Distinct visual processing networks for foveal and peripheral visual fields

Abstract

Foveal and peripheral vision are two distinct modes of visual processing essential for navigating the world. However, it remains unclear if they engage different neural mechanisms and circuits within the visual attentional system. Here, we trained macaques to perform a free-gaze visual search task using natural face and object stimuli and recorded a large number of 14588 visually responsive neurons from a broadly distributed network of brain regions involved in visual attentional processing. Foveal and peripheral units had substantially different proportions across brain regions and exhibited systematic differences in encoding visual information and visual attention. The spike-LFP coherence of foveal units was more extensively modulated by both attention and visual selectivity, thus indicating differential engagement of the attention and visual coding network compared to peripheral units. Furthermore, we delineated the interaction and coordination between foveal and peripheral processing for spatial attention and saccade selection. Finally, the search became more efficient with increasing target-induced desynchronization, and foveal and peripheral units exhibited different correlations between neural responses and search behavior. Together, the systematic differences between foveal and peripheral processing provide valuable insights into how the brain processes and integrates visual information from different regions of the visual field. Significance StatementThis study investigates the systematic differences between foveal and peripheral vision, two crucial components of visual processing essential for navigating our surroundings. By simultaneously recording from a large number of neurons in the visual attentional neural network, we revealed substantial variations in the proportion and functional characteristics of foveal and peripheral units across different brain regions. We uncovered differential modulation of functional connectivity by attention and visual selectivity, elucidated the intricate interplay between foveal and peripheral processing in spatial attention and saccade selection, and linked neural responses to search behavior. Overall, our study contributes to a deeper understanding of how the brain processes and integrates visual information for active visual behaviors.