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Journal of Neuroscience, Vol 14, 409-441, Copyright © 1994 by Society for Neuroscience
A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs
KD Miller
Division of Biology, California Institute of Technology, Pasadena 91125.
Neurons in the primary visual cortex of higher mammals respond selectively
to light/dark borders of a particular orientation. The receptive fields of
simple cells, a type of orientation-selective cell, consist of adjacent,
oriented regions alternately receiving ON-center and OFF-center excitatory
input. I show that this segregation of inputs within receptive fields can
occur through an activity-dependent competition between ON-center and
OFF-center inputs, just as segregation of inputs between different
postsynaptic cells into ocular dominance columns appears to occur through
activity-dependent competition between left-eye and right-eye inputs. These
different outcomes are proposed to result, not from different mechanisms,
but from different spatial structures of the correlations in neural
activity among the competing inputs in each case. Simple cells result if
ON-center inputs are best correlated with other ON-center inputs, and OFF
with OFF, at small retinotopic separations, but ON-center inputs are best
correlated with OFF-center inputs at larger separations. This hypothesis
leads robustly to development of simple cell receptive fields selective for
orientation and spatial frequency, and to the continuous and periodic
arrangement of preferred orientation across the cortex. Input correlations
determine the mean preferred spatial frequency and degree of orientation
selectivity. Estimates of these correlations based on measurements in adult
cat retina (Mastronarde, 1983a,b) produce quantitative predictions for the
mean preferred spatial frequencies of cat simple cells across
eccentricities that agree with experiments (Movshon et al., 1978b).
Intracortical interactions are the primary determinant of cortical
organization. Simple cell spatial phases can play a key role in this
organization, so arrangements of spatial phases and preferred orientations
may need to be studied together to understand either alone. Possible
origins for other cortical features including spatial frequency clusters,
afferent ON/OFF segregation, blobs, pinwheels, and opponent inhibition
within simple cell receptive fields are suggested. A number of strong
experimental tests of the hypothesis are proposed.
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