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Variable Gain Control in Local Cortical Circuitry Supports Context-Dependent Modulation by Long-Range Connections

David C. Somers, Louis J. Toth, Emanuel Todorov, S. Chenchal Rao, Dae-Shik Kim, Sacha B. Nelson, Athanassios G. Siapas, and Mriganka Sur.
Department of Brain & Cognitive Sciences
Massachusetts Institute of Technology
Cambridge, MA 02139
{somers,emo,thanos}@ai.mit.edu, {ljtoth,chenchal,dskim}@mit.edu, nelson@binah.cc.brandeis.edu, msur@wccf.mit.edu

Abstract

Long-range horizontal connections within the primary visual cortex link cells with similar orientation preference over large regions of visual space. These connections are thought to underlie orientation-specific response modulations from beyond a neuron's classical receptive field. The nature of such modulations appears paradoxical as similar surround stimuli can both strongly facilitate and suppress responses in a cell population. We describe a biologically detailed model of primary visual cortex that reconciles these data by proposing that fixed-strength, long-range inputs can have both facilitatory and suppressive effects on the same group of neurons. The sign of the effect varies with the gain control state of the central cortical circuitry. The gain state varies with the level of local activation, with high gain for weak central drive, and low gain for strong central drive. Computer simulations demonstrate that long-range inputs, via interactions with the local circuitry, facilitate responses when central stimulation is weak and suppress responses when central stimulation is strong. We present experimental evidence to support the idea of bi-phasic response modulation. By imaging intrinsic signals in primary visual cortex of cats, we demonstrate the presence of long-range influences that change dynamically from facilitatory to suppressive when the level of local drive changes from low to high. Such context-dependent control of cortical response gain appears well suited to underlie a range of physiological and psychophysical phenomena in the visual system.




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