Retinal constraints on orientation specificity in cat visual cortex.

Most retinal ganglion cells (Levick and Thibos, 1982) and cortical cells (Leventhal, 1983; Leventhal et al., 1984) subserving peripheral vision respond best to stimuli that are oriented radially, i.e., like the spokes of a wheel with the area centralis at the hub. We have extended this work by comparing directly the distributions of orientations represented in topographically corresponding regions of retina and visual cortex. Both central and peripheral regions were studied. The relations between the orientations of neighboring ganglion cells and the manner in which the overrepresentation of radial orientations is accommodated in the functional architecture of visual cortex were also studied. Our results are based on an analysis of the orientations of the dendritic fields of 1296 ganglion cells throughout the retina and the preferred orientations of 1389 cells located in retinotopically corresponding regions of cortical areas 17, 18, and 19 in the cat. We find that horizontal and vertical orientations are overrepresented in regions of both retina and visual cortex subserving the central 5 degrees of vision. The distributions of the orientations of retinal ganglion cells and cortical cells subserving the horizontal, vertical, and diagonal meridians outside the area centralis differ significantly. The distribution of the preferred orientations of the S (simple) cells in areas 17, 18 and 19 subserving a given part of the retina corresponds to the distribution of the dendritic field orientations of the ganglion cells in that part of retina. The distribution of the preferred orientations of C (complex) cells with narrow receptive fields in area 17 but not C cells with wide receptive fields in areas 17, 18, or 19 subserving a given part of the retina matches the distribution of the orientations of the ganglion cells in that part of retina. The orientations of all of the alpha-cells in 5-9 mm2 patches of retina along the horizontal, vertical, and oblique meridians were determined. A comparison of the orientations of neighboring cells indicates that other than a mutual tendency to be oriented radially, ganglion cells with similar orientations are not clustered in the retina. Reconstructions of electrode penetrations into regions of visual cortex representing peripheral retina indicate that columns subserving radial orientations are wider than those subserving nonradial orientations. Our results provide evidence that the distribution of the preferred orientations of simple cells in visual cortex subserving any region of the visual field matches the distribution of the orientations of the ganglion cells subserving the same region of the visual field.(ABSTRACT TRUNCATED AT 400 WORDS)