Cortical Reorganization after Long-Term Adaptation to Retinal Lesions in Humans

Abstract

Single-unit recordings demonstrated that the adult mammalian visual cortex is capable of reorganizing after induced retinal lesions. In humans, whether the adult cortex is capable of reorganizing has only been studied using functional magnetic resonance imaging, with equivocal results. Here, we exploited the phenomenon of visual crowding, a major limitation on object recognition, to show that, in humans with long-standing retinal (macular) lesions that afflict the fovea and thus use their peripheral vision exclusively, the signature properties of crowding are distinctly different from those of the normal periphery. Crowding refers to the inability to recognize objects when the object spacing is smaller than the critical spacing. Critical spacing depends only on the retinal location of the object, scales linearly with its distance from the fovea, and is approximately two times larger in the radial than the tangential direction with respect to the fovea, thus demonstrating the signature radial-tangential anisotropy of the crowding zone. Using retinal imaging combined with behavioral measurements, we mapped out the crowding zone at the precise peripheral retinal locations adopted by individuals with macular lesions as the new visual reference loci. At these loci, the critical spacings are substantially smaller along the radial direction than expected based on the normal periphery, resulting in a lower scaling of critical spacing with the eccentricity of the peripheral locus and a loss in the signature radial-tangential anisotropy of the crowding zone. These results imply a fundamental difference in the substrate of cortical processing in object recognition following long-term adaptation to macular lesions.