Asymmetric connections, duplicate layers, and a vertically inverted map in the primary visual system.

Abstract

The achiasmatic mutation is a remarkable and rare visual system mutation carried in a line of black sheepdogs. In affected animals, the optic chiasm is missing, and each retina projects entirely to the ipsilateral hemisphere. As a result of this navigational error, maps of visual space in the lateral geniculate nucleus (LGN) have a unique structure with mirror reversals of field position across the A-A1 border. Animals also have a persistent and severe congenital nystagmus. In this report we analyze a novel variant of the achiasmatic mutation, one in which retinal axons from only one eye successfully cross midline and in which the great majority of fibers from both eyes terminate in a single lateral geniculate nucleus. The dominant optic tract contains four times as many axons as the other tract. The hyperinnervated LGN has a lamination pattern consisting of duplicate and partly interwoven layers. A multiunit mapping study of visual cortex (primarily area 17 along the marginal gyrus) shows that receptive field topography and orientation selectivity are normal. The size of central binocular visual space is nearly normal and is flanked by monocular domains in the periphery. However, there is an inexplicable vertical inversion in the orientation of the cortical representation: superior fields are located rostrally, and inferior fields are located caudally. Despite a host of drastic abnormalities at all level of the visual system, from retina to cortex, this animal was behaviorally indistinguishable from normal dogs and did not have any detectable oculomotor abnormalities.