The retinal ganglion cell mosaic defines orientation columns in striate cortex.

Abstract

A computer simulation was used to demonstrate that the tangential organization of orientation columns is a natural consequence of the orderly projection of the mosaic of retinal ganglion cells onto the visual cortex. Parameters of the simulation were taken from published anatomical and electrophysiological data, and the resulting columnar organization of the simulated visual cortex shows many similarities with observations from animals. The model is able to account for a variety of experimental observations, including the presence of orientation columns in visually inexperienced animals.One of the striking features of the cortical representation of the visual field is the grouping of neurons with similar preferred orientations into the orientation columns described by Hubel and Wiesel (1,2). This columnar organization is already present in kittens at the time ofeye opening and must, therefore, be determined by intrinsic developmental processes that are independent of visual experience (3-6). In a previous report, I showed how the orientation tuning of visual cortex neurons could be calculated from the pattern of convergence of on-and off-center afferents (7). Using this calculation procedure, I show here that the tangential organization of the orientation columns is a natural consequence of the orderly projection of the retinal ganglion cell mosaic onto the cortex.Wissle and his collaborators (8, 9) have shown that retinal ganglion cells (RGCs) of the cat are arranged in a lattice-like mosaic with regular cell-to-cell spacings. Similar arrangements were found for both the P (8) and a (9) morphological types, which Boycott and Wassle (10) and Wassle et al. (11) have shown to correspond to the X and Y physiological types (12-15), respectively. For both the X and Y cells, on-and off-center RGCs form their own lattices, and the on and off lattices are superimposed independently of each other (8,9). Since the signals from RGCs are relayed through the lateral geniculate nucleus (LGN) without substantial modification (16)(17)(18)(19), the RGC mosaic represents the pattern of visual input to the cortex. Thus, as emphasized by Wassle et al. (8), the RGC mosaic serves as an important constraint on the construction of cortical receptive fields. THE SIMULATIONWhat I present here is the result, by computer simulation, of the developmental process whereby the RGC mosaic projects retinotopically by way of the LGN onto the cortex. The simulation begins with two sets of coordinates, corresponding to the retinal positions of the on-and off-center RGCs.The receptive fields of the cortical neurons are then defined as a convergence of RGC inputs, and their responses are calculated using the procedure described in a previous report (7). The positions of the RGCs in the retinal mosaic were measured from figure 9 of Wassle et al. (8) after photographic enlargement and were corrected for tissue shrinkage by the areal shrinkage factor of 0.5 provided by the authors. Other parameters of the simulation were also obtained from exper...

Link between orientation and retinotopic maps in primary visual cortex

“…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.…”

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

“…A small number of simple quantitative models have appeared over the years (e.g., Nielsen, 1983;Ferster, 1987;Soodak, 1987). The majority of these models have been restricted to single-cell receptive fields, and none have investigated the temporal dynamics of a population of interacting cortical neurons.…”

Cortical column design: a link between the maps of preferred orientation and orientation tuning strength?

“…Related to this approach is work which shows that self-organizing feature maps (Kohonen 1990) generate column structures which share many properties with orientation (or ocular dominance) columns in visual cortex (Obermayer et al 1990(Obermayer et al , 1991. Similar maps are obtained if one assumes that the connections between neurons satisfy some geometric constraints (Soodak 1987). Basically, the maps minimize the total length of connections between like neurons, with the exception of a few long-range connections (Durbin and Mitchison 1990).…”

“…We will, however, adopt the point of view that the measured tuning strength map does, in fact, reflect the distribution of orientation selectivity in cortex, and we will investigate the consequences of this assumption. We will show that the link between orientation preference and tuning strength permits description of the properties of both maps (preferred orientation and orientation strength) with a minimal set of parameters which probably also underlie most of the previously proposed models of cortical map formation and structure (von der Malsburg 1973;Nass and Cooper 1975;Perez et al 1975;Cooper et al 1979;von der Malsburg and Cowan 1982;Swindale 1982;Linsker 1986a, b;Soodak 1987;Durbin and Mitchison 1990;Miller 1990;Obermayer et al 1990Obermayer et al , 1991.…”