Retinal origin of orientation maps in visual cortex

Abstract

The orientation map is a hallmark of primary visual cortex in higher mammals. It is not yet known how orientation maps develop, what function they play in visual processing and why some species lack them. Here we advance the notion that quasi-periodic orientation maps are established by moiré interference of regularly spaced ON and OFF-center retinal ganglion cell mosaics. A key prediction of the theory is that the centers of iso-orientation domains must be arranged in a hexagonal lattice on the cortical surface. Here we show that such pattern is observed in individuals of four different species: monkey, cat, tree shrew and ferret. The proposed mechanism explains how orientation maps can develop without requiring precise patterns of spontaneous activity or molecular guidance. Further, it offers a possible account for the emergence of orientation tuning in single neurons despite the absence of orderly orientation maps in rodents species.

Link between orientation and retinotopic maps in primary visual cortex

“…Thus, we reasoned robust map properties predicted by the seeding mechanism might be detectable in the adult. Indeed, previous work has shown that the predicted hexagonal structure of the interference pattern is reflected in the organization of the orientation map (16,18). Here we use the model to derive a peculiar prediction relating orientation and retinotopic maps and confirm that it holds in tree shrew primary visual cortex.…”

“…We first consider an ideal version of the model, which helps develop an intuition for how the link between the maps come about. Suppose the receptive fields of ON-center and OFF-center retinal ganglion cells (RGCs) of a given class lie at the vertices of a perfect hexagonal grid (16). When two such patterns, having slightly different periodicities and orientations, are superimposed, the result is a periodic interference pattern (Fig.…”

“…1A). The period of the interference pattern depends on the ratio between periods of the component lattices and their relative orientation (16). An important property of the interference pattern is that the nearest neighbor of an ON-center cell is an OFF-center cell and vice versa.…”

“…An important property of the interference pattern is that the nearest neighbor of an ON-center cell is an OFF-center cell and vice versa. Thus, one may consider the interference pattern as composed of ON/OFF pairs or dipoles (15,16). Our hypothesis is that in the early stages of development cortical cells have inputs dominated by individual dipoles that generate orientation-tuned receptive fields with side-by-side subregions of opposite sign (8,16,19) (Fig.…”

“…Building on earlier work (14,15), we have recently proposed that orientation maps may be established initially by the interference pattern of ON-and OFF-center, quasi-periodic retinal mosaics (16). Normal visual experience and activity-dependent synaptic learning can subsequently help maintain and refine this initial organization.…”