Distributed network processes account for the majority of variance in localized visual category selectivity

Abstract

A central goal of neuroscience is to understand how function-relevant brain activations are generated. Here we test the hypothesis that function-relevant brain activations are generated primarily by distributed network flows. We focused on visual processing in human cortex, given the long-standing literature supporting the functional relevance of brain activations in visual cortex regions exhibiting visual category selectivity. We began by using fMRI data from N=352 human participants to identify category-specific responses in visual cortex for images of faces, places, body parts, and tools. We then systematically tested the hypothesis that distributed network flows can generate these localized visual category selective responses. This was accomplished using a recently developed approach for simulating - in a highly empirically constrained manner - the generation of task-evoked brain activations by modeling activity flowing over intrinsic brain connections. We next tested refinements to our hypothesis, focusing on how stimulus-driven network interactions initialized in V1 generate downstream visual category selectivity. We found evidence that network flows directly from V1 were sufficient for generating visual category selectivity, but that additional, globally distributed (whole-cortex) network flows increased category selectivity further. Using null network architectures we also found that each regions unique intrinsic "connectivity fingerprint" was key to the generation of category selectivity. These results generalized across regions associated with all four visual categories tested (bodies, faces, places, and tools), and provide evidence that the human brains intrinsic network organization plays a prominent role in the generation of functionally relevant, localized responses. Author SummaryA fundamental question in neuroscience has persisted for over a century: to what extent do distributed processes drive brain function? The existence of category-selective regions within visual cortex provides long-standing evidence supporting localized computations, wherein specialized functions (e.g., selective responsiveness to face images) are thought to be primarily generated by within-region processes. This account was recently updated to include category selectivity dispersed across visual cortex, in the absence of category-selective regions. Here we provide groundwork evidence demonstrating that locally-exhibited visual-category-selective responses can be accurately generated via distributed activity flowing over globally connected systems. These processes were simulated via empirically-based computational models initialized by stimulus-evoked activity patterns and empirical connectivity matching each category-selective regions unique intrinsic functional connectivity fingerprint. Results demonstrate that activity flowing over the human brains distributed network architecture can account for the generation of category selectivity in visual cortex regions.