The neural basis of rapid unfamiliar face individuation with human intracerebral recordings

Rapid individuation of conspecifics' faces is ecologically important in the human species, whether the face belongs to a familiar or unfamiliar individual. Here we tested a large group (N = 69) of epileptic patients implanted with intracerebral electrodes throughout the ventral occipito-temporal cortex (VOTC). We used a frequency-tagging visual stimulation paradigm optimized to objectively measure face individuation with direct neural recordings. This enabled providing an extensive map of the significantly larger neural responses to upright than to inverted unfamiliar faces, i.e. reflecting visual face individuation processes that go beyond physical image differences. These high-level face individuation responses are both distributed and anatomically confined to a strip of cortex running from the inferior occipital gyrus all along the lateral fusiform gyrus, with a large right hemispheric dominance. Importantly, face individuation responses are limited anteriorly to the bilateral anterior fusiform gyrus and surrounding sulci, with a near absence of significant responses in the extensively sampled temporal pole. This large-scale mapping provides original evidence that face individuation is supported by a distributed yet anatomically constrained population of neurons in the human VOTC, and highlights the importance of probing this function with face stimuli devoid of associated semantic, verbal and affective information.