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We compared neural responses to naturalistic videos and representations in deep network models trained with static and dynamic information. Models trained with dynamic information showed greater correspondence with neural representations in all brain regions, including those previously associated with the processing of static information. Among the models trained with dynamic information, those based on optic flow accounted for unique variance in neural responses that were not captured by Masked Autoencoders. This effect was strongest in ventral and dorsal brain regions, indicating that despite the Masked Autoencoders’ effectiveness at a variety of tasks, their representations diverge from representations in the human brain in the early stages of visual processing. 

Category selectivity is a fundamental principle of organization of perceptual brain regions. Human occipitotemporal cortex is subdivided into areas that respond preferentially to faces, bodies, artifacts, and scenes. However, observers need to combine information about objects from different categories to form a coherent understanding of the world. How is this multicategory information encoded in the brain? Studying the multivariate interactions between brain regions of male and female human subjects with fMRI and artificial neural networks, we found that the angular gyrus shows joint statistical dependence with multiple category-selective regions. Adjacent regions show effects for the combination of scenes and each other category, suggesting that scenes provide a context to combine information about the world. Additional analyses revealed a cortical map of areas that encode information across different subsets of categories, indicating that multicategory information is not encoded in a single centralized location, but in multiple distinct brain regions. SIGNIFICANCE STATEMENTMany cognitive tasks require combining information about entities from different categories. However, visual information about different categorical objects is processed by separate, specialized brain regions. How is the joint representation from multiple category-selective regions implemented in the brain? Using fMRI movie data and state-of-the-art multivariate statistical dependence based on artificial neural networks, we identified the angular gyrus encoding responses across face-, body-, artifact-, and scene-selective regions. Further, we showed a cortical map of areas that encode information across different subsets of categories. These findings suggest that multicategory information is not encoded in a single centralized location, but at multiple cortical sites which might contribute to distinct cognitive functions, offering insights to understand integration in a variety of domains. 

Recent neuroimaging evidence challenges the classical view that face identity and facial expression are processed by segregated neural pathways, showing that information about identity and expression are encoded within common brain regions. This article tests the hypothesis that integrated representations of identity and expression arise spontaneously within deep neural networks. A subset of the CelebA dataset is used to train a deep convolutional neural network (DCNN) to label face identity (chance = 0.06%, accuracy = 26.5%), and the FER2013 dataset is used to train a DCNN to label facial expression (chance = 14.2%, accuracy = 63.5%). The identity-trained and expression-trained networks each successfully transfer to labeling both face identity and facial expression on the Karolinska Directed Emotional Faces dataset. This study demonstrates that DCNNs trained to recognize face identity and DCNNs trained to recognize facial expression spontaneously develop representations of facial expression and face identity, respectively. Furthermore, a congruence coefficient analysis reveals that features distinguishing between identities and features distinguishing between expressions become increasingly orthogonal from layer to layer, suggesting that deep neural networks disentangle representational subspaces corresponding to different sources. 

A large body of past work has sought to identify the underlying dimensions that capture our trait knowledge of other people. However, the importance of particular traits in determining our overall impressions of others is not well understood, and different traits may be fundamental for impressions of famous versus unfamiliar people. For instance, we may focus on competence when evaluating a famous person, but on trustworthiness when evaluating a stranger. To examine the structure of overall impressions of famous people and of unfamiliar people, we probed the contributions of 13 different trait judgments to perceived similarity judgments. We found that different sets of traits best predicted perceived similarity between famous people versus between unfamiliar people; however, the relationship between each trait and perceived similarity generalized to some extent from famous people to unfamiliar people, suggesting a degree of overlap in the structure of overall impressions. 

According to a classical view of face perception (Bruce and Young, 1986; Haxby et al., 2000), face identity and facial expression recognition are performed by separate neural substrates (ventral and lateral temporal face-selective regions, respectively). However, recent studies challenge this view, showing that expression valence can also be decoded from ventral regions (Skerry and Saxe, 2014; Li et al., 2019), and identity from lateral regions (Anzellotti and Caramazza, 2017). These findings could be reconciled with the classical view if regions specialized for one task (either identity or expression) contain a small amount of information for the other task (that enables above-chance decoding). In this case, we would expect representations in lateral regions to be more similar to representations in deep convolutional neural networks (DCNNs) trained to recognize facial expression than to representations in DCNNs trained to recognize face identity (the converse should hold for ventral regions). We tested this hypothesis by analyzing neural responses to faces varying in identity and expression. Representational dissimilarity matrices (RDMs) computed from human intracranial recordings (n= 11 adults; 7 females) were compared with RDMs from DCNNs trained to label either identity or expression. We found that RDMs from DCNNs trained to recognize identity correlated with intracranial recordings more strongly in all regions tested—even in regions classically hypothesized to be specialized for expression. These results deviate from the classical view, suggesting that face-selective ventral and lateral regions contribute to the representation of both identity and expression. SIGNIFICANCE STATEMENTPrevious work proposed that separate brain regions are specialized for the recognition of face identity and facial expression. However, identity and expression recognition mechanisms might share common brain regions instead. We tested these alternatives using deep neural networks and intracranial recordings from face-selective brain regions. Deep neural networks trained to recognize identity and networks trained to recognize expression learned representations that correlate with neural recordings. Identity-trained representations correlated with intracranial recordings more strongly in all regions tested, including regions hypothesized to be expression specialized in the classical hypothesis. These findings support the view that identity and expression recognition rely on common brain regions. This discovery may require reevaluation of the roles that the ventral and lateral neural pathways play in processing socially relevant stimuli. 

Cognitive tasks engage multiple brain regions. Studying how these regions interact is key to understand the neural bases of cognition. Standard approaches to model the interactions between brain regions rely on univariate statistical dependence. However, newly developed methods can capture multivariate dependence. Multivariate pattern dependence (MVPD) is a powerful and flexible approach that trains and tests multivariate models of the interactions between brain regions using independent data. In this article, we introduce PyMVPD: an open source toolbox for multivariate pattern dependence. The toolbox includes linear regression models and artificial neural network models of the interactions between regions. It is designed to be easily customizable. We demonstrate example applications of PyMVPD using well-studied seed regions such as the fusiform face area (FFA) and the parahippocampal place area (PPA). Next, we compare the performance of different model architectures. Overall, artificial neural networks outperform linear regression. Importantly, the best performing architecture is region-dependent: MVPD subdivides cortex in distinct, contiguous regions whose interaction with FFA and PPA is best captured by different models. 

Abstract Here, we propose a novel technique to investigate nonlinear interactions between brain regions that captures both the strength and type of the functional relationship. Inspired by the field of functional analysis, we propose that the relationship between activity in separate brain areas can be viewed as a point in function space, identified by coordinates along an infinite set of basis functions. Using Hermite polynomials as bases, we estimate a subset of these values that serve as “functional coordinates,” characterizing the interaction between BOLD activity across brain areas. We provide a proof of the convergence of the estimates in the limit, and we validate the method with simulations in which the ground truth is known, additionally showing that functional coordinates detect statistical dependence even when correlations (“functional connectivity”) approach zero. We then use functional coordinates to examine neural interactions with a chosen seed region: the fusiform face area (FFA). Using k-means clustering across each voxel’s functional coordinates, we illustrate that adding nonlinear basis functions allows for the discrimination of interregional interactions that are otherwise grouped together when using only linear dependence. Finally, we show that regions in V5 and medial occipital and temporal lobes exhibit significant nonlinear interactions with the FFA. 

Recent neural evidence challenges the traditional view that face identity and facial expressions are processed by segregated neural pathways, showing that information about identity and expression are encoded within common brain regions. This article tests the hypothesis that integrated representations of identity and expression arise naturally within neural networks. Deep networks trained to recognize expression and deep networks trained to recognize identity spontaneously develop representations of identity and expression, respectively. These findings serve as a “proof-of-concept” that it is not necessary to discard task-irrelevant information for identity and expression recognition.