrarily to popular belief, danger does not shut down our capacities for social interaction.

Nature and determinants of social actions during a mass shooting.

Reactions to danger have been depicted as antisocial but research has shown that supportive behaviors (e.g., helping injured others, giving information or reassuring others) prevail in life-threatening circumstances. Why is it so? Previous accounts have put the emphasis on the role of psychosocial factors, such as the maintenance of social norms or the degree of identification between hostages. Other determinants, such as the possibility to escape and distance to danger may also greatly contribute to shaping people's reactions to deadly danger. To examine the role of those specific physical constraints, we interviewed 32 survivors of the attacks at 'Le Bataclan' (on the evening of 13-11-2015 in Paris, France). Consistent with previous findings, supportive behaviors were frequently reported. We also found that impossibility to egress, minimal protection from danger and interpersonal closeness with other crowd members were associated with higher report of supportive behaviors. As we delved into the motives behind reported supportive behaviors, we found that they were mostly described as manifesting cooperative (benefits for both interactants) or altruistic (benefits for other(s) at cost for oneself) tendencies, rather than individualistic (benefits for oneself at cost for other(s)) ones. Our results show that supportive behaviors occur during mass shootings, particularly if people cannot escape, are under minimal protection from the danger, and feel interpersonal closeness with others. Crucially, supportive behaviors underpin a diversity of motives. This last finding calls for a clear-cut distinction between the social strategies people use when exposed to deadly danger, and the psychological motivations underlying them.

Impact of total sleep deprivation and related mood changes on approach-avoidance decisions to threat-related facial displays.

STUDY OBJECTIVES: Total sleep deprivation is known to have significant detrimental effects on cognitive and socio-emotional functioning. Nonetheless, the mechanisms by which total sleep loss disturbs decision-making in social contexts are poorly understood. Here, we investigated the impact of total sleep deprivation on approach/avoidance decisions when faced with threatening individuals, as well as the potential moderating role of sleep-related mood changes. METHODS: Participants (n = 34) made spontaneous approach/avoidance decisions in the presence of task-irrelevant angry or fearful individuals, while rested or totally sleep deprived (27 h of continuous wakefulness). Sleep-related changes in mood and sustained attention were assessed using the Positive and Negative Affective Scale and the psychomotor vigilance task, respectively. RESULTS: Rested participants avoided both fearful and angry individuals, with stronger avoidance for angry individuals, in line with previous results. On the contrary, totally sleep deprived participants favored neither approach nor avoidance of fearful individuals, while they still comparably avoided angry individuals. Drift-diffusion models showed that this effect was accounted for by the fact that total sleep deprivation reduced value-based evidence accumulation toward avoidance during decision making. Finally, the reduction of positive mood after total sleep deprivation positively correlated with the reduction of fearful display avoidance. Importantly, this correlation was not mediated by a sleep-related reduction in sustained attention. CONCLUSIONS: All together, these findings support the underestimated role of positive mood-state alterations caused by total sleep loss on approach/avoidance decisions when facing ambiguous socio-emotional displays, such as fear.

Individual differences in socioaffective skills influence the neural bases of fear processing: the case of alexithymia.

Being exposed to fear signals makes us feel threatened and prompts us to prepare an adaptive response. In our previous studies, we suggested that amygdala (AMG) and premotor cortex (PM) play a role in the preparation of the observers' motor response required by the situation. The present experiment aimed at assessing how interindividual differences in alexithymia--a personality trait associated with deficits in emotional reactivity and regulation--influence the neural network associated with the perception of fear. Using fMRI, we scanned 34 healthy subjects while they were passively observing fearful body expressions. Applying a dimensional approach, we performed correlation analyses between fear-related brain areas and alexithymia scores among all participants. Using a categorical approach, we conducted a between-group comparison (13 high vs. 12 low-alexithymia subjects). Our results were threefold. First, the right AMG activity in response to fearful stimuli was negatively correlated with the level of difficulty to identify emotions. Second, PM activity was linked to reduced subjective emotional reactivity. Third, the between-group comparison revealed greater activity in anterior cingulate cortex (ACC) for high than low-alexithymia scorers. Moreover, the relationship between ACC and PM was in opposite direction in individuals with high (negative link) and low (positive link) alexithymia. Therefore, compared to our previous findings, we hereby further reveal how ACC interacts with PM to sustain self-regulation of one's own emotional state in response to threatening social signals. Moreover, this neural mechanism could account for the description of the "cold-blooded" personality of individuals with alexithymia.