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

Abstract

In order to arrive at a quantitative understanding of the dynamics of cortical neuronal networks, we simulated a detailed model of the primary visual pathway of the adult cat. This computer model comprises a 5 degrees x 5 degrees patch of the visual field at a retinal eccentricity of 4.5 degrees and includes 2048 ON- and OFF-center retinal beta-ganglion cells, 8192 geniculate X-cells, and 4096 simple cells in layer IV in area 17. The neurons are implemented as improved integrate-and-fire units. Cortical receptive fields are determined by the pattern of afferent convergence and by inhibitory intracortical connections. Orientation columns are implemented continuously with a realistic receptive field scatter and jitter in the preferred orientations. We first show that realistic ON-OFF-responses, orientation selectivity, velocity low-pass behaviour, null response, and responses to spot stimuli can be obtained with an appropriate alignment of geniculate neurons converging onto the cortical simple cell (Hubel and Wiesel, 1962) and in the absence of intracortical connections. However, the average receptive field elongation (length to width) required to obtain realistic orientation tuning is 4.0, much higher than the average observed elongation. This strongly argues for additional intracortical mechanisms sharpening orientation selectivity. In the second stage, we simulated five different inhibitory intracortical connection patterns (random, local, sparse-local, circular, and cross-orientation) in order to investigate the connection specificity necessary to achieve orientation tuning. Inhibitory connection schemes were superimposed onto Hubel and Wiesel-type receptive fields with an elongation of 1.78. Cross-orientation inhibition gave rise to different horizontal and vertical orientation tuning curves, something not observed experimentally. A combination of two inhibitory schemes, local and circular inhibition (a weak form of cross-orientation inhibition), is in good agreement with observed receptive field properties. The specificity required to establish these connections during development is low. We propose that orientation selectivity is caused by at least three different mechanisms (“eclectic” model): a weak afferent geniculate bias, broadly tuned cross-orientation inhibition, and some iso-orientation inhibition. The most surprising finding is that an isotropic connection scheme, circular inhibition, in which a cell inhibits all of its postsynaptic target cells at a distance of approximately 500 microns, enhances orientation tuning and leads to a significant directional bias. This is caused by the embedding of cortical cells within a columnar structure and does not depend on our specific assumptions.

Intracortical Origins of Interocular Suppression in the Visual Cortex

“…A dense network of horizontal inhibitory connections (Kisvárday and Eysel, 1993;Kisvárday et al, 1994) appears ideally suited for this role. Indeed, pharmacological studies, in which either inhibitory inputs to the recorded neurons were blocked locally (Sillito, 1977(Sillito, , 1979 or neurons in nearby regions of cortex with differing orientation preferences were inactivated (Crook and Eysel, 1992;Crook et al, 1997Crook et al, , 1998, demonstrated a reduction in orientation selectivity, supporting the hypothesis that inhibitory interactions between neurons of different orientation preferences play an important role in the generation of cortical orientation selectivity (Sillito, 1979;Wörgötter and Koch, 1991;Somers et al, 1995;Carandini and Ringach, 1997). An alternative view interprets cross-orientation inhibition as a means of response normalization with respect to local image contrast (Heeger, 1992;Carandini and Heeger, 1994;.…”

“…It therefore seems reasonable to conclude that any cortical component of suppression by a superimposed mask should rather be iso-orientation, not cross-orientation, tuned. The functional role of those predominantly iso-oriented inputs may be the refinement of cortical orientation selectivity, as proposed by recurrent models (Wörgötter and Koch, 1991;Somers et al, 1995). By comparison, interocular suppression will have to involve projections across at least one ocular dominance column Responses to a blank screen are given by the symbols on the far right, marked blank.…”

The Role of Thalamic Inputs in Surround Receptive Fields of Barrel Neurons

“…A similar controversy surrounds the source of inputs that determine orientation selectivity in visual cortical neurons (for review, see Ferster and Koch, 1987), with some arguing for a purely thalamocortical mechanism (Hubel and Wiesel, 1962;Dalva et al, 1997), whereas others argue for a predominant intracortical mechanism (Wolf et al, 1986;Douglas et al, 1995). Others still have argued for an "eclectic" model in which weak thalamocortical inputs are modified by an intracortical mechanism (Worgotter and Koch, 1991).…”

Emergence of orientation selective simple cells simulated in deterministic and stochastic neural networks

“…This extreme narrowing might be due to lateral inhibition within layer IVc, where neighbouring cells suppress the activity of the considered cell when the stimulus orientation slightly deviates from the optimal orientation of his cell. This is corroborated by W6rg6tter and Koch (1991), who discussed the role of lateral inhibition for the response behaviour of mature neural networks. These authors showed, that different inhibitory mechanisms lead to a significant narrowing of orientation tuning curves obtained from their model neurons.…”