Mismatch between human early visual cortex and perception in spatial extent representation: Radial bias shapes cortical representation while co-axial bias shapes perception

Abstract

AbstractAn object occupies an enclosed region in the visual field, which defines its spatial extent. Humans display exquisite finesse in spatial extent perception. Recent series of human neuroimaging and monkey single-cell studies suggest the spatial representation encoded in the early visual cortex (EVC) as the neural substrate of spatial extent estimation. Guided by this “EVC hypothesis” on spatial extent estimation, we predicted that human estimation of spatial extents would reflect the topographic biases known to exist in EVC’s spatial representation, the co-axial and radial biases. To test this prediction, we concurrently assessed those two spatial biases in both EVC’s and perceptual spatial representations by probing the anisotropy of EVC’s population receptive fields, on the one hand, and that of humans’ spatial extent estimation, on the other hand. To our surprise, we found a marked topographic mismatch between EVC’s and perceptual representations of oriented visual patterns, the radial bias in the former and the co-axial bias in the latter. Amid this topographic mismatch, the extent to which the anisotropy of spatial extents is modulated by stimulus orientation is correlated across individuals between EVC and perception. Our findings seem to require a revision of the current understanding of EVC’s functional architecture and contribution to visual perception: EVC’s spatial representation (i) is governed by the radial bias but only weakly modulated by the co-axial bias, and (ii) do contribute to spatial extent perception, but in a limited way where additional neural mechanisms are called in to counteract the radial bias in EVC.Significant statementPrevious anatomical and functional studies suggest both radial and co-axial biases as topographic factors governing the spatial representation of the early visual cortex (EVC). On the other hand, EVC’s fine-grained spatial representation has been considered the most plausible neural substrate for exquisite human perception of spatial extents. Based on these suggestions, we reasoned that these two topographic biases are likely to be shared between EVC’s and perceptual representations of spatial extents. However, our neuroimaging and psychophysics experiments implicate a need for revising those two suggestions. Firstly, the co-axial bias seems to exert only a modulatory influence on EVC’s functional architecture. Secondly, human spatial extent perception requires further contribution from neural mechanisms that correct EVC’s spatial representation for its radial bias.