Direction Selectivity of Synaptic Potentials in Simple Cells of the Cat
Visual Cortex.
Bharathi Jagadeesh, Heidi Sue Wheat, Leonid L. Kontsevich, Christopher W.
Tyler and David Ferster.
Laboratory of Neuropsychology, NIMH/NIH, Building 49, 1b80, Bethesda, MD
20892. Department of Neurobiology and Physiology, 2153 N. Campus Drive,
Northwestern University, Evanston, IL 60208. Smith-Kettlewell Eye Research
Institute, 2232 Webster Street, San Francisco, CA 94115.
APStracts 4:172N, 1997.
ABSTRACT
The direction selectivity of simple cells in the visual cortex is generated at
least in part by nonlinear mechanisms. If a neuron were spatially linear, its
responses to moving stimuli could be predicted accurately from linear
combinations of its responses to stationary stimuli presented at different
positions within the receptive field. In extracellular recordings, this has
not been found to be the case. While the extracellular experiments demonstrate
the presence of a nonlinearity, the cellular process underlying the
nonlinearity, whether an early synaptic mechanism such as a shunting
inhibition or simply the spike threshold at the output, is not known. To
differentiate between these possibilities, we have recorded intracellularly
from simple cells of the intact cat with the whole-cell patch technique. A
linear model of direction selectivity was used to analyze the synaptic
potentials evoked by stationary sine wave gratings. The model predicted the
responses of cells to moving gratings with considerable accuracy. The degree
of direction selectivity and the time-course of the responses to moving
gratings were both well matched by the model. The direction selectivity of the
synaptic potentials was considerably smaller than that of the intracellularly
recorded action potential, indicating that a nonlinear mechanism such as
threshold enhances the direction selectivity of the cell's output over that of
its synaptic inputs. At the input stage, however, the cells apparently sum
their synaptic inputs in a highly linear fashion.
A more highly constrained test of linearity of synaptic summation based on
principal component analysis was applied to the responses of direction
selective cells to stationary gratings. The analysis confirms that the
summation in these cells is highly linear. The principal component analysis is
consistent with a model in which direction selectivity in cortical simple
cells is generated by only two subunits, each with a different receptive field
position and response time course. The response time course for each of the
two subunits is derived for four analyzed cells. Each derived subunit is
linear in spatial summation, suggesting that the neurons that comprise each
subunit are either geniculate X-cells or receive their primary synaptic input
from X-cells. The amplitude of the response of each subunit is linearly
related to the contrast of the stimulus. The subunits are nonlinear in the
time domain, however: the response to a stationary stimulus whose contrast is
modulated sinusoidally in time is non-sinusoidal. The principal component
analysis does not exclude models of direction selectivity based on more than
two subunits, but such higher-order models would have to include the
constraint that the extra subunits form a smooth continuum of interpolation
between the properties derived from the two subunit solution.
Received 11 January 1997; accepted in final form 24 July 1997.
APS Manuscript Number J0024-7.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 28 August 1997