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The Journal of Neuroscience, November 12, 2003, 23(32):10201-10213

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Behavioral/Systems/Cognitive
Different Roles for Simple-Cell and Complex-Cell Inhibition in V1

Thomas Z. Lauritzen^1,4 and Kenneth D. Miller^1,2,3,4

¹Graduate Group in Biophysics, ²Departments of Physiology and Otolaryngology, ³Sloan-Swartz Center for Theoretical Neurobiology, and ⁴W. M. Keck Center for Integrative Neuroscience, University of California, San Francisco, California 94143-0444

Previously, we proposed a model of the circuitry underlying simple-cell responses in cat primary visual cortex (V1) layer 4. We argued that the ordered arrangement of lateral geniculate nucleus inputs to a simple cell must be supplemented by a component of feedforward inhibition that is untuned for orientation and responds to high temporal frequencies to explain the sharp contrast-invariant orientation tuning and low-pass temporal frequency tuning of simple cells. The temporal tuning also requires a significant NMDA component in geniculocortical synapses. Recent experiments have revealed cat V1 layer 4 inhibitory neurons with two distinct types of receptive fields (RFs): complex RFs with mixed ON/OFF responses lacking in orientation tuning, and simple RFs with normal, sharp-orientation tuning (although, some respond to all orientations). We show that complex inhibitory neurons can provide the inhibition needed to explain simple-cell response properties. Given this complex cell inhibition, antiphase or "push-pull" inhibition from tuned simple inhibitory neurons acts to sharpen spatial frequency tuning, lower responses to low temporal frequency stimuli, and increase the stability of cortical activity.

Key words: visual cortex; contrast invariance; orientation tuning; simple cell; complex cell; V1; inhibition; push-pull; stability

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Received May 27, 2003; revised September 10, 2003; accepted September 12, 2003.

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