Intracerebral electrical stimulation to understand the neural basis of human face identity recognition.

Abstract

Recognizing people's identity by their faces is a key function in the human species, supported by regions of the ventral occipito-temporal cortex (VOTC). In the last decade, there have been several reports of perceptual face distortion during direct electrical stimulation (DES) with subdural electrodes positioned over a well-known face-selective VOTC region of the right lateral middle fusiform gyrus (LatMidFG; i.e., the "Fusiform Face Area", FFA). However, transient impairments of face identity recognition (FIR) have been extremely rare and only behaviorally quantified during DES with intracerebral (i.e., depth) electrodes in stereo-electroencephalography (SEEG). The three detailed cases reported so far, summarized here, were specifically impaired at FIR during DES inside different anatomical VOTC regions of the right hemisphere: the inferior occipital gyrus (IOG) and the LatMidFG, as well as a region that lies at the heart of a large magnetic susceptibility artifact in functional magnetic resonance imaging (fMRI): the anterior fusiform gyrus (AntFG). In the first two regions, the eloquent electrode contacts were systematically associated with the highest face-selective and (unfamiliar) face individuation responses as measured with intracerebral electrophysiology. Stimulation in the right AntFG did not lead to perceptual changes but also caused an inability to remember having been presented face pictures, as if the episode was never recorded in memory. These observations support the view of an extensive network of face-selective VOTC regions subtending human FIR, with at least three critical nodes in the right hemisphere associated with differential intrinsic and extrinsic patterns of reentrant connectivity.