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.

A familiar face and person processing area in the human temporal pole.

How does the brain process the faces of familiar people? Neuropsychological studies have argued for an area of the temporal pole (TP) linking faces with person identities, but magnetic susceptibility artifacts in this region have hampered its study with fMRI. Using data acquisition and analysis methods optimized to overcome this artifact, we identify a familiar face response in TP, reliably observed in individual brains. This area responds strongly to visual images of familiar faces over unfamiliar faces, objects, and scenes. However, TP did not just respond to images of faces, but also to a variety of high-level social cognitive tasks, including semantic, episodic, and theory of mind tasks. The response profile of TP contrasted with a nearby region of the perirhinal cortex that responded specifically to faces, but not to social cognition tasks. TP was functionally connected with a distributed network in the association cortex associated with social cognition, while PR was functionally connected with face-preferring areas of the ventral visual cortex. This work identifies a missing link in the human face processing system that specifically processes familiar faces, and is well placed to integrate visual information about faces with higher-order conceptual information about other people. The results suggest that separate streams for person and face processing reach anterior temporal areas positioned at the top of the cortical hierarchy.

Processing communicative facial and vocal cues in the superior temporal sulcus.

Facial and vocal cues provide critical social information about other humans, including their emotional and attentional states and the content of their speech. Recent work has shown that the face-responsive region of posterior superior temporal sulcus ("fSTS") also responds strongly to vocal sounds. Here, we investigate the functional role of this region and the broader STS by measuring responses to a range of face movements, vocal sounds, and hand movements using fMRI. We find that the fSTS responds broadly to different types of audio and visual face action, including both richly social communicative actions, as well as minimally social noncommunicative actions, ruling out hypotheses of specialization for processing speech signals, or communicative signals more generally. Strikingly, however, responses to hand movements were very low, whether communicative or not, indicating a specific role in the analysis of face actions (facial and vocal), not a general role in the perception of any human action. Furthermore, spatial patterns of response in this region were able to decode communicative from noncommunicative face actions, both within and across modality (facial/vocal cues), indicating sensitivity to an abstract social dimension. These functional properties of the fSTS contrast with a region of middle STS that has a selective, largely unimodal auditory response to speech sounds over both communicative and noncommunicative vocal nonspeech sounds, and nonvocal sounds. Region of interest analyses were corroborated by a data-driven independent component analysis, identifying face-voice and auditory speech responses as dominant sources of voxelwise variance across the STS. These results suggest that the STS contains separate processing streams for the audiovisual analysis of face actions and auditory speech processing.

Parts-based representations of perceived face movements in the superior temporal sulcus.

Facial motion is a primary source of social information about other humans. Prior fMRI studies have identified regions of the superior temporal sulcus (STS) that respond specifically to perceived face movements (termed fSTS), but little is known about the nature of motion representations in these regions. Here we use fMRI and multivoxel pattern analysis to characterize the representational content of the fSTS. Participants viewed a set of specific eye and mouth movements, as well as combined eye and mouth movements. Our results demonstrate that fSTS response patterns contain information about face movements, including subtle distinctions between types of eye and mouth movements. These representations generalize across the actor performing the movement, and across small differences in visual position. Critically, patterns of response to combined movements could be well predicted by linear combinations of responses to individual eye and mouth movements, pointing to a parts-based representation of complex face movements. These results indicate that the fSTS plays an intermediate role in the process of inferring social content from visually perceived face movements, containing a representation that is sufficiently abstract to generalize across low-level visual details, but still tied to the kinematics of face part movements.

Using individual functional channels of interest to study cortical development with fNIRS.

Functional near-infrared spectroscopy (fNIRS) is a noninvasive neuroimaging technique that could be uniquely effective for investigating cortical function in human infants. However, prior efforts have been hampered by the difficulty of aligning arrays of fNIRS optodes placed on the scalp to anatomical or functional regions of underlying cortex. This challenge can be addressed by identifying channels of interest in individual participants, and then testing the reliability of those channels' response profiles in independent data. Using this approach, cortical regions with preferential responses to faces versus scenes, and to scenes versus faces, were observed reliably in both adults and infants. By contrast, standard analysis techniques did not reliably identify significant responses to both categories in either age group. These results reveal scene-responsive regions, and confirm face-responsive regions, in preverbal infants. More generally, the analysis approach will be a robust and sensitive tool for future characterization of the early functional development of the human brain.

Functional Organization of Social Perception and Cognition in the Superior Temporal Sulcus.

The superior temporal sulcus (STS) is considered a hub for social perception and cognition, including the perception of faces and human motion, as well as understanding others' actions, mental states, and language. However, the functional organization of the STS remains debated: Is this broad region composed of multiple functionally distinct modules, each specialized for a different process, or are STS subregions multifunctional, contributing to multiple processes? Is the STS spatially organized, and if so, what are the dominant features of this organization? We address these questions by measuring STS responses to a range of social and linguistic stimuli in the same set of human participants, using fMRI. We find a number of STS subregions that respond selectively to certain types of social input, organized along a posterior-to-anterior axis. We also identify regions of overlapping response to multiple contrasts, including regions responsive to both language and theory of mind, faces and voices, and faces and biological motion. Thus, the human STS contains both relatively domain-specific areas, and regions that respond to multiple types of social information.

Occipital cortex of blind individuals is functionally coupled with executive control areas of frontal cortex.

In congenital blindness, the occipital cortex responds to a range of nonvisual inputs, including tactile, auditory, and linguistic stimuli. Are these changes in functional responses to stimuli accompanied by altered interactions with nonvisual functional networks? To answer this question, we introduce a data-driven method that searches across cortex for functional connectivity differences across groups. Replicating prior work, we find increased fronto-occipital functional connectivity in congenitally blind relative to blindfolded sighted participants. We demonstrate that this heightened connectivity extends over most of occipital cortex but is specific to a subset of regions in the inferior, dorsal, and medial frontal lobe. To assess the functional profile of these frontal areas, we used an n-back working memory task and a sentence comprehension task. We find that, among prefrontal areas with overconnectivity to occipital cortex, one left inferior frontal region responds to language over music. By contrast, the majority of these regions responded to working memory load but not language. These results suggest that in blindness occipital cortex interacts more with working memory systems and raise new questions about the function and mechanism of occipital plasticity.

Neural signatures of autism.

Functional magnetic resonance imaging of brain responses to biological motion in children with autism spectrum disorder (ASD), unaffected siblings (US) of children with ASD, and typically developing (TD) children has revealed three types of neural signatures: (i) state activity, related to the state of having ASD that characterizes the nature of disruption in brain circuitry; (ii) trait activity, reflecting shared areas of dysfunction in US and children with ASD, thereby providing a promising neuroendophenotype to facilitate efforts to bridge genomic complexity and disorder heterogeneity; and (iii) compensatory activity, unique to US, suggesting a neural system-level mechanism by which US might compensate for an increased genetic risk for developing ASD. The distinct brain responses to biological motion exhibited by TD children and US are striking given the identical behavioral profile of these two groups. These findings offer far-reaching implications for our understanding of the neural systems underlying autism.

Three systems of insular functional connectivity identified with cluster analysis.

Despite much research on the function of the insular cortex, few studies have investigated functional subdivisions of the insula in humans. The present study used resting-state functional connectivity magnetic resonance imaging (MRI) to parcellate the human insular lobe based on clustering of functional connectivity patterns. Connectivity maps were computed for each voxel in the insula based on resting-state functional MRI (fMRI) data and segregated using cluster analysis. We identified 3 insular subregions with distinct patterns of connectivity: a posterior region, functionally connected with primary and secondary somatomotor cortices; a dorsal anterior to middle region, connected with dorsal anterior cingulate cortex, along with other regions of a previously described control network; and a ventral anterior region, primarily connected with pregenual anterior cingulate cortex. Applying these regions to a separate task data set, we found that dorsal and ventral anterior insula responded selectively to disgusting images, while posterior insula did not. These results demonstrate that clustering of connectivity patterns can be used to subdivide cerebral cortex into anatomically and functionally meaningful subregions; the insular regions identified here should be useful in future investigations on the function of the insula.

Dissociable brain mechanisms for processing social exclusion and rule violation.

Social exclusion inherently involves an element of expectancy violation, in that we expect other people to follow the unwritten rule to include us in social interactions. In this functional magnetic resonance imaging (fMRI) study, we employed a unique modification of an interactive virtual ball-tossing game called "Cyberball" (Williams et al., 2000) and a novel paradigm called "Cybershape," in which rules are broken in the absence of social exclusion, to dissociate brain regions that process social exclusion from rule violations more generally. Our Cyberball game employed an alternating block design and removed evoked responses to events when the participant was throwing the ball in inclusion to make this condition comparable to exclusion, where participants did not throw. With these modifications, we replicated prior findings of ventral anterior cingulate cortex (vACC), insula, and posterior cingulate cortex activity evoked by social exclusion relative to inclusion. We also identified exclusion-evoked activity in the hippocampi, left ventrolateral prefrontal cortex, and left middle temporal gyrus. Comparing social exclusion and rule violation revealed a functional dissociation in the active neural systems as well as differential functional connectivity with vACC. Some overlap was observed in regions differentially modulated by social exclusion and rule violation, including the vACC and lateral parietal cortex. These overlapping brain regions showed different activation during social exclusion compared to rule violation, each relative to fair play. Comparing activation patterns to social exclusion and rule violation allowed for the dissociation of brain regions involved in the experience of exclusion versus expectancy violation.

Development of neural systems for processing social exclusion from childhood to adolescence.

Adolescence is a period of development in which peer relationships become especially important. A computer-based game (Cyberball) has been used to explore the effects of social exclusion in adolescents and adults. The current functional magnetic resonance imaging (fMRI) study used Cyberball to extend prior work to the cross-sectional study of younger children and adolescents (7 to 17 years), identifying age-related changes in the neural correlates of social exclusion across the important transition from middle childhood into adolescence. Additionally, a control task illustrated the specificity of these age-related changes for social exclusion as distinct from expectancy violation more generally. During exclusion, activation in and functional connectivity between ventrolateral prefrontal cortex and ventral anterior cingulate cortex increased with age. These effects were specific to social exclusion and did not exist for expectancy violation. Our results illustrate developmental changes from middle childhood through adolescence in both affective and regulatory brain regions during social exclusion.

Organization of high-level visual cortex in human infants.

How much of the structure of the human mind and brain is already specified at birth, and how much arises from experience? In this article, we consider the test case of extrastriate visual cortex, where a highly systematic functional organization is present in virtually every normal adult, including regions preferring behaviourally significant stimulus categories, such as faces, bodies, and scenes. Novel methods were developed to scan awake infants with fMRI, while they viewed multiple categories of visual stimuli. Here we report that the visual cortex of 4-6-month-old infants contains regions that respond preferentially to abstract categories (faces and scenes), with a spatial organization similar to adults. However, precise response profiles and patterns of activity across multiple visual categories differ between infants and adults. These results demonstrate that the large-scale organization of category preferences in visual cortex is adult-like within a few months after birth, but is subsequently refined through development.

Enhanced neural responses to rule violation in children with autism: a comparison to social exclusion.

The present study aimed to explore the neural correlates of two characteristic deficits in autism spectrum disorders (ASD); social impairment and restricted, repetitive behavior patterns. To this end, we used comparable experiences of social exclusion and rule violation to probe potentially atypical neural networks in ASD. In children and adolescents with and without ASD, we used the interactive ball-toss game (Cyberball) to elicit social exclusion and a comparable game (Cybershape) to elicit a non-exclusive rule violation. Using functional magnetic resonance imaging (fMRI), we identified group differences in brain responses to social exclusion and rule violation. Though both groups reported equal distress following exclusion, the right insula and ventral anterior cingulate cortex were hypoactive during exclusion in children with ASD. In rule violation, right insula and dorsal prefrontal cortex were hyperactive in ASD. Right insula showed a dissociation in activation; it was hypoactive to social exclusion and hyperactive to rule violation in the ASD group. Further probed, different regions of right insula were modulated in each game, highlighting differences in regional specificity for which subsequent analyses revealed differences in patterns of functional connectivity. These results demonstrate neurobiological differences in processing social exclusion and rule violation in children with ASD.

Reading about the actions of others: biological motion imagery and action congruency influence brain activity.

Prior neuroimaging research has implicated regions within and near the posterior superior temporal sulcus (pSTS) in the visual processing of biological motion and of the intentions implied by specific movements. However, it is unknown whether this region is engaged during the processing of human motion at a conceptual level, such as during story comprehension. Here, we obtained functional magnetic resonance images from subjects reading brief stories that described a human character's background and then concluded with an action or decision made by the character. Half of the stories contained incidental descriptions of biological motion (such as the character's walking or grasping) while the remaining half did not. As a second factor, the final action of the story was either congruent or incongruent with the character's background and implied goals and intentions. Stories that contained biological motion strongly activated the pSTS bilaterally, along with ventral temporal areas, premotor cortex, left motor cortex, and the precuneus. Active regions of pSTS in individual subjects closely overlapped with regions identified with a separate biological motion localizer (point-light display) task. Reading incongruent versus congruent stories activated dorsal anterior cingulate cortex and bilateral anterior insula. These results support the hypothesis that reading can engage higher visual cortex in a content-specific manner, and suggest that the presence of biological motion should be controlled as a potential confound in fMRI studies using story comprehension tasks.