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. We provide an original contribution to this debate by comparing face-selective and word-selective responses in a large group of patients (N=37) implanted with intracerebral electrodes in the ventral occipito-temporal cortex (VOTC). Both face-selective (i.e., significantly different responses to faces vs. nonface objects) and word-selective (i.e., significantly different responses to words vs. pseudofonts) neural activity is isolated through frequency-tagging (Jonas et al., 2016; Lochy et al., 2018, respectively). Critically, this approach allows disentangling category-selective neural responses from general visual responses. Overall, we find that 69.26% of significant contacts show either face- or word-selectivity, with the expected right and left hemispheric dominance, respectively (Fig.1A,B). Moreover, the center of mass for word-contacts is more lateral than for face-contacts, with no differences in postero-anterior axis (Fig.2A). 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 (FG+sulci;Fig.2B), while a postero-anterior dissociation is found in the inferior occipital gyrus (IOG;Fig.2C). Despite their spatial dissociations in the FG+sulci and IOG, most overlap in category-selective responses is found in these regions (Fig.1C). Critically, in the overlap-contacts, across the whole brain or specifically in the FG+sulci, between-category (word-face) selective-amplitudes showed no-to-weak correlations, despite strong correlations for within-category (face-face, word-word) selective-amplitudes (Fig.3A), and a strong correlation in non-selective general-amplitudes to words-faces. Moreover, substantial overlap and no-to-weak correlations were observed between faces and a control category (houses) known to be functionally dissociated from faces. Overall, we conclude that category-selectivity for faces and words is largely dissociated in the human VOTC, with a limited spatial overlap likely due to the distant recording of dissociated populations of neurons rather than to shared category-selective representations.