Specialized Networks for Social Cognition in the Primate Brain.

Primates have evolved diverse cognitive capabilities to navigate their complex social world. To understand how the brain implements critical social cognitive abilities, we describe functional specialization in the domains of face processing, social interaction understanding, and mental state attribution. Systems for face processing are specialized from the level of single cells to populations of neurons within brain regions to hierarchically organized networks that extract and represent abstract social information. Such functional specialization is not confined to the sensorimotor periphery but appears to be a pervasive theme of primate brain organization all the way to the apex regions of cortical hierarchies. Circuits processing social information are juxtaposed with parallel systems involved in processing nonsocial information, suggesting common computations applied to different domains. The emerging picture of the neural basis of social cognition is a set of distinct but interacting subnetworks involved in component processes such as face perception and social reasoning, traversing large parts of the primate brain.

The time course of person perception from voices in the brain.

When listeners hear a voice, they rapidly form a complex first impression of who the person behind that voice might be. We characterize how these multivariate first impressions from voices emerge over time across different levels of abstraction using electroencephalography and representational similarity analysis. We find that for eight perceived physical (gender, age, and health), trait (attractiveness, dominance, and trustworthiness), and social characteristics (educatedness and professionalism), representations emerge early (~80 ms after stimulus onset), with voice acoustics contributing to those representations between ~100 ms and 400 ms. While impressions of person characteristics are highly correlated, we can find evidence for highly abstracted, independent representations of individual person characteristics. These abstracted representationse merge gradually over time. That is, representations of physical characteristics (age, gender) arise early (from ~120 ms), while representations of some trait and social characteristics emerge later (~360 ms onward). The findings align with recent theoretical models and shed light on the computations underpinning person perception from voices.

The neuropeptide drosulfakinin enhances choosiness and protects males from the aging effects of social perception.

The motivation to reproduce is a potent natural drive, and the social behaviors that induce it can severely impact animal health and lifespan. Indeed, in Drosophila males, accelerated aging associated with reproduction arises not from the physical act of courtship or copulation but instead from the motivational drive to court and mate. To better understand the mechanisms underlying social effects on aging, we studied male choosiness for mates. We found that increased activity of insulin-producing cells (IPCs) of the fly brain potentiated choosiness without consistently affecting courtship activity. Surprisingly, this effect was not caused by insulins themselves, but instead by drosulfakinin (DSK), another neuropeptide produced in a subset of the IPCs, acting through one of the two DSK receptors, CCKLR-17D1. Activation of Dsk+ IPC neurons also decreased food consumption, while activation of Dsk+ neurons outside of IPCs affected neither choosiness nor feeding, suggesting an overlap between Dsk+neurons modulating choosiness and those influencing satiety. Broader activation of Dsk+ neurons (both within and outside of the IPCs) was required to rescue the detrimental effect of female pheromone exposure on male lifespan, as was the function of both DSK receptors. The same broad set of Dsk+ neurons was found to reinforce normally aversive feeding interactions, but only after exposure to female pheromones, suggesting that perception of the opposite sex gates rewarding properties of these neurons. We speculate that broad Dsk+ neuron activation is associated with states of satiety and social experience, which under stressful conditions is rewarding and beneficial for lifespan.

Hostile Attribution Bias Shapes Neural Synchrony in the Left Ventromedial Prefrontal Cortex during Ambiguous Social Narratives.

Hostile attribution bias refers to the tendency to interpret social situations as intentionally hostile. While previous research has focused on its developmental origins and behavioral consequences, the underlying neural mechanisms remain underexplored. Here, we employed functional near-infrared spectroscopy (fNIRS) to investigate the neural correlates of hostile attribution bias. While undergoing fNIRS, male and female participants listened to and provided attribution ratings for 21 hypothetical scenarios where a character's actions resulted in a negative outcome for the listener. Ratings of hostile intentions were averaged to measure hostile attribution bias. Using intersubject representational similarity analysis, we found that participants with similar levels of hostile attribution bias exhibited higher levels of neural synchrony during narrative listening, suggesting shared interpretations of the scenarios. This effect was localized to the left ventromedial prefrontal cortex (VMPFC) and was particularly prominent in scenarios where the character's intentions were highly ambiguous. We then grouped participants into high and low bias groups based on a median split of their hostile attribution bias scores. A similarity-based classifier trained on the neural data classified participants as having high or low bias with 75% accuracy, indicating that the neural time courses during narrative listening was systematically different between the two groups. Furthermore, hostile attribution bias correlated negatively with attributional complexity, a measure of one's tendency to consider multifaceted causes when explaining behavior. Our study sheds light on the neural mechanisms underlying hostile attribution bias and highlights the potential of using fNIRS to develop nonintrusive and cost-effective neural markers of this sociocognitive bias.

Neural Representations of Observed Interpersonal Synchrony/Asynchrony in the Social Perception Network.

The visual perception of individuals is thought to be mediated by a network of regions in the occipitotemporal cortex that supports specialized processing of faces, bodies, and actions. In comparison, we know relatively little about the neural mechanisms that support the perception of multiple individuals and the interactions between them. The present study sought to elucidate the visual processing of social interactions by identifying which regions of the social perception network represent interpersonal synchrony. In an fMRI study with 32 human participants (26 female, 6 male), we used multivoxel pattern analysis to investigate whether activity in face-selective, body-selective, and interaction-sensitive regions across the social perception network supports the decoding of synchronous versus asynchronous head-nodding and head-shaking. Several regions were found to support significant decoding of synchrony/asynchrony, including extrastriate body area (EBA), face-selective and interaction-sensitive mid/posterior right superior temporal sulcus, and occipital face area. We also saw robust cross-classification across actions in the EBA, suggestive of movement-invariant representations of synchrony/asynchrony. Exploratory whole-brain analyses also identified a region of the right fusiform cortex that responded more strongly to synchronous than to asynchronous motion. Critically, perceiving interpersonal synchrony/asynchrony requires the simultaneous extraction and integration of dynamic information from more than one person. Hence, the representation of synchrony/asynchrony cannot be attributed to augmented or additive processing of individual actors. Our findings therefore provide important new evidence that social interactions recruit dedicated visual processing within the social perception network that extends beyond that engaged by the faces and bodies of the constituent individuals.

Identifying interindividual variability of social perception and associated brain anatomical correlations in children with autism spectrum disorder using eye-tracking and diffusion tensor imaging MRI (DTI-MRI).

Even though deficits in social cognition constitute a core characteristic of autism spectrum disorders, a large heterogeneity exists regarding individual social performances and its neural basis remains poorly investigated. Here, we used eye-tracking to objectively measure interindividual variability in social perception and its correlation with white matter microstructure, measured with diffusion tensor imaging MRI, in 25 children with autism spectrum disorder (8.5 ± 3.8 years). Beyond confirming deficits in social perception in participants with autism spectrum disorder compared 24 typically developing controls (10.5 ± 2.9 years), results revealed a large interindividual variability of such behavior among individuals with autism spectrum disorder. Whole-brain analysis showed in both autism spectrum disorder and typically developing groups a positive correlation between number of fixations to the eyes and fractional anisotropy values mainly in right and left superior longitudinal tracts. In children with autism spectrum disorder a correlation was also observed in right and left inferior longitudinal tracts. Importantly, a significant interaction between group and number of fixations to the eyes was observed within the anterior portion of the right inferior longitudinal fasciculus, mainly in the right anterior temporal region. This additional correlation in a supplementary region suggests the existence of a compensatory brain mechanism, which may support enhanced performance in social perception among children with autism spectrum disorder.

A multimodal interface for speech perception: the role of the left superior temporal sulcus in social cognition and autism.

Multimodal integration is crucial for human interaction, in particular for social communication, which relies on integrating information from various sensory modalities. Recently a third visual pathway specialized in social perception was proposed, which includes the right superior temporal sulcus (STS) playing a key role in processing socially relevant cues and high-level social perception. Importantly, it has also recently been proposed that the left STS contributes to audiovisual integration of speech processing. In this article, we propose that brain areas along the right STS that support multimodal integration for social perception and cognition can be considered homologs to those in the left, language-dominant hemisphere, sustaining multimodal integration of speech and semantic concepts fundamental for social communication. Emphasizing the significance of the left STS in multimodal integration and associated processes such as multimodal attention to socially relevant stimuli, we underscore its potential relevance in comprehending neurodevelopmental conditions characterized by challenges in social communication such as autism spectrum disorder (ASD). Further research into this left lateral processing stream holds the promise of enhancing our understanding of social communication in both typical development and ASD, which may lead to more effective interventions that could improve the quality of life for individuals with atypical neurodevelopment.

Atypical neural encoding of faces in individuals with autism spectrum disorder.

Individuals with autism spectrum disorder (ASD) experience pervasive difficulties in processing social information from faces. However, the behavioral and neural mechanisms underlying social trait judgments of faces in ASD remain largely unclear. Here, we comprehensively addressed this question by employing functional neuroimaging and parametrically generated faces that vary in facial trustworthiness and dominance. Behaviorally, participants with ASD exhibited reduced specificity but increased inter-rater variability in social trait judgments. Neurally, participants with ASD showed hypo-activation across broad face-processing areas. Multivariate analysis based on trial-by-trial face responses could discriminate participant groups in the majority of the face-processing areas. Encoding social traits in ASD engaged vastly different face-processing areas compared to controls, and encoding different social traits engaged different brain areas. Interestingly, the idiosyncratic brain areas encoding social traits in ASD were still flexible and context-dependent, similar to neurotypicals. Additionally, participants with ASD also showed an altered encoding of facial saliency features in the eyes and mouth. Together, our results provide a comprehensive understanding of the neural mechanisms underlying social trait judgments in ASD.

Get out of my head: social evaluative brain states carry over into post-feedback rest and influence remembering how others view us.

Learning how others perceive us helps us tune our behavior to form adaptive relationships. But which perceptions stick with us? And when in the learning process are they codified in memory? We leveraged a popular television series-The Office-to answer these questions. Prior to their functional magnetic resonance imaging (fMRI) session, viewers of The Office reported which characters they identified with, as well as which characters they perceived another person (i.e. counterpart) was similar to. During their fMRI scan, participants found out which characters other people thought they and the counterpart were like, and also completed rest scans. Participants remembered more feedback inconsistent with their self-views (vs. views of the counterpart). Although neural activity while encoding self-inconsistent feedback did not meaningfully predict memory, returning to the inconsistent self feedback during subsequent rest did. During rest, participants reinstated neural patterns engaged while receiving self-inconsistent feedback in the dorsomedial prefrontal cortex (DMPFC). DMPFC reinstatement also quadratically predicted self-inconsistent memory, with too few or too many reinstatements compromising memory performance. Processing social feedback during rest may impact how we remember and integrate the feedback, especially when it contradicts our self-views.

Computational Social Psychology.

Social psychologists attempt to explain how we interact by appealing to basic principles of how we think. To make good on this ambition, they are increasingly relying on an interconnected set of formal tools that model inference, attribution, value-guided decision making, and multi-agent interactions. By reviewing progress in each of these areas and highlighting the connections between them, we can better appreciate the structure of social thought and behavior, while also coming to understand when, why, and how formal tools can be useful for social psychologists.

Deep models of superficial face judgments.

The diversity of human faces and the contexts in which they appear gives rise to an expansive stimulus space over which people infer psychological traits (e.g., trustworthiness or alertness) and other attributes (e.g., age or adiposity). Machine learning methods, in particular deep neural networks, provide expressive feature representations of face stimuli, but the correspondence between these representations and various human attribute inferences is difficult to determine because the former are high-dimensional vectors produced via black-box optimization algorithms. Here we combine deep generative image models with over 1 million judgments to model inferences of more than 30 attributes over a comprehensive latent face space. The predictive accuracy of our model approaches human interrater reliability, which simulations suggest would not have been possible with fewer faces, fewer judgments, or lower-dimensional feature representations. Our model can be used to predict and manipulate inferences with respect to arbitrary face photographs or to generate synthetic photorealistic face stimuli that evoke impressions tuned along the modeled attributes.

Impression management attenuates the effect of ability on trust in economic exchange.

Are competent actors still trusted when they promote themselves? The answer to this question could have far-reaching implications for understanding trust production in a variety of economic exchange settings in which ability and impression management play vital roles, from succeeding in one's job to excelling in the sales of goods and services. Much social science research assumes an unconditional positive impact of an actor's ability on the trust placed in that actor: in other words, competence breeds trust. In this report, however, we challenge this assumption. Across a series of experiments, we manipulated both the ability and the self-promotion of a trustee and measured the level of trust received. Employing both online laboratory studies (n = 5,606) and a field experiment (n = 101,520), we find that impression management tactics (i.e., self-promotion and intimidation) can substantially backfire, at least for those with high ability. An explanation for this effect is encapsuled in attribution theory, which argues that capable actors are held to higher standards in terms of how kind and honest they are expected to be. Consistent with our social attribution account, mediation analyses show that competence combined with self-promotion decreases the trustee's perceived benevolence and integrity and, in turn, the level of trust placed in that actor.

Americans discount the effect of friction on voter turnout.

Whether or not someone turns out to vote depends on their beliefs (such as partisanship or sense of civic duty) and on friction-external barriers such as long travel distance to the polls. In this exploratory study, we tested whether people underestimate the effect of friction on turnout and overestimate the effect of beliefs. We surveyed a representative sample of eligible US voters before and after the 2020 election (n = 1,280). Participants' perceptions consistently underemphasized friction and overemphasized beliefs (mean d = 0.94). In participants' open-text explanations, 91% of participants listed beliefs, compared with just 12% that listed friction. In contrast, turnout was shaped by beliefs only slightly more than friction. The actual belief-friction difference was about one-fourth the size of participants' perceptions (d = 0.24). This bias emerged across a range of survey measures (open- and close-ended; other- and self-judgments) and was implicated in downstream consequences such as support for friction-imposing policies and failing to plan one's vote.

Spiritual over physical formidability determines willingness to fight and sacrifice through loyalty in cross-cultural populations.

Across 11 studies involving six countries from four continents (n = 3,285), we extend insights from field investigations in conflict zones to offline and online surveys to show that personal spiritual formidability-the conviction and immaterial resources (values, strengths of beliefs, character) of a person to fight-is positively associated with the will to fight and sacrifice for others. The physical formidability of groups in conflict has long been promoted as the primary factor in human decisions to fight or flee in times of conflict. Here, studies in Spain, Iraq, Lebanon, Palestine, and Morocco reveal that personal spiritual formidability, a construct distinct from religiosity, is more strongly associated with the willingness to fight and make costly self-sacrifices for the group than physical formidability. A follow-on study among cadets of the US Air Force Academy further indicates that this effect is mediated by a stronger loyalty to the group, a finding replicated in a separate study with a European sample. The results demonstrate that personal spiritual formidability is a primary determinant of the will to fight across cultures, and this individual-level factor, propelled by loyal bonds made with others, disposes citizens and combatants to fight at great personal risk.

P1, N170, and N250 Event-related Potential Components Reflect Temporal Perception Processing in Face and Body Personal Identification.

Human faces and bodies represent various socially important signals. Although adults encounter numerous new people in daily life, they can recognize hundreds to thousands of different individuals. However, the neural mechanisms that differentiate one person from another person are unclear. This study aimed to clarify the temporal dynamics of the cognitive processes of face and body personal identification using face-sensitive ERP components (P1, N170, and N250). The present study performed three blocks (face-face, face-body, and body-body) of different ERP adaptation paradigms. Furthermore, in the above three blocks, ERP components were used to compare brain biomarkers under three conditions (same person, different person of the same sex, and different person of the opposite sex). The results showed that the P1 amplitude for the face-face block was significantly greater than that for the body-body block, that the N170 amplitude for a different person of the same sex condition was greater than that for the same person condition in the right hemisphere only, and that the N250 amplitude gradually increased as the degree of face and body sex-social categorization grew closer (i.e., same person condition > different person of the same sex condition > different person of the opposite sex condition). These results suggest that early processing of the face and body processes the face and body separately and that structural encoding and personal identification of the face and body process the face and body collaboratively.

Neural Tracking of Perceived Parent, but Not Peer, Norms Is Associated with Longitudinal Changes in Adolescent Attitudes about Externalizing Behaviors.

Adolescents' perceptions of parent and peer norms about externalizing behaviors influence the extent to which they adopt similar attitudes, yet little is known about how the trajectories of perceived parent and peer norms are related to trajectories of personal attitudes across adolescence. Neural development of midline regions implicated in self-other processing may underlie developmental changes in parent and peer influence. Here, we examined whether neural processing of perceived parent and peer norms in midline regions during self-evaluations would be associated with trajectories of personal attitudes about externalizing behaviors. Trajectories of adolescents' perceived parent and peer norms were examined longitudinally with functional neuroimaging (n = 165; ages 11-16 years across three waves; 86 girls, 79 boys; 29.7% White, 21.8% Black, 35.8% Latinx, 12.7% other/multiracial). Behavioral results showed perceived parent norms were less permissive than adolescents' own attitudes about externalizing behaviors, whereas perceived peer norms were more permissive than adolescents' own attitudes, effects that increased from early to middle adolescence. Although younger adolescents reported less permissive attitudes when they spontaneously tracked perceived parent norms in the ventromedial and medial pFCs during self-evaluations, this effect weakened as they aged. No brain-behavior effects were found when tracking perceived peer norms. These findings elucidate how perceived parent and peer norms change in parallel with personal attitudes about externalizing behaviors from early to middle adolescence and underscore the importance of spontaneous neural tracking of perceived parent norms during self-evaluations for buffering permissive personal attitudes, particularly in early adolescence.

Social Perception in the Infant Brain and Its Link to Social Behavior.

The current longitudinal study (n = 98) utilized a developmental cognitive neuroscience approach to examine whether and how variability in social perception is linked to social behavior in early human development. Cortical responses to processing dynamic faces were investigated using functional near-infrared spectroscopy at 7 months. Individual differences in sociability were measured using the Early Childhood Behavior Questionnaire at 18 months. Confirming previous work with infants and adults, functional near-infrared spectroscopy results show that viewing changing faces recruited superior temporal cortices in 7-month-old infants, adding to the view that this brain system is specialized in social perception from early in ontogeny. Our longitudinal results show that greater engagement of the right superior temporal cortex at 7 months predicts higher levels of sociability at 18 months. This suggests that early variability in social perception is linked to later differences in overtly displayed social behavior, providing novel longitudinal evidence for a social brain-behavior association.

The Timing of Gaze Direction Perception: ERP Decoding and Task Modulation.

Distinguishing the direction of another person's eye gaze is extremely important in everyday social interaction, as it provides critical information about people's attention and, therefore, intentions. The temporal dynamics of gaze processing have been investigated using event-related potentials (ERPs) recorded with electroencephalography (EEG). However, the moment at which our brain distinguishes the gaze direction (GD), irrespectively of other facial cues, remains unclear. To solve this question, the present study aimed to investigate the time course of gaze direction processing, using an ERP decoding approach, based on the combination of a support vector machine and error-correcting output codes. We recorded EEG in young healthy subjects, 32 of them performing GD detection and 34 conducting face orientation tasks. Both tasks presented 3D realistic faces with five different head and gaze orientations each: 30°, 15° to the left or right, and 0°. While the classical ERP analyses did not show clear GD effects, ERP decoding analyses revealed that discrimination of GD, irrespective of head orientation, started at 140 ms in the GD task and at 120 ms in the face orientation task. GD decoding accuracy was higher in the GD task than in the face orientation task and was the highest for the direct gaze in both tasks. These findings suggest that the decoding of brain patterns is modified by task relevance, which changes the latency and the accuracy of GD decoding.

Macaque claustrum, pulvinar and putative dorsolateral amygdala support the cross-modal association of social audio-visual stimuli based on meaning.

Social communication draws on several cognitive functions such as perception, emotion recognition and attention. The association of audio-visual information is essential to the processing of species-specific communication signals. In this study, we use functional magnetic resonance imaging in order to identify the subcortical areas involved in the cross-modal association of visual and auditory information based on their common social meaning. We identified three subcortical regions involved in audio-visual processing of species-specific communicative signals: the dorsolateral amygdala, the claustrum and the pulvinar. These regions responded to visual, auditory congruent and audio-visual stimulations. However, none of them was significantly activated when the auditory stimuli were semantically incongruent with the visual context, thus showing an influence of visual context on auditory processing. For example, positive vocalization (coos) activated the three subcortical regions when presented in the context of positive facial expression (lipsmacks) but not when presented in the context of negative facial expression (aggressive faces). In addition, the medial pulvinar and the amygdala presented multisensory integration such that audiovisual stimuli resulted in activations that were significantly higher than those observed for the highest unimodal response. Last, the pulvinar responded in a task-dependent manner, along a specific spatial sensory gradient. We propose that the dorsolateral amygdala, the claustrum and the pulvinar belong to a multisensory network that modulates the perception of visual socioemotional information and vocalizations as a function of the relevance of the stimuli in the social context. SIGNIFICANCE STATEMENT: Understanding and correctly associating socioemotional information across sensory modalities, such that happy faces predict laughter and escape scenes predict screams, is essential when living in complex social groups. With the use of functional magnetic imaging in the awake macaque, we identify three subcortical structures-dorsolateral amygdala, claustrum and pulvinar-that only respond to auditory information that matches the ongoing visual socioemotional context, such as hearing positively valenced coo calls and seeing positively valenced mutual grooming monkeys. We additionally describe task-dependent activations in the pulvinar, organizing along a specific spatial sensory gradient, supporting its role as a network regulator.

Face Processing Systems: From Neurons to Real-World Social Perception.

Primate face processing depends on a distributed network of interlinked face-selective areas composed of face-selective neurons. In both humans and macaques, the network is divided into a ventral stream and a dorsal stream, and the functional similarities of the areas in humans and macaques indicate they are homologous. Neural correlates for face detection, holistic processing, face space, and other key properties of human face processing have been identified at the single neuron level, and studies providing causal evidence have established firmly that face-selective brain areas are central to face processing. These mechanisms give rise to our highly accurate familiar face recognition but also to our error-prone performance with unfamiliar faces. This limitation of the face system has important implications for consequential situations such as eyewitness identification and policing.