Neural Mechanisms of Social Cognition in Primates.

Activity in a network of areas spanning the superior temporal sulcus, dorsomedial frontal cortex, and anterior cingulate cortex is concerned with how nonhuman primates negotiate the social worlds in which they live. Central aspects of these circuits are retained in humans. Activity in these areas codes for primates' interactions with one another, their attempts to find out about one another, and their attempts to prevent others from finding out too much about themselves. Moreover, important features of the social world, such as dominance status, cooperation, and competition, modulate activity in these areas. We consider the degree to which activity in these regions is simply encoding an individual's own actions and choices or whether this activity is especially and specifically concerned with social cognition. Recent advances in comparative anatomy and computational modeling may help us to gain deeper insights into the nature and boundaries of primate social cognition.

Encoding of dynamic facial information in the middle dorsal face area.

Faces in motion reveal a plethora of information through visual dynamics. Faces can move in complex patterns while transforming facial shape, e.g., during the generation of different emotional expressions. While motion and shape processing have been studied extensively in separate research enterprises, much less is known about their conjunction during biological motion. Here, we took advantage of the discovery in brain-imaging studies of an area in the dorsal portion of the macaque monkey superior temporal sulcus (STS), the middle dorsal face area (MD), with selectivity for naturalistic face motion. To gain mechanistic insights into the coding of facial motion, we recorded single-unit activity from MD, testing whether and how MD cells encode face motion. The MD population was highly sensitive to naturalistic facial motion and facial shape. Some MD cells responded only to the conjunction of facial shape and motion, others were selective for facial shape even without movement, and yet others were suppressed by facial motion. We found that this heterogeneous MD population transforms face motion into a higher dimensional activity space, a representation that would allow for high sensitivity to relevant small-scale movements. Indeed, we show that many MD cells carry such sensitivity for eye movements. We further found that MD cells encode motion of head, mouth, and eyes in a separable manner, requiring the use of multiple reference frames. Thus, MD is a bona fide face-motion area that uses highly heterogeneous cell populations to create codes capturing even complex facial motion trajectories.

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.

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.

Alternative Brain Connectivity Underscores Age-Related Differences in the Processing of Interactive Biological Motion.

Rapidly recognizing and understanding others' social interactions is an important ability that relies on deciphering multiple sources of information, for example, perceiving body information and inferring others' intentions. Despite recent advances in characterizing the brain basis of this ability in adults, its developmental underpinnings are virtually unknown. Here, we used fMRI to investigate which sources of social information support superior temporal sulcus responses to interactive biological motion (i.e., 2 interacting point-light human figures) at different developmental intervals in human participants (of either sex): Children show supportive functional connectivity with key nodes of the mentalizing network, while adults show stronger reliance on regions associated with body- and dynamic social interaction/biological motion processing. We suggest that adults use efficient action-intention understanding via body and biological motion information, while children show a stronger reliance on hidden mental state inferences as a potential means of learning to better understand others' interactive behavior.SIGNIFICANCE STATEMENT Recognizing others' interactive behavior is a critical human skill that depends on different sources of social information (e.g., observable body-action information, inferring others' hidden mental states, etc.). Understanding the brain-basis of this ability and characterizing how it emerges across development are important goals in social neuroscience. Here, we used fMRI to investigate which sources of social information support interactive biological motion processing in children (6-12 years) and adults. These results reveal a striking developmental difference in terms of how wider-brain connectivity shapes functional responses to interactive biological motion that suggests a reliance on distinct neuro-cognitive strategies in service of interaction understanding (i.e., children and adults show a greater reliance on explicit and implicit intentional inference, respectively).

Neural decoding of emotional prosody in voice-sensitive auditory cortex predicts social communication abilities in children.

During social interactions, speakers signal information about their emotional state through their voice, which is known as emotional prosody. Little is known regarding the precise brain systems underlying emotional prosody decoding in children and whether accurate neural decoding of these vocal cues is linked to social skills. Here, we address critical gaps in the developmental literature by investigating neural representations of prosody and their links to behavior in children. Multivariate pattern analysis revealed that representations in the bilateral middle and posterior superior temporal sulcus (STS) divisions of voice-sensitive auditory cortex decode emotional prosody information in children. Crucially, emotional prosody decoding in middle STS was correlated with standardized measures of social communication abilities; more accurate decoding of prosody stimuli in the STS was predictive of greater social communication abilities in children. Moreover, social communication abilities were specifically related to decoding sadness, highlighting the importance of tuning in to negative emotional vocal cues for strengthening social responsiveness and functioning. Findings bridge an important theoretical gap by showing that the ability of the voice-sensitive cortex to detect emotional cues in speech is predictive of a child's social skills, including the ability to relate and interact with others.

Genetic determinants of individual variation in the superior temporal sulcus of chimpanzees (Pan troglodytes).

The superior temporal sulcus (STS) is a conserved fold that divides the middle and superior temporal gyri. In humans, there is considerable variation in the shape, folding pattern, lateralization, and depth of the STS that have been reported to be associated with social cognition and linguistic functions. We examined the role that genetic factors play on individual variation in STS morphology in chimpanzees. The surface area and depth of the STS were quantified in sample of 292 captive chimpanzees comprised of two genetically isolated population of individuals. The chimpanzees had been previously genotyped for AVPR1A and KIAA0319, two genes that play a role in social cognition and communication in humans. Single nucleotide polymorphisms in the KIAA0319 and AVPR1A genes were associated with average depth as well as asymmetries in the STS. By contrast, we found no significant effects of these KIA0319 and AVPR1A polymorphism on surface area and depth measures for the central sulcus. The overall findings indicate that genetic factors account for a small to moderate amount of variation in STS morphology in chimpanzees. These findings are discussed in the context of the role of the STS in social cognition and language in humans and their potential evolutionary origins.

From teeth to brain: dental caries causally affects the cortical thickness of the banks of the superior temporal sulcus.

OBJECTIVES: Dental caries is one of the most prevalent oral diseases and causes of tooth loss. Cross-sectional studies observed epidemiological associations between dental caries and brain degeneration disorders, while it is unknown whether dental caries causally affect the cerebral structures. This study tested whether genetically proxied DMFS (the sum of Decayed, Missing, and Filled tooth Surfaces) causally impacts the brain cortical structure using Mendelian randomization (MR). METHODS: The summary-level GWAS meta-analysis data from the GLIDE consortium were used for DMFS, including 26,792 participants. ENIGMA (Enhancing NeuroImaging Genetics through Meta Analysis) consortium GWAS summary data of 51,665 patients were used for brain structure. This study estimated the causal effects of DMFS on the surface area (SA) and thickness (TH) of the global cortex and functional cortical regions accessed by magnetic resonance imaging (MRI). Inverse-variance weighted (IVW) was used as the primary estimate, the MR pleiotropy residual sum and outlier (MR-PRESSO), the MR-Egger intercept test, and leave-one-out analyses were used to examine the potential horizontal pleiotropy. RESULTS: Genetically proxied DMFS decreases the TH of the banks of the superior temporal sulcus (BANSSTS) with or without global weighted (weighted, ß = - 0.0277 mm, 95% CI: - 0.0470 mm to - 0.0085 mm, P = 0.0047; unweighted, ß = - 0.0311 mm, 95% CI: - 0.0609 mm to - 0.0012 mm, P = 0.0412). The causal associations were robust in various sensitivity analyses. CONCLUSIONS: Dental caries causally decrease the cerebral cortical thickness of the BANKSSTS, a cerebral cortical region crucial for language-related functions, and is the most affected brain region in Alzheimer's disease. This investigation provides the first evidence that dental caries causally affects brain structure, proving the existence of teeth-brain axes. This study also suggested that clinicians should highlight the causal effects of dental caries on brain disorders during the diagnosis and treatments, the cortical thickness of BANKSSTS is a promising diagnostic measurement for dental caries-related brain degeneration.

Segregation of Neural Circuits Involved in Social Gaze and Non-Social Arrow Cues: Evidence from an Activation Likelihood Estimation Meta-Analysis.

Orienting attention by social gaze cues shares some characteristics with orienting attention by non-social arrow cues, but it is unclear whether they rely on similar neural mechanisms. The present ALE-meta-analysis assessed the pattern of brain activation reported in 40 single experiments (18 with arrows, 22 with gaze), with a total number of 806 participants. Our findings show that the network for orienting attention by social gaze and by non-social arrow cues is in part functionally segregated. Orienting by both types of cues relies on the activity of brain regions involved in endogenous attention (the superior frontal gyrus). Importantly, only orienting by gaze cues was also associated with the activity of brain regions involved in exogenous attention (medial frontal gyrus), processing gaze, and mental state attribution (superior temporal sulcus, temporoparietal junction).

Anatomical correlates of face patches in macaque inferotemporal cortex.

Primate brains typically have regions within the ventral visual stream that are selectively responsive to faces. In macaques, these face patches are located in similar parts of inferotemporal cortex across individuals although correspondence with particular anatomical features has not been reported previously. Here, using high-resolution functional and anatomical imaging, we show that small "bumps," or buried gyri, along the lower bank of the superior temporal sulcus are predictive of the location of face-selective regions. Recordings from implanted multielectrode arrays verified that these bumps contain face-selective neurons. These bumps were present in monkeys raised without seeing faces and that lack face patches, indicating that these anatomical landmarks are predictive of, but not sufficient for, the presence of face selectivity. These bumps are found across primate species that span taxonomy lines, indicating common evolutionary developmental mechanisms. The bumps emerge during fetal development in macaques, indicating that they arise from general developmental mechanisms that result in the regularity of cortical folding of the entire brain.

Decoding of the other's focus of attention by a temporal cortex module.

Faces attract the observer's attention toward objects and locations of interest for the other, thereby allowing the two agents to establish joint attention. Previous work has delineated a network of cortical "patches" in the macaque cortex, processing faces, eventually also extracting information on the other's gaze direction. Yet, the neural mechanism that links information on gaze direction, guiding the observer's attention to the relevant object, has remained elusive. Here we present electrophysiological evidence for the existence of a distinct "gaze-following patch" (GFP) with neurons that establish this linkage in a highly flexible manner. The other's gaze and the object, singled out by the gaze, are linked only if this linkage is pertinent within the prevailing social context. The properties of these neurons establish the GFP as a key switch in controlling social interactions based on the other's gaze.

The role of motion in the neural representation of social interactions in the posterior temporal cortex.

Humans are an inherently social species, with multiple focal brain regions sensitive to various visual social cues such as faces, bodies, and biological motion. More recently, research has begun to investigate how the brain responds to more complex, naturalistic social scenes, identifying a region in the posterior superior temporal sulcus (SI-pSTS; i.e., social interaction pSTS), amongst others, as an important region for processing social interaction. This research, however, has presented images or videos, and thus the contribution of motion to social interaction perception in these brain regions is not yet understood. In the current study, 22 participants viewed videos, image sequences, scrambled image sequences and static images of either social interactions or non-social independent actions. Combining univariate and multivariate analyses, we confirm that bilateral SI-pSTS plays a central role in dynamic social interaction perception but is much less involved when 'interactiveness' is conveyed solely with static cues. Regions in the social brain, including SI-pSTS and extrastriate body area (EBA), showed sensitivity to both motion and interactive content. While SI-pSTS is somewhat more tuned to video interactions than is EBA, both bilateral SI-pSTS and EBA showed a greater response to social interactions compared to non-interactions and both regions responded more strongly to videos than static images. Indeed, both regions showed higher responses to interactions than independent actions in videos and intact sequences, but not in other conditions. Exploratory multivariate regression analyses suggest that selectivity for simple visual motion does not in itself drive interactive sensitivity in either SI-pSTS or EBA. Rather, selectivity for interactions expressed in point-light animations, and selectivity for static images of bodies, make positive and independent contributions to this effect across the LOTC region. Our results strongly suggest that EBA and SI-pSTS work together during dynamic interaction perception, at least when interactive information is conveyed primarily via body information. As such, our results are also in line with proposals of a third visual stream supporting dynamic social scene perception.

Multisensory mental imagery of fatigue: Evidence from an fMRI study.

Functional imaging experimental designs measuring fatigue, defined as a subjective lack of physical and/or mental energy characterizing a wide range of neurologic conditions, are still under development. Nineteen right-handed healthy subjects (9 M and 10 F, mean age 43.15 ± 8.34 years) were evaluated by means of functional magnetic resonance imaging (fMRI), asking them to perform explicit, first-person, mental imagery of fatigue-related multisensory sensations. Short sentences designed to assess the principal manifestations of fatigue from the Multidimensional Fatigue Symptom Inventory were presented. Participants were asked to imagine the corresponding sensations (Sensory Imagery, SI). As a control, they had to imagine the visual scenes (Visual Imagery, VI) described in short phrases. The SI task (vs. VI task) differentially activated three areas: (i) the precuneus, which is involved in first-person perspective taking; (ii) the left superior temporal sulcus, which is a multisensory integration area; and (iii) the left inferior frontal gyrus, known to be involved in mental imagery network. The SI fMRI task can be used to measure processing involved in mental imagery of fatigue-related multisensory sensations.

Using child-friendly movie stimuli to study the development of face, place, and object regions from age 3 to 12 years.

Scanning young children while they watch short, engaging, commercially-produced movies has emerged as a promising approach for increasing data retention and quality. Movie stimuli also evoke a richer variety of cognitive processes than traditional experiments, allowing the study of multiple aspects of brain development simultaneously. However, because these stimuli are uncontrolled, it is unclear how effectively distinct profiles of brain activity can be distinguished from the resulting data. Here we develop an approach for identifying multiple distinct subject-specific Regions of Interest (ssROIs) using fMRI data collected during movie-viewing. We focused on the test case of higher-level visual regions selective for faces, scenes, and objects. Adults (N = 13) were scanned while viewing a 5.6-min child-friendly movie, as well as a traditional localizer experiment with blocks of faces, scenes, and objects. We found that just 2.7 min of movie data could identify subject-specific face, scene, and object regions. While successful, movie-defined ssROIS still showed weaker domain selectivity than traditional ssROIs. Having validated our approach in adults, we then used the same methods on movie data collected from 3 to 12-year-old children (N = 122). Movie response timecourses in 3-year-old children's face, scene, and object regions were already significantly and specifically predicted by timecourses from the corresponding regions in adults. We also found evidence of continued developmental change, particularly in the face-selective posterior superior temporal sulcus. Taken together, our results reveal both early maturity and functional change in face, scene, and object regions, and more broadly highlight the promise of short, child-friendly movies for developmental cognitive neuroscience.

The roles of the LpSTS and DLPFC in self-prioritization: A transcranial magnetic stimulation study.

The Self-Attention Network (SAN) has been proposed to describe the underlying neural mechanism of the self-prioritization effect, yet the roles of the key nodes in the SAN-the left posterior superior temporal sulcus (LpSTS) and the dorsolateral prefrontal cortex (DLPFC)-still need to be clarified. One hundred and nine participants were randomly assigned into the LpSTS group, the DLPFC group, or the sham group. We used the transcranial magnetic stimulation (TMS) technique to selectively disrupt the functions of the corresponding targeted region, and observed its impacts on self-prioritization effect based on the difference between the performance of the self-matching task before and after the targeted stimulation. We analyzed both model-free performance measures and HDDM-based performance measures for the self-matching task. The results showed that the inhibition of LpSTS could lead to reduced performance in processing self-related stimuli, which establishes a causal role for the LpSTS in self-related processing and provide direct evidence to support the SAN framework. However, the results of the DLPFC group from HDDM analysis were distinct from the results based on response efficiency. Our investigation further the understanding of the differentiated roles of key nodes in the SAN in supporting the self-salience in information processing.

Doll play prompts social thinking and social talking: Representations of internal state language in the brain.

Doll play provides opportunities for children to practice social skills by creating imaginary worlds, taking others' perspectives, and talking about others' internal states. Previous research using functional near-infrared spectroscopy (fNIRS) found a region over the posterior superior temporal sulcus (pSTS) was more active during solo doll play than solo tablet play, implying that doll play might present opportunities for rehearsing theory of mind and empathy skills, even when playing alone. In this research, we addressed this more directly by investigating 4-8-year-old children's (N = 33) use of internal state language (ISL; i.e., references to emotions, desires, and cognitions) when playing with dolls and on tablets, both by themselves and with a social partner, and their associated brain activity in the pSTS using fNIRS. We found that children used more ISL about others when playing with dolls than when playing on tablets, particularly when they were playing alone. This mirrored the patterns seen in pSTS activity in previous research. When individual variability in ISL about others was considered, more ISL about others was linked to stronger pSTS activation. Thus, variability in pSTS activity during play is not about the perceptual or physical differences between toys (e.g., dolls are more human-like) but about what children think about when they engage in different kinds of play. This is the first research to investigate brain activity during spontaneously occurring ISL and indicates that children have a tendency to take and discuss others' perspectives during doll play, with implications for social processing in the brain. A video abstract of this article can be viewed at https://youtu.be/58HgxbuhBzU.

Top-Down Attention Guidance Shapes Action Encoding in the pSTS.

The posterior superior temporal sulcus (pSTS) is a brain region characterized by perceptual representations of human body actions that promote the understanding of observed behavior. Increasingly, action observation is recognized as being strongly shaped by the expectations of the observer (Kilner 2011; Koster-Hale and Saxe 2013; Patel et al. 2019). Therefore, to characterize top-down influences on action observation, we evaluated the statistical structure of multivariate activation patterns from the action observation network (AON) while observers attended to the different dimensions of action vignettes (the action kinematics, goal, or identity of avatars jumping or crouching). Decoding accuracy varied as a function of attention instruction in the right pSTS and left inferior frontal cortex (IFC), with the right pSTS classifying actions most accurately when observers attended to the action kinematics and the left IFC classifying most accurately when observed attended to the actor's goal. Functional connectivity also increased between the right pSTS and right IFC when observers attended to the actions portrayed in the vignettes. Our findings are evidence that the attentive state of the viewer modulates sensory representations in the pSTS, consistent with proposals that the pSTS occupies an interstitial zone mediating top-down context and bottom-up perceptual cues during action observation.

Behavioral and neural correlates of social network size: The unique and common contributions of face recognition and extraversion.

OBJECTIVES: Humans are inherently social creatures and can gain advantages from larger network size. Researches have shown that different cognitive and personality factors may result in individual differences of social network size (SNS). Here, we focused on whether face recognition ability and extraversion were related to SNS and the neural basis underlying the relations. METHODS: Behaviorally, we adopted the face-inversion task, NEO personality inventory, and computerized SNS test to explore the relationships between face recognition, extraversion, and SNS. Neurally, we used resting state functional magnetic resonance imaging and fractional amplitude of low-frequency fluctuation (fALFF) analysis method to investigate the neural correlates of SNS and then revealed whether face recognition and extraversion were related to SNS relevant brain regions. RESULTS: We found that individuals with better face recognition ability and more extraverted personality had larger size of social network. In addition, we found that SNS was positively associated with the fALFF in the ventromedial prefrontal cortex (vmPFC), right superior temporal sulcus, and precuneus. Interestingly, the fALFF in the vmPFC significantly correlated with face recognition ability. CONCLUSIONS: Our study suggests that both face recognition and extraversion may be important correlates of SNS, and the underlying spontaneous neural substrates are partially dissociable.

Dissociating the functions of three left posterior superior temporal regions that contribute to speech perception and production.

Prior studies have shown that the left posterior superior temporal sulcus (pSTS) and left temporo-parietal junction (TPJ) both contribute to phonological short-term memory, speech perception and speech production. Here, by conducting a within-subjects multi-factorial fMRI study, we dissociate the response profiles of these regions and a third region - the anterior ascending terminal branch of the left superior temporal sulcus (atSTS), which lies dorsal to pSTS and ventral to TPJ. First, we show that each region was more activated by (i) 1-back matching on visually presented verbal stimuli (words or pseudowords) compared to 1-back matching on visually presented non-verbal stimuli (pictures of objects or non-objects), and (ii) overt speech production than 1-back matching, across 8 types of stimuli (visually presented words, pseudowords, objects and non-objects and aurally presented words, pseudowords, object sounds and meaningless hums). The response properties of the three regions dissociated within the auditory modality. In left TPJ, activation was higher for auditory stimuli that were non-verbal (sounds of objects or meaningless hums) compared to verbal (words and pseudowords), irrespective of task (speech production or 1-back matching). In left pSTS, activation was higher for non-semantic stimuli (pseudowords and hums) than semantic stimuli (words and object sounds) on the dorsal pSTS surface (dpSTS), irrespective of task. In left atSTS, activation was not sensitive to either semantic or verbal content. The contrasting response properties of left TPJ, dpSTS and atSTS was cross-validated in an independent sample of 59 participants, using region-by-condition interactions. We also show that each region participates in non-overlapping networks of frontal, parietal and cerebellar regions. Our results challenge previous claims about functional specialisation in the left posterior superior temporal lobe and motivate future studies to determine the timing and directionality of information flow in the brain networks involved in speech perception and production.