Dissociated face- and word-selective intracerebral responses in the human ventral occipito-temporal cortex

Abstract

The extent to which faces and written words share neural circuitry in the human brain is actively debated. Here we compared face-selective and word-selective responses in a large group of patients (N = 37) implanted with intracerebral depth electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. nonface visual objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated through frequency-tagging. Critically, this sensitive approach allows to objectively quantify category-selective neural responses and disentangle them from general visual responses. About 70% of significant contacts show either only face-selectivity or only word-selectivity, with the expected right and left hemispheric dominance, respectively. Spatial dissociations are also found within core regions of face and word processing, with a medio-lateral dissociation in the fusiform gyrus (FG) and surrounding sulci, while a postero-anterior dissociation is found in the inferior occipital gyrus (IOG). Only 30% of the significant contacts show both face- and word-selective responses. Critically, in these contacts, across the VOTC or in the FG and surrounding sulci, between-category selective-amplitudes (faces vs. words) showed no-to-weak correlations, despite strong correlations in both the within-category selective amplitudes (face-face, word-word) and the general visual responses to words and faces. Overall, we conclude that category-selectivity for faces and written words is largely dissociated in the human VOTC. Significance StatementIn modern human societies, faces and written words have become arguably the most significant stimuli of the visual environment. Despite extensive research in neuropsychology, electroencephalography and neuroimaging over the past three decades, whether these two types of visual signals are recognized by similar or dissociated processes and neural networks remains unclear. Here we provide an original contribution to this outstanding scientific issue by directly comparing frequency-tagged face- and word-selective neural responses in a large group of epileptic patients implanted with intracerebral electrodes covering the ventral occipito-temporal cortex. While general visual responses to words and faces show significant overlap, the respective category-selective responses are neatly dissociated in spatial location and magnitude, pointing to largely dissociated processes and neural networks.