People-selectivity, audiovisual integration and heteromodality in the superior temporal sulcus

The functional role of the superior temporal sulcus (STS) has been implicated in a number of studies, including those investigating face perception, voice perception, and face–voice integration. However, the nature of the STS preference for these ‘social stimuli’ remains unclear, as does the location within the STS for specific types of information processing. The aim of this study was to directly examine properties of the STS in terms of selective response to social stimuli. We used functional magnetic resonance imaging (fMRI) to scan participants whilst they were presented with auditory, visual, or audiovisual stimuli of people or objects, with the intention of localising areas preferring both faces and voices (i.e., ‘people-selective’ regions) and audiovisual regions designed to specifically integrate person-related information. Results highlighted a ‘people-selective, heteromodal’ region in the trunk of the right STS which was activated by both faces and voices, and a restricted portion of the right posterior STS (pSTS) with an integrative preference for information from people, as compared to objects. These results point towards the dedicated role of the STS as a ‘social-information processing’ centre

Who is that? Brain networks and mechanisms for identifying individuals

Social animals can identify conspecifics by many forms of sensory input. However, whether the neuronal computations that support this ability to identify individuals rely on modality-independent convergence or involve ongoing synergistic interactions along the multiple sensory streams remains controversial. Direct neuronal measurements at relevant brain sites could address such questions, but this requires better bridging the work in humans and animal models. Here, we overview recent studies in nonhuman primates on voice and face identity-sensitive pathways and evaluate the correspondences to relevant findings in humans. This synthesis provides insights into converging sensory streams in the primate anterior temporal lobe (ATL) for identity processing. Furthermore, we advance a model and suggest how alternative neuronal mechanisms could be tested

Reduced neural sensitivity to social stimuli in infants at risk for autism

In the hope of discovering early markers of autism, attention has recently turned to the study of infants at risk owing to being the younger siblings of children with autism. Because the condition is highly heritable, later-born siblings of diagnosed children are at substantially higher risk for developing autism or the broader autism phenotype than the general population. Currently, there are no strong predictors of autism in early infancy and diagnosis is not reliable until around 3 years of age. Because indicators of brain functioning may be sensitive predictors, and atypical social interactions are characteristic of the syndrome, we examined whether temporal lobe specialization for processing visual and auditory social stimuli during infancy differs in infants at risk. In a functional near-infrared spectroscopy study, infants aged 4–6 months at risk for autism showed less selective neural responses to social stimuli (auditory and visual) than low-risk controls. These group differences could not be attributed to overall levels of attention, developmental stage or chronological age. Our results provide the first demonstration of specific differences in localizable brain function within the first 6 months of life in a group of infants at risk for autism. Further, these differences closely resemble known patterns of neural atypicality in children and adults with autism. Future work will determine whether these differences in infant neural responses to social stimuli predict either later autism or the broader autism phenotype frequently seen in unaffected family members

Developmental changes in infant brain activity during naturalistic social experiences

Between 6 and 12 months, typically developing infants undergo a socio-cognitive ‘revolution’. The Interactive Specialization (IS) theory of brain development predicts that these behavioral changes will be underpinned by developmental increases in the power and topographic extent of socially selective cortical responses. To test this hypothesis, we used EEG to examine developmental changes in cortical selectivity for ecologically valid dynamic social versus non-social stimuli in a large cohort of 6- and 12-month-old infants. Consistent with the Interactive Specialization model, results showed that differences in EEG theta activity between social and non-social stimuli became more pronounced and widespread with age. Differences in EEG activity were most clearly elicited by a live naturalistic interaction, suggesting that measuring brain activity in ecologically valid contexts is central to mapping social brain development in infancy

Specialized Signals for Spatial Attention in the Ventral and Dorsal Visual Streams

Neuroscientists have traditionally conceived the visual system as having a ventral stream of vision for perception and a dorsal one associated with vision for action. However functional differences between them have become relatively blurred in recent years, not the least by the systematic parallel mapping of functions allowed by functional magnetic resonance imaging (fMRI). Here, using fMRI to simultaneously monitor several brain regions, we first studied a hallmark ventral stream computation: the processing of faces. We did so by probing responses to motion, an attribute whose processing is typically associated with the dorsal stream. In humans, it is known that face-selective regions in the superior temporal sulcus (STS) show enhanced responses to facial motion that are absent in the rest of the face-processing system. In macaques, face areas also exist, but their functional specializations for facial motion are unknown. We showed static and moving face and non-face objects to macaques and humans in an fMRI experiment in order to isolate potential functional specializations in the ventral stream face-processing system and to motivate putative homologies across species. Our results revealed all macaque face areas showed enhanced responses to moving faces. There was a difference between more dorsal face areas in the fundus of the STS, which are embedded in motion responsive cortex and ventral ones, where enhanced responses to motion interacted with object category and could not be explained by their proximity to motion responsive cortex. In humans watching the same stimuli, only the STS face area showed an enhancement for motion. These results suggest specializations for motion exist in the macaque face-processing network but they do not lend themselves to a direct equalization between human and macaque face areas. We then proceeded to compare ventral and dorsal stream functions in terms of their code for spatial attention, whose control was typically associated with the dorsal stream and prefrontal areas. We took advantage of recent fMRI studies that provide a systematic map of cortical areas modulated by spatial attention and suggest PITd, a ventral stream area in the temporal lobe, can support endogenous attention control. Covert attention and stimulus selection by saccades are represented in the same maps of visual space in attention control areas. Difficulties interpreting this multiplicity of functions led to the proposal that they encode priority maps, where multiple sources are summed to form a single priority signal, agnostic as to its eventual use by downstream areas. Using a paradigm that dissociates covert attention and response selection, we test this hypothesis with fMRI-guided electrophysiology in two cortical areas: parietal area LIP, where the priority map was first proposed to apply, and temporal area PITd. Our results indicate LIP sums disparate signals, but as a consequence independent channels of spatial information exist for attention and response planning. PITd represents relevant locations and, rather than summing signals, contains a single map for covert attention. Our findings have the potential to resolve a longstanding controversy about the nature of spatial signals in LIP and establish PITd as a robust map for covert attention in the ventral stream. Together, our results suggest that while the distribution of labor between ventral stream and dorsal stream areas is less linear than what a what a rough depiction of them can suggest, it is illuminated by their proposed function as supporting vision for perception and vision for action respectively

Neural Univariate Activity and Multivariate Pattern in the Posterior Superior Temporal Sulcus Differentially Encode Facial Expression and Identity

Faces contain a variety of information such as one’s identity and expression. One prevailing model suggests a functional division of labor in processing faces that different aspects of facial information are processed in anatomically separated and functionally encapsulated brain regions. Here, we demonstrate that facial identity and expression can be processed in the same region, yet with different neural coding strategies. To this end, we employed functional magnetic resonance imaging to examine two types of coding schemes, namely univariate activity and multivariate pattern, in the posterior superior temporal cortex (pSTS) - a face-selective region that is traditionally viewed as being specialized for processing facial expression. With the individual difference approach, we found that participants with higher overall face selectivity in the right pSTS were better at differentiating facial expressions measured outside of the scanner. In contrast, individuals whose spatial pattern for faces in the right pSTS was less similar to that for objects were more accurate in identifying previously presented faces. The double dissociation of behavioral relevance between overall neural activity and spatial neural pattern suggests that the functional-division-of-labor model on face processing is over-simplified, and that coding strategies shall be incorporated in a revised model

Event-related alpha suppression in response to facial motion

This article has been made available through the Brunel Open Access Publishing Fund.While biological motion refers to both face and body movements, little is known about the visual perception of facial motion. We therefore examined alpha wave suppression as a reduction in power is thought to reflect visual activity, in addition to attentional reorienting and memory processes. Nineteen neurologically healthy adults were tested on their ability to discriminate between successive facial motion captures. These animations exhibited both rigid and non-rigid facial motion, as well as speech expressions. The structural and surface appearance of these facial animations did not differ, thus participants decisions were based solely on differences in facial movements. Upright, orientation-inverted and luminance-inverted facial stimuli were compared. At occipital and parieto-occipital regions, upright facial motion evoked a transient increase in alpha which was then followed by a significant reduction. This finding is discussed in terms of neural efficiency, gating mechanisms and neural synchronization. Moreover, there was no difference in the amount of alpha suppression evoked by each facial stimulus at occipital regions, suggesting early visual processing remains unaffected by manipulation paradigms. However, upright facial motion evoked greater suppression at parieto-occipital sites, and did so in the shortest latency. Increased activity within this region may reflect higher attentional reorienting to natural facial motion but also involvement of areas associated with the visual control of body effectors. © 2014 Girges et al

Effects of Temporal and Spatial Context Within the Macaque Face-Processing System

Temporal and spatial context play a key role in vision as a whole, and in face perception specifically. However, little is known about the neurophysiological mechanisms by which contextual cues exert their effects. Anatomically distinct face patches in the macaque brain analyze facial form, and studies of the activity within these patches have begun to clarify the neural machinery that underlies facial perception. This system provides a uniquely valuable opportunity to study how context affects the perception of form. We used functional magnetic resonance imaging (fMRI) to investigate the brain activity of macaque monkeys while they viewed faces placed in either temporal or spatial context. Facial motion transmits rich and ethologically vital information, but the way that the brain interprets such natural temporal context is poorly understood. Facial motion activates the face patches and surrounding areas, yet it is not known whether this motion is processed by its own specialized neural machinery, and if so, what that machinery’s organization might be. To address these questions, we monitored the brain activity of macaque monkeys while they viewed low- and high-level motion and form stimuli. We found that, beyond classical motion areas and the known face patch system, moving faces recruited a heretofore-unrecognized face patch. Although all face patches displayed distinctive selectivity for face motion over object motion, only two face patches preferred naturally moving faces, while three others preferred randomized, rapidly varying sequences of facial form. This functional divide was anatomically specific, segregating dorsal from ventral face patches, thereby revealing a new organizational principle of the macaque face-processing system. Like facial motion, bodies can provide valuable social context, revealing emotion and identity. Little is known about the joint processing of faces and bodies, even though there is reason to believe that their neural representations are intertwined. To identify interaction between the neural representations of face and body, we monitored the brain activity of the same monkeys while they viewed pictures of whole monkeys, isolated monkey heads, and isolated monkey bodies. We found that certain areas, including anterior face patches, responded more to whole monkeys than would be predicted by summing the separate responses to isolated heads and isolated bodies. The supralinear response was specific to viewing the conjunction of head and body; heads placed atop nonbody objects did not evoke this activity signature. However, a supralinear context response was elicited by pixelated, ambiguous faces presented on bodies. The size of this response suggests that the supralinear signal in this case did not result from the disambiguation of the ambiguous faces. These studies of contextually evoked activity within the macaque face processing system deepen our understanding of the cortical organization of both visual context and face processing, and identify promising sites for future research into the mechanisms underlying these critical aspects of perception

Network Interactions Explain Sensitivity to Dynamic Faces in the Superior Temporal Sulcus

The superior temporal sulcus (STS) in the human and monkey is sen-sitive to the motion of complex forms such as facial and bodily actions. We used functional magnetic resonance imaging (fMRI) to explore network-level explanations for how the form and motion information in dynamic facial expressions might be combined in the human STS. Ventral occipitotemporal areas selective for facial form were localized in occipital and fusiform face areas (OFA and FFA), and motion sensitivity was localized in the more dorsal temporal area V5. We then tested various connectivity models that modeled communication between the ventral form and dorsal motion path-ways. We show that facial form information modulated transmission of motion information from V5 to the STS, and that this face-selective modulation likely originated in OFA. This finding shows that form-selective motion sensitivity in the STS can be explained in terms of modulation of gain control on information flow in the motion pathway, and provides a substantial constraint for theories of the perception of faces and biological motion