Monocular core zones and binocular border strips in primate striate cortex revealed by the contrasting effects of enucleation, eyelid suture, and retinal laser lesions on cytochrome oxidase activity

Abstract

In primate striate cortex, geniculocortical afferents in layer IVc terminate in parallel stripes called ocular dominance columns. We propose that this segregation of ocular inputs generates a related but distinct columnar system of monocular core zones alternating with binocular border strips. Evidence for this functional parcellation was obtained by comparing the effects of enucleation, eyelid suture, and retinal laser lesions on cytochrome oxidase (CO) activity in eight macaques. Enucleation produced a high-contrast pattern of dark and light columns in layer IVc, corresponding precisely to the ocular dominance columns, whereas eyelid suture produced a low-contrast pattern of thin dark columns alternating with wide pale columns. [3H]Proline eye injection showed that the thin dark columns corresponded to the core zones of the open eye's ocular dominance columns. The wide pale columns resulted from loss of CO activity in the sutured eye's core zones and within both eyes' border strips. Loss of CO activity within both eyes' border strips suggested that these regions are binocular. To confirm our findings, we compared different CO patterns in the same cortex by making retinal laser lesions in four animals. They produced a CO pattern tantamount to 'focal' enucleation, although contrast was low when laser damage was confined to the outer retina. CO levels in cortical scotomas remained severely depressed for months after retinal lesions, even when the other eye was enucleated. This observation provided little anatomical support for the notion of topographic plasticity after visual deafferentation. In a single human subject with macular degeneration, CO revealed a low-contrast pattern of ocular dominance columns, resembling the pattern in monkeys with laser-induced photoreceptor damage.