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Participant-specific, functionally defined brain areas are usually mapped with functional localizers and estimated by making contrasts between responses to single categories of input. Naturalistic stimuli engage multiple brain systems in parallel, provide more ecologically plausible estimates of real-world statistics, and are friendly to special populations. The current study shows that cortical functional topographies in individual participants can be estimated with high fidelity from naturalistic stimuli. Importantly, we demonstrate that robust, individualized estimates can be obtained even when participants watched different movies, were scanned with different parameters/scanners, and were sampled from different institutes across the world. Our results create a foundation for future studies that allow researchers to estimate a broad range of functional topographies based on naturalistic movies and a normative database, making it possible to integrate high-level cognitive functions across datasets from laboratories worldwide. 

Abstract Quantifying how brain functional architecture differs from person to person is a key challenge in human neuroscience. Current individualized models of brain functional organization are based on brain regions and networks, limiting their use in studying fine-grained vertex-level differences. In this work, we present the individualized neural tuning (INT) model, a fine-grained individualized model of brain functional organization. The INT model is designed to have vertex-level granularity, to capture both representational and topographic differences, and to model stimulus-general neural tuning. Through a series of analyses, we demonstrate that (a) our INT model provides a reliable individualized measure of fine-grained brain functional organization, (b) it accurately predicts individualized brain response patterns to new stimuli, and (c) for many benchmarks, it requires only 10–20 minutes of data for good performance. The high reliability, specificity, precision, and generalizability of our INT model affords new opportunities for building brain-based biomarkers based on naturalistic neuroimaging paradigms. 

Deep convolutional neural networks (DCNNs) trained for face identification can rival and even exceed human-level performance. The ways in which the internal face representations in DCNNs relate to human cognitive representations and brain activity are not well understood. Nearly all previous studies focused on static face image processing with rapid display times and ignored the processing of naturalistic, dynamic information. To address this gap, we developed the largest naturalistic dynamic face stimulus set in human neuroimaging research (700+ naturalistic video clips of unfamiliar faces). We used this naturalistic dataset to compare representational geometries estimated from DCNNs, behavioral responses, and brain responses. We found that DCNN representational geometries were consistent across architectures, cognitive representational geometries were consistent across raters in a behavioral arrangement task, and neural representational geometries in face areas were consistent across brains. Representational geometries in late, fully connected DCNN layers, which are optimized for individuation, were much more weakly correlated with cognitive and neural geometries than were geometries in late-intermediate layers. The late-intermediate face-DCNN layers successfully matched cognitive representational geometries, as measured with a behavioral arrangement task that primarily reflected categorical attributes, and correlated with neural representational geometries in known face-selective topographies. Our study suggests that current DCNNs successfully capture neural cognitive processes for categorical attributes of faces but less accurately capture individuation and dynamic features. 

The functional connectome supports information transmission through the brain at various spatial scales, from exchange between broad cortical regions to finer-scale, vertex-wise connections that underlie specific information processing mechanisms. In adults, while both the coarse- and fine-scale functional connectomes predict cognition, the fine scale can predict up to twice the variance as the coarse-scale functional connectome. Yet, past brain-wide association studies, particularly using large developmental samples, focus on the coarse connectome to understand the neural underpinnings of individual differences in cognition. Using a large cohort of children (age 9–10 years;n = 1,115 individuals; both sexes; 50% female, including 170 monozygotic and 219 dizygotic twin pairs and 337 unrelated individuals), we examine the reliability, heritability, and behavioral relevance of resting-state functional connectivity computed at different spatial scales. We use connectivity hyperalignment to improve access to reliable fine-scale (vertex-wise) connectivity information and compare the fine-scale connectome with the traditional parcel-wise (coarse scale) functional connectomes. Though individual differences in the fine-scale connectome are more reliable than those in the coarse-scale, they are less heritable. Further, the alignment and scale of connectomes influence their ability to predict behavior, whereby some cognitive traits are equally well predicted by both connectome scales, but other, less heritable cognitive traits are better predicted by the fine-scale connectome. Together, our findings suggest there are dissociable individual differences in information processing represented at different scales of the functional connectome which, in turn, have distinct implications for heritability and cognition. 

Processes evoked by seeing a personally familiar face encompass recognition of visual appearance and activation of social and person knowledge. Whereas visual appearance is the same for all viewers, social and person knowledge may be more idiosyncratic. Using between-subject multivariate decoding of hyperaligned functional magnetic resonance imaging data, we investigated whether representations of personally familiar faces in different parts of the distributed neural system for face perception are shared across individuals who know the same people. We found that the identities of both personally familiar and merely visually familiar faces were decoded accurately across brains in the core system for visual processing, but only the identities of personally familiar faces could be decoded across brains in the extended system for processing nonvisual information associated with faces. Our results show that personal interactions with the same individuals lead to shared neural representations of both the seen and unseen features that distinguish their identities. 

Intelligent thought is the product of efficient neural information processing, which is embedded in fine-grained, topographically organized population responses and supported by fine-grained patterns of connectivity among cortical fields. Previous work on the neural basis of intelligence, however, has focused on coarse-grained features of brain anatomy and function because cortical topographies are highly idiosyncratic at a finer scale, obscuring individual differences in fine-grained connectivity patterns. We used a computational algorithm, hyperalignment, to resolve these topographic idiosyncrasies and found that predictions of general intelligence based on fine-grained (vertex-by-vertex) connectivity patterns were markedly stronger than predictions based on coarse-grained (region-by-region) patterns. Intelligence was best predicted by fine-grained connectivity in the default and frontoparietal cortical systems, both of which are associated with self-generated thought. Previous work overlooked fine-grained architecture because existing methods could not resolve idiosyncratic topographies, preventing investigation where the keys to the neural basis of intelligence are more likely to be found. 

Information that is shared across brains is encoded in idiosyncratic fine-scale functional topographies. Hyperalignment captures shared information by projecting pattern vectors for neural responses and connectivities into a common, high-dimensional information space, rather than by aligning topographies in a canonical anatomical space. Individual transformation matrices project information from individual anatomical spaces into the common model information space, preserving the geometry of pairwise dissimilarities between pattern vectors, and model cortical topography as mixtures of overlapping, individual-specific topographic basis functions, rather than as contiguous functional areas. The fundamental property of brain function that is preserved across brains is information content, rather than the functional properties of local features that support that content. In this Perspective, we present the conceptual framework that motivates hyperalignment, its computational underpinnings for joint modeling of a common information space and idiosyncratic cortical topographies, and discuss implications for understanding the structure of cortical functional architecture. 

Abstract How does STEM knowledge learned in school change students’ brains? Using fMRI, we presented photographs of real-world structures to engineering students with classroom-based knowledge and hands-on lab experience, examining how their brain activity differentiated them from their “novice” peers not pursuing engineering degrees. A data-driven MVPA and machine-learning approach revealed that neural response patterns of engineering students were convergent with each other and distinct from novices’ when considering physical forces acting on the structures. Furthermore, informational network analysis demonstrated that the distinct neural response patterns of engineering students reflected relevant concept knowledge: learned categories of mechanical structures. Information about mechanical categories was predominantly represented in bilateral anterior ventral occipitotemporal regions. Importantly, mechanical categories were not explicitly referenced in the experiment, nor does visual similarity between stimuli account for mechanical category distinctions. The results demonstrate how learning abstract STEM concepts in the classroom influences neural representations of objects in the world.