Cerebral Cortex, Vol. 13, No. 1, 73-82,
January 2003
© 2003 Oxford University Press
Understanding Layer 4 of the Cortical Circuit: A Model Based on Cat V1
Departments of Physiology and Otolaryngology, W.M. Keck Center for Integrative Neuroscience, Sloan-Swartz Center for Theoretical Neurobiology at UCSF, University of California, San Francisco, CA 94143–0444, USA
Address correspondence to: Kenneth Miller, Department of Physiology, University of California at San Francisco, 513 Parnassus, San Francisco, CA 94143–0444, USA. Email: ken{at}phy.ucsf.edu.
This paper reviews theoretical and experimental results on the processing of layer 4, the input-recipient layer, of cat primary visual cortex (V1). A wide range of experimental data can be understood from a model in which response tuning of layer 4 cells is largely determined by a local interplay of feedforward excitation (from thalamus) and feedforward inhibition (from layer 4 inhibitory interneurons driven by thalamus). Feedforward inhibition dominates excitation, inherits its tuning from the thalamic input and sharpens the tuning of excitatory cells. At least a strong component of the feedforward inhibition received by a cell is spatially opponent to the excitation it receives, meaning that inhibition is driven by dark in regions of the visual field in which excitation is driven by light, and vice versa. The idea of opponent inhibition can be generalized to mean inhibition driven by input patterns that are strongly anti-correlated with the patterns that excite a cell. This paper argues that dominant feedforward opponent inhibition may be a general principle of cortical layer 4. This leads to the suggestion that the properties that show columnar organization – invariance across the vertical depth of cortex – may be properties that are shared by ‘opposite’ (anticorrelated) stimulus pairs. This contrasts with the more common idea that a column represents a set of cells that all share similar stimulus preferences.
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