Geometry of anisotropic contextual interactions in the visual cortex places fundamental limits on spatial vision.

Abstract

Crowding, the impaired ability to accurately recognize a target stimulus among distractors, is a major bottleneck in visual perception. The spatial configuration of distractors in relation to the target profoundly influences perceptual fidelity. Notably, when a distractor is placed at a more eccentric point on the radial axis (termed ‘radial-out crowding’), it exerts the strongest impairment. Despite the pronounced perceptual anisotropy, the prevalent assumption underlying our understanding of contextual interactions in the visual cortex assumes isotropy. We investigated how distractor stimuli in different spatial configurations impacted the representation of a target stimulus in laminar microcircuits in the primary visual cortex (V1). Our study reveals that radial-out crowding more strongly impacts the ability to decode the target orientation from V1 population activity compared to other spatial configurations. This effect was strongest among putative excitatory neurons in the superficial and input layers, which are the primary neural populations involved in feed-forward information propagation. Remarkably, the feedback pathway involving the deep cortical layers does not exhibit anisotropy. Mechanistically, the anisotropy is explained by a tuned suppression and untuned facilitation of orientation responses, leading to an anisotropic broadening of tuning curves in the feedforward pathway, but not in the feedback pathway. These results underscore the non-uniform spatial integration of information by neurons in the visual cortex, establishing the presence of anisotropic contextual interactions in the earliest stages of cortical processing. By elucidating the distinct roles of feed-forward and feedback pathways in the context of crowding, this study advances our understanding of the intricate interplay between spatial arrangement, neural circuitry, and the constraints on perceptual fidelity during early visual processing.