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Journal of Neuroscience, Vol 11, 1959-1979, Copyright © 1991 by Society for Neuroscience
A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity
F Worgotter and C Koch
Computation and Neural Systems Program, California Institute of Technology, Pasadena 91125.
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.(ABSTRACT TRUNCATED AT 400 WORDS)
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