Converging evidence that left extrastriate body area supports visual sensitivity to social interactions.

Navigating our complex social world requires processing the interactions we observe. Recent psychophysical and neuroimaging studies provide parallel evidence that the human visual system may be attuned to efficiently perceive dyadic interactions. This work implies, but has not yet demonstrated, that activity in body-selective cortical regions causally supports efficient visual perception of interactions. We adopt a multi-method approach to close this important gap. First, using a large fMRI dataset (n = 92), we found that the left hemisphere extrastriate body area (EBA) responds more to face-to-face than non-facing dyads. Second, we replicated a behavioral marker of visual sensitivity to interactions: categorization of facing dyads is more impaired by inversion than non-facing dyads. Third, in a pre-registered experiment, we used fMRI-guided transcranial magnetic stimulation to show that online stimulation of the left EBA, but not a nearby control region, abolishes this selective inversion effect. Activity in left EBA, thus, causally supports the efficient perception of social interactions.

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.

Behavioral and neural markers of visual configural processing in social scene perception.

Research on face perception has revealed highly specialized visual mechanisms such as configural processing, and provided markers of interindividual differences -including disease risks and alterations- in visuo-perceptual abilities that traffic in social cognition. Is face perception unique in degree or kind of mechanisms, and in its relevance for social cognition? Combining functional MRI and behavioral methods, we address the processing of an uncharted class of socially relevant stimuli: minimal social scenes involving configurations of two bodies spatially close and face-to-face as if interacting (hereafter, facing dyads). We report category-specific activity for facing (vs. non-facing) dyads in visual cortex. That activity shows face-like signatures of configural processing -i.e., stronger response to facing (vs. non-facing) dyads, and greater susceptibility to stimulus inversion for facing (vs. non-facing) dyads-, and is predicted by performance-based measures of configural processing in visual perception of body dyads. Moreover, we observe that the individual performance in body-dyad perception is reliable, stable-over-time and correlated with the individual social sensitivity, coarsely captured by the Autism-Spectrum Quotient. Further analyses clarify the relationship between single-body and body-dyad perception. We propose that facing dyads are processed through highly specialized mechanisms -and brain areas-, analogously to other biologically and socially relevant stimuli such as faces. Like face perception, facing-dyad perception can reveal basic (visual) processes that lay the foundations for understanding others, their relationships and interactions.

Visual object categorization in infancy.

Humans make sense of the world by organizing things into categories. When and how does this process begin? We investigated whether real-world object categories that spontaneously emerge in the first months of life match categorical representations of objects in the human visual cortex. Using eye tracking, we measured the differential looking time of 4-, 10-, and 19-mo-olds as they looked at pairs of pictures belonging to eight animate or inanimate categories (human/nonhuman, faces/bodies, real-world size big/small, natural/artificial). Taking infants' looking times as a measure of similarity, for each age group, we defined a representational space where each object was defined in relation to others of the same or of a different category. This space was compared with hypothesis-based and functional MRI-based models of visual object categorization in the adults' visual cortex. Analyses across different age groups showed that, as infants grow older, their looking behavior matches neural representations in ever-larger portions of the adult visual cortex, suggesting progressive recruitment and integration of more and more feature spaces distributed over the visual cortex. Moreover, the results characterize infants' visual categorization as an incremental process with two milestones. Between 4 and 10 mo, visual exploration guided by saliency gives way to an organization according to the animate-inanimate distinction. Between 10 and 19 mo, a category spurt leads toward a mature organization. We propose that these changes underlie the coupling between seeing and thinking in the developing mind.

Moving Toward versus Away from Another: How Body Motion Direction Changes the Representation of Bodies and Actions in the Visual Cortex.

Representing multiple agents and their mutual relations is a prerequisite to understand social events such as interactions. Using functional magnetic resonance imaging on human adults, we show that visual areas dedicated to body form and body motion perception contribute to processing social events, by holding the representation of multiple moving bodies and encoding the spatial relations between them. In particular, seeing animations of human bodies facing and moving toward (vs. away from) each other increased neural activity in the body-selective cortex [extrastriate body area (EBA)] and posterior superior temporal sulcus (pSTS) for biological motion perception. In those areas, representation of body postures and movements, as well as of the overall scene, was more accurate for facing body (vs. nonfacing body) stimuli. Effective connectivity analysis with dynamic causal modeling revealed increased coupling between EBA and pSTS during perception of facing body stimuli. The perceptual enhancement of multiple-body scenes featuring cues of interaction (i.e., face-to-face positioning, spatial proximity, and approaching signals) was supported by the participants' better performance in a recognition task with facing body versus nonfacing body stimuli. Thus, visuospatial cues of interaction in multiple-person scenarios affect the perceptual representation of body and body motion and, by promoting functional integration, streamline the process from body perception to action representation.

The Representation of Two-Body Shapes in the Human Visual Cortex.

Human social nature has shaped visual perception. A signature of the relationship between vision and sociality is a particular visual sensitivity to social entities such as faces and bodies. We asked whether human vision also exhibits a special sensitivity to spatial relations that reliably correlate with social relations. In general, interacting people are more often situated face-to-face than back-to-back. Using functional MRI and behavioral measures in female and male human participants, we show that visual sensitivity to social stimuli extends to images including two bodies facing toward (vs away from) each other. In particular, the inferior lateral occipital cortex, which is involved in visual-object perception, is organized such that the inferior portion encodes the number of bodies (one vs two) and the superior portion is selectively sensitive to the spatial relation between bodies (facing vs nonfacing). Moreover, functionally localized, body-selective visual cortex responded to facing bodies more strongly than identical, but nonfacing, bodies. In this area, multivariate pattern analysis revealed an accurate representation of body dyads with sharpening of the representation of single-body postures in facing dyads, which demonstrates an effect of visual context on the perceptual analysis of a body. Finally, the cost of body inversion (upside-down rotation) on body recognition, a behavioral signature of a specialized mechanism for body perception, was larger for facing versus nonfacing dyads. Thus, spatial relations between multiple bodies are encoded in regions for body perception and affect the way in which bodies are processed.SIGNIFICANCE STATEMENT Human social nature has shaped visual perception. Here, we show that human vision is not only attuned to socially relevant entities, such as bodies, but also to socially relevant spatial relations between those entities. Body-selective regions of visual cortex respond more strongly to multiple bodies that appear to be interacting (i.e., face-to-face), relative to unrelated bodies, and more accurately represent single body postures in interacting scenarios. Moreover, recognition of facing bodies is particularly susceptible to perturbation by upside-down rotation, indicative of a particular visual sensitivity to the canonical appearance of facing bodies. This encoding of relations between multiple bodies in areas for body-shape recognition suggests that the visual context in which a body is encountered deeply affects its perceptual analysis.

Seeing social events: The visual specialization for dyadic human-human interactions.

Detection and recognition of social interactions unfolding in the surroundings is as vital as detection and recognition of faces, bodies, and animate entities in general. We have demonstrated that the visual system is particularly sensitive to a configuration with two bodies facing each other as if interacting. In four experiments using backward masking on healthy adults, we investigated the properties of this dyadic visual representation. We measured the inversion effect (IE), the cost on recognition, of seeing bodies upside-down as opposed to upright, as an index of visual sensitivity: the greater the visual sensitivity, the greater the IE. The IE was increased for facing (vs. nonfacing) dyads, whether the head/face direction was visible or not, which implies that visual sensitivity concerns two bodies, not just two faces/heads. Moreover, the difference in IE for facing versus nonfacing dyads disappeared when one body was replaced by another object. This implies selective sensitivity to a body facing another body, as opposed to a body facing anything. Finally, the IE was reduced when reciprocity was eliminated (one body faced another, but the latter faced away). Thus, the visual system is sensitive selectively to dyadic configurations that approximate a prototypical social exchange with two bodies spatially close and mutually accessible to one another. These findings reveal visual configural representations encompassing multiple objects, which could provide fast and automatic parsing of complex relationships beyond individual faces or bodies. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Computational Feature Analysis of Body Movements Reveals Hierarchical Brain Organization.

Social species spend considerable time observing the body movements of others to understand their actions, predict their emotions, watch their games, or enjoy their dance movements. Given the important information obtained from body movements, we still know surprisingly little about the details of brain mechanisms underlying movement perception. In this fMRI study, we investigated the relations between movement features obtained from automated computational analyses of video clips and the corresponding brain activity. Our results show that low-level computational features map to specific brain areas related to early visual- and motion-sensitive regions, while mid-level computational features are related to dynamic aspects of posture encoded in occipital-temporal cortex, posterior superior temporal sulcus and superior parietal lobe. Furthermore, behavioral features obtained from subjective ratings correlated with activity in higher action observation regions. Our computational feature-based analysis suggests that the neural mechanism of movement encoding is organized in the brain not so much by semantic categories than by feature statistics of the body movements.