Behavioral and neural mechanisms of face-specific attention during goal-directed visual search.

Abstract

Goal-directed visual attention is a fundamental cognitive process that enables animals to selectively focus on specific regions of the visual field while filtering out irrelevant information. However, given the domain specificity of social behaviors, it remains unclear whether attention to faces versus non-faces recruits different neurocognitive processes. In this study, we simultaneously recorded activity from temporal and frontal nodes of the attention network while macaques performed a goal-directed visual search task. V4 and inferotemporal (IT) visual category-selective units, selected during cue presentation, discriminated fixations on targets and distractors during the search, but were differentially engaged by face and house targets. V4 and IT category-selective units also encoded fixation transitions and search dynamics. Compared to distractors, fixations on targets reduced spike-LFP coherence within the temporal cortex. Importantly, target-induced desynchronization between the temporal and prefrontal cortices was only evident for face targets, suggesting that attention to faces differentially engaged the prefrontal cortex. We further revealed bidirectional theta influence between the temporal and prefrontal cortices using Granger causality, which was again disproportionate for faces. Finally, we showed that the search became more efficient with increasing target-induced desynchronization. Together, our results suggest domain specificity for attending to faces and an intricate interplay between visual attention and social processing neural networks.Significance Statement Visual attention stands as a cornerstone in the tapestry of visual perception. This study explores the neurocognitive mechanisms underlying goal-directed visual attention, specifically in the context of social versus non-social stimuli. By simultaneously recording neural activity from temporal and frontal nodes of the attention network in macaques, we elucidated how attentional processes differed when directed towards social or non-social targets. Our findings revealed distinct neural signatures for social versus non-social stimuli, suggesting domain specificity in the allocation of attentional resources. Moreover, we demonstrated an intricate interplay between visual attention and social processing neural networks, highlighting the complexity of social cognition in primates. These insights advance our understanding of the neural basis of social attention in primates.