Retinal constraints on orientation specificity in cat visual cortex

Abstract

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)

Origins of feature selectivities and maps in the mammalian primary visual cortex

“…However, these models work on the assumption that LGN RFs are circular, which we now know is not the case. Many studies [3,19,[25][26][27][28][29]34,41,51] suggest that the LGN orientation biases may be important in generating the orientation selectivity of individual cortical neurons, but we propose further that these biases may also be a defining factor in the generation of the overall architecture of the striate cortex. In this respect, most computational models might have omitted an essential element needed to produce a comprehensive scheme that underlies both individual response properties and the overall functional architecture.…”

“…Alternative schemes have promoted other mechanisms in place of or in addition to excitatory convergence to explain orientation selectivity. These include intracortical cross-orientation inhibition [15][16][17][18][19][20] ( Figure 1B), intracortical iso-orientation facilitation [3,18,[21][22][23][24], mild orientation selectivity already present in LGN responses [3,[25][26][27][28][29] (Figure 1C), ON and OFF spatially offset excitatory inputs [30,31] (Figure 1D), or LGN cells with adjacent RFs that provide excitatory and inhibitory inputs [32] ( Figure 1E). Some have also implicated multiple mechanisms in the generation of orientation selectivity [3,18,33].…”

“…They assume that any orientation selectivity observed in the feedforward input from the thalamus is through a process of excitatory convergence from LGN cells with circular RFs. Such an assumption ignores a large body of evidence for the presence of mild but significant biases to stimulus orientation seen in the responses of cells in the LGN [25][26][27][35][36][37][38] and the retina [39,40] of every species studied so far. In addition, excitatory convergence along the long axis of the RF is also not essential in models that propose either excitation and inhibition on a simple cell arising from two geniculate inputs with spatially offset RFs [32] (Figure 1E) or pooling of inputs from adjacent ON and OFF center units [30,31] ( Figure 1D).…”

“…(B) Inhibition from cells in columns tuned to the orthogonal orientation generates, or at least sharpens, the orientation selectivity [15][16][17][18][19][20]. (C) The direct geniculo-striate projection -monosynaptic excitation from an LGN cell biased in its response to bars of different orientations, and a disynaptic inhibition not selective to orientation (or preferring the orthogonal orientation), lead to sharpening of the bias transmitted from the retina by the thalamic neurons [3,[25][26][27][28][29]. (D) Signals arising from adjacent retinal cells with spatially offset ON and OFF inputs form a dipole that not only leads to the orientation selectivity of the cortical simple cell, but also the retinal mosaic of such dipoles seeds the cortical orientation domains [30,31].…”

A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity

“…It has been reported (Vidyasagar and Urbas, 1982;Cleland et al, 1983;Schall et al, 1986;Vidyasagar, 1987;Shou and Leventhal, 1989) that geniculate cells are not circularly symmetric, but do show significant asymmetries for the orientation of bars and gratings. This orientation sensitivity is particularly pronounced at spatial frequencies above 1 cycle per degree.…”