Anisotropy in visual crowding is reflected in inter-laminar interactions of macaque V1

Spatial vision is the ability to perceive visual objects within 3-dimensional space, and its dysfunction is detrimental to our ability to interact with the visual world. Our visual experience is a result of the concerted activity of neuronal ensembles in the sensory hierarchy. How the organization of objects in space influences interactions in this hierarchy is poorly understood. We investigated this question in the inter-laminar interactions in the visual cortex, a canonical motif of hierarchical information processing. We analyzed laminar electrophysiological recordings in cortical area V1 while monkeys viewed stimuli in isolation or with flanking stimuli at various spatial configurations that are known to exert a “crowding” effect on perception. Visual crowding is thought to be the primary limitation on object perception in peripheral vision, and the psychophysically identified “crowding zone” of impaired object identification is highly anisotropic. Employing reduced rank regression techniques, we assessed the extent to which trial-to-trial variability in the superficial layer could be predicted by the input layer. We found that the overall prediction accuracy in the inter-laminar communication subspace was weaker in the presence of crowding stimuli. Furthermore, the prediction accuracy was worst when the flanking stimuli were in the visual subspace that causes the strongest perceptual crowding effects. When we quantified the temporal dynamics of the prediction accuracy, the overall degradation due to crowding had a latency of ~45ms after the onset of visual responses in superficial layers of V1. The degradation specific to the visual subspace with the strongest crowding effects had an additional latency of ~14-18ms. Our results suggest a model in which perceptual impairment under crowding is mediated by visual context integration in the superficial layer of V1. The delays suggest that contextual inputs are conveyed through feedback pathways, and that the anisotropy in contextual inputs is the neural substrate of perceptual experience.