Saloni Sharma¹ (), Margaret Livingstone¹; ¹Harvard Medical School

Faces convey essential information about identity and expression, which are central to social communication. Decades of research have shown that face-selective regions in the primate inferotemporal (IT) cortex are involved in such aspects of visual face processing. Previous work has shown that monkeys raised without seeing faces instead develop a behavioral preference and IT neural selectivity for the socially relevant and experienced stimuli - hands. This is dramatically different from control monkeys who, like humans, prioritize looking at faces and show neural face-only selectivity. This divergence raises an important question: how does early sensory deprivation impact core IT functions, such as facial expression and identity processing? Here, we conducted behavioral and electrophysiological experiments with three such monkeys 2, 3 or 5 years after re-exposure to faces and three typically reared monkeys. To measure behavioral preferences, monkeys freely viewed image pairs of faces, hands or objects. To investigate neural selectivity, we presented the monkeys with images of faces, hands and objects while monkeys passively fixated. Finally, to investigate facial expression and identity tuning, we presented 18 monkey identities and two expressions – threat and neutral. Behaviorally, the monkeys with 2-3 years of face experience still retain a hand bias when freely viewing images, while the monkey with five years of face experience recovered from the hand bias. However, the IT neurons of all three monkeys never developed normal face selectivity, instead showing mixed selectivity for faces and hands. Further, while we could successfully decode facial identity information across expression and vice-versa in control monkeys, all three face-deprived monkeys failed to show significant expression or identity tuning. These findings suggest that early sensory deprivation disrupts the normal development of neural mechanisms underlying face processing in higher-order visual cortex, highlighting the importance of early experiences in shaping the social brain.

Acknowledgements: R01 EY025670; William Randolph Hearst Fund