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The Journal of Neurophysiology Vol. 84 No. 2 August 2000, pp. 909-926
Copyright ©2000 by the American Physiological Society
1Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois 60208; 2Howard Hughes Medical Institute and Center for Neural Science, New York University, New York, New York 10003; and 3Institute of Neuroinformatics, Swiss Federal Institute of Technology and University of Zurich, CH-8057 Zurich, Switzerland
Anderson, Jeffrey S.,
Matteo Carandini, and
David Ferster.
Orientation Tuning of Input Conductance, Excitation, and
Inhibition in Cat Primary Visual Cortex. J. Neurophysiol. 84: 909-926, 2000. The input conductance of cells in
the cat primary visual cortex (V1) has been shown recently to grow
substantially during visual stimulation. Because increasing conductance
can have a divisive effect on the synaptic input, theoretical proposals
have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by
increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with
stimulus contrast. We set out to test these proposals and to determine
the visual properties and possible synaptic origin of the conductance
increases. We recorded the membrane potential of cat V1 cells while
injecting steady currents and presenting drifting grating patterns of
varying contrast and orientation. Input conductance grew with stimulus
contrast by 20-300%, generally more in simple cells (40-300%) than
in complex cells (20-120%), and in simple cells was strongly
modulated in time. Conductance was invariably maximal for stimuli of
the preferred orientation. Thus conductance changes contribute to a
gain control mechanism, but the strength of this gain control does not
depend uniquely on contrast. By assuming that the conductance changes
are entirely synaptic, we further derived the excitatory and inhibitory
synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and
inhibition had similar preferred orientations and did not appear to
differ in tuning width, suggesting that the intracortical synaptic
inputs to simple cells of cat V1 originate from cells with similar
orientation tuning. This finding is at odds with models where
orientation tuning in simple cells is achieved by inhibition at
off-optimal orientations or sharpened by inhibition that is more
broadly tuned than excitation.
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