Category-selective neural decreases in the human ventral occipito-temporal cortex as defined with intracranial...

Visual recognition is supported in humans by category-selective neural activity in the ventral occipito-temporal cortex (VOTC). While category-selectivity is generally defined as an increase in neural activity (i.e., larger responses) for a given visual category of interest, category-selective decreases have also been reported yet generally ignored. Here we use electrophysiological intracerebral recordings across the VOTC of a large human sample (N = 140; >11k recording sites) to characterize and compare category-selective neural decreases relative to increases, in response to images of faces. Face-selective high frequency broadband (HFB: 30-160 Hz) neural activity elicited by natural images of faces periodically embedded in a train of nonface objects was objectively quantified in the frequency-domain, then defined as increases or decreases in the time-domain, revealing quantitative and qualitative differences between the two types of responses. About 40% of the recording sites reflect category-selective decreases that are spatially distinct from increases, being distributed more posteriorly and medially in the VOTC, without the characteristic right hemispheric lateralization of increases and an overall weaker signal amplitude. While category-exclusive increases are frequently encountered especially in the anterior temporal lobe, category-exclusive decreases are rare at the neural population level. Category-selective decreases are largely concurrent with increases, yet emerging slightly later and of shorter duration, with population-level increases arguably playing a more significant function in visual recognition. While a majority of signal decreases appear to reflect reduced activity to face than to non-face images, a sizeable proportion of signal decreases potentially manifest category-selective inhibition. Our findings of large-scale category-selective decreases in human VOTC suggest that these responses play a role in visual recognition distinct from neural response increase, including potential category-selective inhibition.