Investigating the Large-Scale Topographic Organization of the Visual System in Humans and Macaques

Abstract

A fundamental question in vision neuroscience is how information from our environment is represented throughout the visual system. Much of visual cortex consists of several orderly representations of our environment along sensory surfaces. These topographic representations, referred to as visual field maps, are thought to facilitate the processing and communication of visual information. Using neuroimaging, we investigated the organization of visual field maps across visual cortex and the connectivity between cortical areas that support visuo-spatial processing. We identified 26 distinct visual field maps in humans and 15 in monkeys. These maps revealed several parallels, and a few dissociations, in the organization of the visual system between species. Many of these maps were within regions of cortex thought to lack organized representations of visual space. At a coarser scale, several visual maps formed distinct clusters with maps within a cluster sharing similar functional response properties. Functional and anatomical connectivity between human visual field maps emphasized local connections that, broadly, distinguished dorsal and ventral cortex and paralleled the well-established organization of the macaque visual system. Functional connectivity analyses also revealed a novel, large-scale organization based on eccentricity representations, in which areas with non-overlapping visual field representations, but matching eccentricity representations, were correlated. This eccentricity-based organization provides a new functional parcellation scheme of the visual cortex, which may be crucial for the integration of information across visual maps. Together, these data provide clear criteria for the comparison of human and macaque visual systems. They demonstrate that the representation of visual space is a major organizational principle of the primate visual system from individual maps to broad pathways consisting of several maps. This organization extends previous hypotheses on the efficient organization of individual topographic maps and suggests that the primate visual system is organized to efficiently communicate information at multiple spatial scales by broadly minimizing distances between areas involved in similar computational processes.