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.

Category-Selective Representation of Relationships in the Visual Cortex.

Understanding social interaction requires processing social agents and their relationships. The latest results show that much of this process is visually solved: visual areas can represent multiple people encoding emergent information about their interaction that is not explained by the response to the individuals alone. A neural signature of this process is an increased response in visual areas, to face-to-face (seemingly interacting) people, relative to people presented as unrelated (back-to-back). This effect highlighted a network of visual areas for representing relational information. How is this network organized? Using functional MRI, we measured the brain activity of healthy female and male humans (N = 42), in response to images of two faces or two (head-blurred) bodies, facing toward or away from each other. Taking the facing > non-facing effect as a signature of relation perception, we found that relations between faces and between bodies were coded in distinct areas, mirroring the categorical representation of faces and bodies in the visual cortex. Additional analyses suggest the existence of a third network encoding relations between (nonsocial) objects. Finally, a separate occipitotemporal network showed the generalization of relational information across body, face, and nonsocial object dyads (multivariate pattern classification analysis), revealing shared properties of relations across categories. In sum, beyond single entities, the visual cortex encodes the relations that bind multiple entities into relationships; it does so in a category-selective fashion, thus respecting a general organizing principle of representation in high-level vision. Visual areas encoding visual relational information can reveal the processing of emergent properties of social (and nonsocial) interaction, which trigger inferential processes.

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.

Protective factors for children with autism spectrum disorder during COVID-19-related strict lockdowns: a Shanghai autism early developmental cohort study.

BACKGROUND: COVID-19 lockdowns increased the risk of mental health problems, especially for children with autism spectrum disorder (ASD). However, despite its importance, little is known about the protective factors for ASD children during the lockdowns. METHODS: Based on the Shanghai Autism Early Developmental Cohort, 188 ASD children with two visits before and after the strict Omicron lockdown were included; 85 children were lockdown-free, while 52 and 51 children were under the longer and the shorter durations of strict lockdown, respectively. We tested the association of the lockdown group with the clinical improvement and also the modulation effects of parent/family-related factors on this association by linear regression/mixed-effect models. Within the social brain structures, we examined the voxel-wise interaction between the grey matter volume and the identified modulation effects. RESULTS: Compared with the lockdown-free group, the ASD children experienced the longer duration of strict lockdown had less clinical improvement (ß = 0.49, 95% confidence interval (CI) [0.19-0.79], p = 0.001) and this difference was greatest for social cognition (2.62 [0.94-4.30], p = 0.002). We found that this association was modulated by parental agreeableness in a protective way (-0.11 [-0.17 to -0.05], p = 0.002). This protective effect was enhanced in the ASD children with larger grey matter volumes in the brain's mentalizing network, including the temporal pole, the medial superior frontal gyrus, and the superior temporal gyrus. CONCLUSIONS: This longitudinal neuroimaging cohort study identified that the parental agreeableness interacting with the ASD children's social brain development reduced the negative impact on clinical symptoms during the strict lockdown.

Metaverse in Mental Health: The Beginning of a Long History.

PURPOSE OF REVIEW: We review the first pilot studies applying metaverse-related technologies in psychiatric patients and discuss the rationale for using this complex federation of technologies to treat mental diseases. Concerning previous virtual-reality applications in medical care, metaverse technologies provide the unique opportunity to define, control, and shape virtual scenarios shared by multi-users to exploit the "synchronized brains" potential exacerbated by social interactions. RECENT FINDINGS: The application of an avatar-based sexual therapy program conducted on a metaverse platform has been demonstrated to be more effective concerning traditional sexual coaching for treating female orgasm disorders. Again, a metaverse-based social skills training program has been tested on children with autism spectrum disorders, demonstrating a significant impact on social interaction abilities. Metaverse-related technologies could enable us to develop new reliable approaches for treating diseases where behavioral symptoms can be addressed using socio-attentive tasks and social-interaction strategies.

The relationships between dynamic resting-state networks and social behavior in autism spectrum disorder revealed by fuzzy entropy-based temporal variability analysis of large-scale network.

Autism spectrum disorder (ASD) is a common neurodevelopmental disorder characterized by a core deficit in social processes. However, it is still unclear whether the core clinical symptoms of the disorder can be reflected by the temporal variability of resting-state network functional connectivity (FC). In this article, we examined the large-scale network FC temporal variability at the local region, within-network, and between-network levels using the fuzzy entropy technique. Then, we correlated the network FC temporal variability to social-related scores. We found that the social behavior correlated with the FC temporal variability of the precuneus, parietal, occipital, temporal, and precentral. Our results also showed that social behavior was significantly negatively correlated with the temporal variability of FC within the default mode network, between the frontoparietal network and cingulo-opercular task control network, and the dorsal attention network. In contrast, social behavior correlated significantly positively with the temporal variability of FC within the subcortical network. Finally, using temporal variability as a feature, we construct a model to predict the social score of ASD. These findings suggest that the network FC temporal variability has a close relationship with social behavioral inflexibility in ASD and may serve as a potential biomarker for predicting ASD symptom severity.

Oxytocin modulates social brain network correlations in resting and task state.

The effects of oxytocin (OT) on the social brain can be tracked upon assessing the neural activity in resting and task states, and developing a system-level framework for characterizing the state-based functional relationships of its distinct effect. Here, we contribute to this framework by examining how OT modulates social brain network correlations during resting and task states, using fMRI. First, we investigated network activation, followed by an analysis of the relationships between networks and individual differences. Subsequently, we evaluated the functional connectivity in both states. Finally, the relationship between networks across states was represented by the predictive power of networks in the resting state for task-evoked activities. The differences in the predicted accuracy between the subjects displayed individual variations in this relationship. Our results showed that the activity of the dorsal default mode network in the resting state had the largest predictive power for task-evoked activation of the precuneus network (PN) only in the OT group. The results also demonstrated that OT reduced the individual variation in PN in the prediction process. These findings suggest a distributed but modulatory effect of OT on the association between resting and task-dependent brain networks.

Synchronous caregiving from birth to adulthood tunes humans' social brain.

Mammalian young are born with immature brain and rely on the mother's body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal-newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal-newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother-child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others' distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others' distinct emotions. Provision of maternal-newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain's sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others' affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.

Transitioning from childhood into adolescence: A comprehensive longitudinal behavioral and neuroimaging study on prosocial behavior and social inclusion.

Acting prosocially and feeling socially included are important factors for developing social relations. However, little is known about the development of neural trajectories of prosocial behavior and social inclusion in the transition from middle childhood to early adolescence. In this pre-registered study, we investigated the development of prosocial behavior, social inclusion, and their neural mechanisms in a three-wave longitudinal design (ages 7-13 years; NT1 = 512; NT2 = 456; NT3 = 336). We used the Prosocial Cyberball Game, a ball tossing game in which one player is excluded, to measure prosocial compensating behavior. Prosocial compensating behavior showed a linear developmental increase, similar to parent-reported prosocial behavior, whereas parent-reported empathy showed a quadratic trajectory with highest levels in late childhood. On a neural level we found a peak in ventral striatum activity during prosocial compensating behavior. Neural activity during social inclusion showed quadratic age effects in anterior cingulate cortex, insula, striatum, and precuneus, and a linear increase in temporo-parietal junction. Finally, changes in prosocial compensating behavior were negatively associated with changes in ventral striatum and mPFC activity during social inclusion, indicating an important co-occurrence between development in brain and social behavior. Together these findings shed a light on the mechanisms underlying social development from childhood into adolescence.

Home alone: A population neuroscience investigation of brain morphology substrates.

As a social species, ready exchange with peers is a pivotal asset - our "social capital". Yet, single-person households have come to pervade metropolitan cities worldwide, with unknown consequences in the long run. Here, we systematically explore the morphological manifestations associated with singular living in ∼40,000 UK Biobank participants. The uncovered population-level signature spotlights the highly associative default mode network, in addition to findings such as in the amygdala central, cortical and corticoamygdaloid nuclei groups, as well as the hippocampal fimbria and dentate gyrus. Both positive effects, equating to greater gray matter volume associated with living alone, and negative effects, which can be interpreted as greater gray matter associations with not living alone, were found across the cortex and subcortical structures Sex-stratified analyses revealed male-specific neural substrates, including somatomotor, saliency and visual systems, while female-specific neural substrates centered on the dorsomedial prefrontal cortex. In line with our demographic profiling results, the discovered neural pattern of living alone is potentially linked to alcohol and tobacco consumption, anxiety, sleep quality as well as daily TV watching. The persistent trend for solitary living will require new answers from public-health decision makers. SIGNIFICANCE STATEMENT: Living alone has profound consequences for mental and physical health. Despite this, there has been a rapid increase in single-person households worldwide, with the long-term consequences yet unknown. In the largest study of its kind, we investigate how the objective lack of everyday social interaction, through living alone, manifests in the brain. Our population neuroscience approach uncovered a gray matter signature that converged on the 'default network', alongside targeted subcortical, sex and demographic profiling analyses. The human urge for social relationships is highlighted by the evolving COVID-19 pandemic. Better understanding of how social isolation relates to the brain will influence health and social policy decision-making of pandemic planning, as well as social interventions in light of global shifts in houseful structures.

Social withdrawal and gender differences: Clinical phenotypes and biological bases.

Evidence from everyday life suggests that differences in social behaviors between males and females exist, both in animal and in humans. These differences can be related to socio-cultural determinants, but also to specialized portions of the brain (the social brain), from the neurotransmitter to the neural network level. The high vulnerability of this system is expressed by the wide range of neuropsychiatric disorders associated with social dysfunctions, particularly social withdrawal. The principal psychiatric disorders with prominent social withdrawal are described, including hikikomori-like syndromes, and anxiety, depressive, autistic, schizophrenic, and personality disorders. It is hypothesized that social withdrawal can be partially independent from other symptoms and likely reflect alterations in the social brain itself, leading to a similar, transdiagnostic social dysfunction, reflecting defects in the social brain across a variety of psychopathological conditions. An overview is provided of gender effects in the biological determinants of social behavior, including: the anatomical structures of the social brain; the dimorphic brain structures, and the modulation of their development by sex steroids; gender differences in "social" neurotransmitters (vasopressin and oxytocin), and in their response to social stress. A better comprehension of gender differences in the phenotypes of social disorders and in the neural bases of social behaviors may provide new insights for timely, focused, innovative, and gender-specific treatments.

Altered neural mechanism of social reward anticipation in individuals with schizophrenia and social anhedonia.

Altered social reward anticipation could be found in schizophrenia (SCZ) patients and individuals with high levels of social anhedonia (SA). However, few research investigated the putative neural processing for altered social reward anticipation in these populations on the SCZ spectrum. This study aimed to examine the underlying neural mechanisms of social reward anticipation in these populations. Twenty-three SCZ patients and 17 healthy controls (HC), 37 SA individuals and 50 respective HCs completed the Social Incentive Delay (SID) imaging task while they were undertaking MRI brain scans. We used the group contrast to examine the alterations of BOLD activation and functional connectivity (FC, psychophysiological interactions analysis). We then characterized the beta-series social brain network (SBN) based on the meta-analysis results from NeuroSynth and examined their prediction effects on real-life social network (SN) characteristics using the partial least squared regression analysis. The results showed that SCZ patients exhibited hypo-activation of the left medial frontal gyrus and the negative FCs with the left parietal regions, while individuals with SA showed the hyper-activation of the left middle frontal gyrus when anticipating social reward. For the beta-series SBNs, SCZ patients had strengthened cerebellum-temporal FCs, while SA individuals had strengthened left frontal regions FCs. However, such FCs of the SBN failed to predict the real-life SN characteristics. These preliminary findings suggested that SCZ patients and SA individuals appear to exhibit altered neural processing for social reward anticipation, and such neural activities showed a weakened association with real-life SN characteristics.

Reading Covered Faces.

Covering faces with masks, due to mandatory pandemic safety regulations, we can no longer rely on the habitual daily-life information. This may be thought-provoking for healthy people, but particularly challenging for individuals with neuropsychiatric and neurodevelopmental conditions. Au fait research on reading covered faces reveals that: 1) wearing masks hampers facial affect recognition, though it leaves reliable inferring basic emotional expressions; 2) by buffering facial affect, masks lead to narrowing of emotional spectrum and dampen veridical evaluation of counterparts; 3) masks may affect perceived face attractiveness; 4) covered (either by masks or other veils) faces have a certain signal function introducing perceptual biases and prejudices; 5) reading covered faces is gender- and age-specific, being more challenging for males and more variable even in healthy aging; 6) the hampering effects of masks on social cognition occur over the globe; and 7) reading covered faces is likely to be supported by the large-scale assemblies of the neural circuits far beyond the social brain. Challenges and limitations of ongoing research and parallels to the Reading the Mind in the Eyes Test are assessed. Clarification of how masks affect face reading in the real world, where we deal with dynamic faces and have entrée to additional valuable social signals such as body language, as well as the specificity of neural networks underlying reading covered faces calls for further tailored research.

Eye Direction Detection and Perception as Premises of a Social Brain: A Narrative Review of Behavioral and Neural Data.

The eyes and the gaze are important stimuli for social interaction in humans. Impaired recognition of facial identity, facial emotions, and inference of the intentions of others may result from difficulties in extracting information relevant to the eye region, mainly the direction of gaze. Therefore, a review of these data is of interest. Behavioral data demonstrating the importance of the eye region and how humans respond to gaze direction are reviewed narratively, and several theoretical models on how visual information on gaze is processed are discussed to propose a unified hypothesis. Several issues that have not yet been investigated are identified. The authors tentatively suggest experiments that might help progress research in this area. The neural aspects are subsequently reviewed to best describe the low-level and higher-level visual information processing stages in the targeted subcortical and cortical areas. A specific neural network is proposed on the basis of the literature. Various gray areas, such as the temporality of the processing of visual information, the question of salience priority, and the coordination between the two hemispheres, remain unclear and require further investigations. Finally, disordered gaze direction detection mechanisms and their consequences on social cognition and behavior are discussed as key deficiencies in several conditions, such as autism spectrum disorder, 22q11.2 deletion, schizophrenia, and social anxiety disorder. This narrative review provides significant additional data showing that the detection and perception of someone's gaze is an essential part of the development of our social brain.

Disorganized attachment behaviors in infancy as predictors of brain morphology and peer rejection in late childhood.

Studies show robust links between disorganized attachment in infancy and socioemotional maladjustment in childhood. Little is known, however, about the links between disorganized attachment and brain development, and whether attachment-related differences in brain morphology translate into meaningful variations in child socioemotional functioning. This study examined the links between infants' disorganized attachment behaviors toward their mothers, whole-brain regional grey matter volume and thickness, and peer rejection in late childhood. Thirty-three children and their mothers took part in this study. The Strange Situation Procedure was used to assess mother-infant attachment when infants were 18 months old. Magnetic resonance imaging was performed when they were 10 years old to assess cortical thickness and grey matter volumes. Children and teachers reported on peer rejection 1 year later, as an indicator of socioemotional maladjustment. Results indicated that disorganized attachment was not associated with grey matter volumes. However, children who exhibited more disorganized attachment behaviors in infancy had significantly thicker cortices in bilateral middle and superior frontal gyri, and extending to the inferior frontal gyrus, as well as the orbitofrontal and insular cortices in the right hemisphere in late childhood. Moreover, children with thicker cortices in these regions experienced greater peer rejection, as rated by themselves and their teachers. Although preliminary, these results are the first to indicate that disorganized attachment may play a role in cortical thickness development and that changes in cortical thickness are associated with differences in child socioemotional functioning.

Behavioral performance and division of labor influence brain mosaicism in the leafcutter ant Atta cephalotes.

Brain evolution is hypothesized to be driven by behavioral selection on neuroarchitecture. We developed a novel metric of relative neuroanatomical investments involved in performing tasks varying in sensorimotor and processing demands across polymorphic task-specialized workers of the leafcutter ant Atta cephalotes and quantified brain size and structure to examine their correlation with our computational approximations. Investment in multisensory and motor integration for task performance was estimated to be greatest for media workers, whose highly diverse repertoire includes leaf-quality discrimination and leaf-harvesting tasks that likely involve demanding sensory and motor processes. Confocal imaging revealed that absolute brain volume increased with worker size and functionally specialized compartmental scaling differed among workers. The mushroom bodies, centers of sensory integration and learning and memory, and the antennal lobes, olfactory input sites, were larger in medias than in minims (gardeners) and significantly larger than in majors ("soldiers"), both of which had lower scores for involvement of olfactory processing in the performance of their characteristic tasks. Minims had a proportionally larger central complex compared to other workers. These results support the hypothesis that variation in task performance influences selection for mosaic brain structure, the independent evolution of proportions of the brain composed of different neuropils.

Chronic cluster headache: A study of the telencephalic and cerebellar cortical thickness.

PURPOSE: Previous studies on brain morphological alterations in chronic cluster headache revealed inconsistent findings. METHOD: The present cross-sectional explorative study determined telencephalic and cerebellar cortex thickness alterations in a relatively wide sample of chronic cluster headache patients (n = 28) comparing them to matched healthy individuals. RESULTS: The combination of two highly robust state-of-the-art approaches for thickness estimation (Freesurfer, CERES), strengthened by functional characterization of the identified abnormal regions, revealed four main results: chronic cluster headache patients show 1) cortical thinning in the right middle cingulate cortex, left posterior insula, and anterior cerebellar lobe, regions involved in nociception's sensory and sensory-motor aspects and possibly in autonomic functions; 2) cortical thinning in the left anterior superior temporal sulcus and the left collateral/lingual sulcus, suggesting neuroplastic maladaptation in areas possibly involved in social cognition, which may promote psychiatric comorbidity; 3) abnormal functional connectivity among some of these identified telencephalic areas; 4) the identified telencephalic areas of cortical thinning present robust interaction, as indicated by the functional connectivity results, with the left posterior insula possibly playing a pivotal role. CONCLUSION: The reported results constitute a coherent and robust picture of the chronic cluster headache brain. Our study paves the way for hypothesis-driven studies that might impact our understanding of the pathophysiology of this condition.

Behavioral Variant Frontotemporal Dementia and Social and Criminal Transgressions.

OBJECTIVE: Behavioral variant frontotemporal dementia (bvFTD) is associated with social and criminal transgressions; studies from countries around the world have documented such behavior in persons with this condition. An overview and analysis of social and criminal transgressions in bvFTD and their potential neurobiological mechanisms can provide a window for understanding the relationship of antisocial behavior and the brain. METHODS: This review evaluated the literature on the frequency of social and criminal transgressions in bvFTD and the neurobiological disturbances that underlie them. RESULTS: There is a high frequency of transgressions among patients with bvFTD due to impairments in neurocognition, such as social perception, behavioral regulation, and theory of mind, and impairments in social emotions, such as self-conscious emotions and empathy. Additionally, there is significant evidence for a specific impairment in an innate sense of morality. Alterations in these neurobiological processes result from predominantly right-hemisphere pathology in frontal (ventromedial, orbitofrontal, inferolateral frontal), anterior temporal (amygdala, temporal pole), limbic (anterior cingulate, amygdala), and insular regions. CONCLUSIONS: Overlapping disturbances in neurocognition, social emotions, and moral reasoning result from disease in the mostly mesial and right-sided frontotemporal network necessary for responding emotionally to others and for behavioral control. With increased sophistication in neurobiological interventions, future goals may be the routine evaluation of these processes among individuals with bvFTD who engage in social and criminal transgressions and the targeting of these neurobiological mechanisms with behavioral, pharmacological, and other interventions.

Hub-connected functional connectivity within social brain network weakens the association with real-life social network in schizophrenia patients.

Hubs in the brain network are the regions with high centrality and are crucial in the network communication and information integration. Patients with schizophrenia (SCZ) exhibit wide range of abnormality in the hub regions and their connected functional connectivity (FC) at the whole-brain network level. Study of the hubs in the brain networks supporting complex social behavior (social brain network, SBN) would contribute to understand the social dysfunction in patients with SCZ. Forty-nine patients with SCZ and 27 healthy controls (HC) were recruited to undertake the resting-state magnetic resonance imaging scanning and completed a social network (SN) questionnaire. The resting-state SBN was constructed based on the automatic analysis results from the NeuroSynth. Our results showed that the left temporal lobe was the only hub of SBN, and its connected FCs strength was higher than the remaining FCs in both two groups. SCZ patients showed the lower association between the hub-connected FCs (compared to the FCs not connected to the hub regions) with the real-life SN characteristics. These results were replicated in another independent sample (30 SCZ and 28 HC). These preliminary findings suggested that the hub-connected FCs of SBN in SCZ patients exhibit the abnormality in predicting real-life SN characteristics.

Variability in Brain Structure and Function Reflects Lack of Peer Support.

Humans are a highly social species. Complex interactions for mutual support range from helping neighbors to building social welfare institutions. During times of distress or crisis, sharing life experiences within one's social circle is critical for well-being. By translating pattern-learning algorithms to the UK Biobank imaging-genetics cohort (n = ~40 000 participants), we have delineated manifestations of regular social support in multimodal whole-brain measurements. In structural brain variation, we identified characteristic volumetric signatures in the salience and limbic networks for high- versus low-social support individuals. In patterns derived from functional coupling, we also located interindividual differences in social support in action-perception circuits related to binding sensory cues and initiating behavioral responses. In line with our demographic profiling analysis, the uncovered neural substrates have potential implications for loneliness, substance misuse, and resilience to stress.