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The Journal of Neurophysiology Vol. 81 No. 3 March 1999, pp. 1212-1224
Copyright ©1999 by the American Physiological Society
Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261
Murthy, Aditya and
Allen L. Humphrey.
Inhibitory contributions to spatiotemporal receptive-field structure
and direction selectivity in simple cells of cat area 17. Intracortical inhibition contributes to direction selectivity in
primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T-oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static
nonlinear amplification, has been shown previously to account for
directional tuning in layer 4. We tested the hypotheses that inhibition
acts by altering S-T structure or the static nonlinearity or both.
Drifting and counterphasing sinewave gratings were used to measure
direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide
(BMI), a GABAA antagonist. S-T orientation was quantified
from fits to response temporal phase versus stimulus spatial phase
data. Bicuculline reduced direction selectivity and S-T orientation in
nearly all cells, and reductions in the two measures were well
correlated (r = 0.81) and reversible. Using conventional linear predictions based on response phase and amplitude, we found that BMI-induced changes in S-T structure also accounted well
for absolute changes in the amplitude and phase of responses to
gratings drifting in the preferred and nonpreferred direction. For each
cell we also calculated an exponent used to estimate the static
nonlinearity. Bicuculline reduced the exponent in most cells, but the
changes were not correlated with reductions in direction selectivity.
We conclude that GABAA-mediated inhibition influences
directional tuning in layer 4 primarily by sculpting S-T
receptive-field structure. The source of the inhibition is likely to be
other simple cells with certain spatiotemporal relationships to their
target. Despite reductions in the two measures, most receptive fields
maintained some directional tuning and S-T orientation during BMI. This
suggests that their excitatory inputs, arising from the lateral
geniculate nucleus and within area 17, are sufficient to create some
S-T orientation and that inhibition accentuates it. Finally, BMI also
reduced direction selectivity in 8 of 10 simple cells tested in layer
6, but the reductions were not accompanied by systematic changes in S-T
structure. This reflects the fact that S-T orientation, as revealed by
our first-order measures of the receptive field, is weak there
normally. Inhibition likely affects layer 6 cells via more complex,
nonlinear interactions.
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