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The Journal of Neuroscience, December 14, 2005, 25(50):11666-11675; doi:10.1523/JNEUROSCI.3414-05.2005

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Behavioral/Systems/Cognitive
Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque

Ben S. Webb,² Neel T. Dhruv,¹ Samuel G. Solomon,³ Chris Tailby,¹ and Peter Lennie¹

¹Center for Neural Science, New York University, New York, New York 10003, ²School of Psychology, University of Nottingham, Nottingham NG7 2RD, United Kingdom, and ³Institute of Biomedical Research, The University of Sydney, New South Wales 2006, Australia

The response of a neuron in striate cortex to an optimally configured visual stimulus is generally reduced when the stimulus is enlarged to encroach on a suppressive region that surrounds its classical receptive field (CRF). To characterize the mechanism that gives rise to this suppression, we measured its spatiotemporal tuning, its susceptibility to contrast adaptation, and its capacity for interocular transfer. Responses to an optimally configured grating confined to the CRF were strongly suppressed by annular surrounding gratings drifting at a wide range of temporal and spatial frequencies (including spatially uniform fields) that extended from well below to well above the range that drives most cortical neurons. Suppression from gratings capable of driving cortical CRFs was profoundly reduced by contrast adaptation and showed substantial interocular transfer. Suppression from stimuli that lay outside the spatiotemporal passband of most cortical CRFs was relatively stronger when the stimulus on the CRF was of low contrast, was generally insusceptible to contrast adaptation, and showed little interocular transfer. Our findings point to the existence of two mechanisms of surround suppression: one that is prominent when high-contrast stimuli drive the CRF, is orientation selective, has relatively sharp spatiotemporal tuning, is binocularly driven, and can be substantially desensitized by adaptation; the other is relatively more prominent when low-contrast stimuli drive the CRF, has very broad spatiotemporal tuning, is monocularly driven, and is insusceptible to adaptation. Its character suggests an origin in the input layers of primary visual cortex, or earlier.

Key words: macaque monkey; striate cortex; receptive field; surround suppression; context; cortical feedback

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Received Aug 12, 2005; revised October 26, 2005; accepted November 1, 2005.

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