Distinct mechanisms of face representation by enhancive and suppressive neurons of the inferior temporal cortex

Face-selective neurons in the inferior temporal (IT) cortex respond to faces by either increasing (ENH) or decreasing (SUP) their spiking activities compared with their baseline. Although nearly half of IT face neurons are selectively suppressed by face stimulation, their role in face representation is not clear. To address this issue, we recorded the spiking activities and local field potential (LFP) from IT cortex of three monkeys while they viewed a large set of visual stimuli. LFP high-gamma (HG-LFP) power indicated the presence of both ENH and SUP face-selective neural clusters in IT cortex. The magnitude of HG-LFP power of the recording sites was correlated with the magnitude of change in the evoked spiking activities of its constituent neurons for both ENH and SUP face clusters. Spatial distribution of the ENH and SUP face clusters suggests the presence of a complex and heterogeneous face hypercluster organization in IT cortex. Importantly, ENH neurons conveyed more face category and SUP neurons conveyed more face identity information at both the single-unit and neuronal population levels. Onset and peak of suppressive single-unit, neuronal population, and HG-LFP power activities lagged those of the ENH ones. These results demonstrate that IT neuronal code for face representation is optimized by increasing sparseness through selective suppression of a subset of face neurons. We suggest that IT cortex contains spatial clusters of both ENH and SUP face neurons with distinct specialized functional role in face representation. NEW & NOTEWORTHY Electrophysiological and imaging studies have suggested that face information is encoded by a network of clusters of enhancive face-selective neurons in the visual cortex of man and monkey. We show that nearly half of face-selective neurons are suppressed by face stimulation. The suppressive neurons form spatial clusters and convey more face identity information than the enhancive face neurons. Our results suggest the presence of two neuronal subsystems for coarse and fine face information processing.