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J Neurophysiol 85: 2130-2149, 2001;
0022-3077/01 $5.00
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The Journal of Neurophysiology Vol. 85 No. 5 May 2001, pp. 2130-2149
Copyright ©2001 by the American Physiological Society

Contrast-Dependent Nonlinearities Arise Locally in a Model of Contrast-Invariant Orientation Tuning

Andrew Kayser,1,3,4,* Nicholas J. Priebe,1,3,4,* and Kenneth D. Miller1,2,3,4,5

 1Department of Physiology,  2Department of Otolaryngology,  3Neuroscience Graduate Program,  4W. M. Keck Center for Integrative Neuroscience, and  5Sloan Center for Theoretical Neurobiology, University of California, San Francisco, California 94143-0444

Kayser, Andrew, Nicholas J. Priebe, and Kenneth D. Miller. Contrast-Dependent Nonlinearities Arise Locally in a Model of Contrast-Invariant Orientation Tuning. J. Neurophysiol. 85: 2130-2149, 2001. We study a recently proposed "correlation-based," push-pull model of the circuitry of layer 4 of cat visual cortex. This model was previously shown to explain the contrast-invariance of cortical orientation tuning. Here we show that it can simultaneously account for several contrast-dependent (c-d) "nonlinearities" in cortical responses. These include an advance with increasing contrast in the temporal phase of response to a sinusoidally modulated stimulus; a change in shape of the temporal frequency tuning curve, so that higher temporal frequencies may give little or no response at low contrast but reasonable responses at high contrast; and contrast saturation that occurs at lower contrasts in cortex than in the lateral geniculate nucleus (LGN). In the context of the model circuit, these properties arise from a mixture of nonlinear cellular and synaptic mechanisms: short-term synaptic depression, spike-rate adaptation, contrast-induced changes in cellular conductance, and the nonzero spike threshold. The former three mechanisms are sufficient to explain the experimentally observed increase in c-d phase advance in cortex relative to LGN. The c-d changes in temporal frequency tuning arise as a threshold effect: voltage modulations in response to higher-frequency inputs are only slightly above threshold at lower contrast, but become robustly suprathreshold at higher contrast. The other three nonlinear mechanisms also play a crucial role in this result, allowing contrast dependence of temporal frequency tuning to coexist with contrast-invariance of orientation tuning. Contrast saturation, and the observation that responses to stimuli of increasing temporal frequency saturate at increasingly high contrasts, can be induced both by the model's push-pull inhibition and by synaptic depression. Previous proposals explained these nonlinear response properties by assuming contrast-invariant orientation tuning as a starting point, and adding normalization by shunting inhibition derived equally from cells of all preferred orientations. The present proposal simultaneously explains both contrast-invariant orientation tuning and these contrast-dependent nonlinearities and requires only processing that is local in orientation, in agreement with intracellular measurements.

* A. Kayser and N. J. Priebe contributed equally to the modeling in this paper.




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