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The Journal of Neuroscience, August 6, 2008, 28(32):8124-8137; doi:10.1523/JNEUROSCI.1317-08.2008

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Behavioral/Systems/Cognitive
Superior Colliculus Inactivation Causes Stable Offsets in Eye Position during Tracking

Ziad M. Hafed,¹ Laurent Goffart,² and Richard J. Krauzlis¹

¹Systems Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, California 92037, and ²Institut de Neurosciences Cognitives de la Méditerranée, Equipe Dynamique de la Perception Visuelle et de l'Action, Unité Mixte de Recherche 6193, Centre National de la Recherche Scientifique, Aix-Marseille Universités, 13402 Marseille, France

Correspondence should be addressed to Ziad M. Hafed, Systems Neurobiology Laboratory, Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: zhafed{at}salk.edu

The primate superior colliculus (SC) is often viewed as composed of two distinct motor zones with complementary functions: a peripheral region that helps generate saccades to eccentric targets and a central one that maintains fixation by suppressing saccades. Here, we directly tested the alternative interpretation that topography in the SC is not strictly motor, nor does it form two distinct zones, but instead forms a single map of behaviorally relevant goal locations. Primates tracked the invisible midpoint between two moving stimuli, such that the stimuli guiding tracking were peripheral whereas the inferred movement goal was foveal and parafoveal. Temporary inactivation of neurons in the central portion of the topographic map of the SC, representing the invisible goal, caused stable offsets in eye position during tracking that were directed away from the retinotopic position encoded by the inactivated SC site. Critically, these offsets were not accompanied by a systematic inability to generate or suppress saccades, and they were not fully explained by motor deficits in saccades, smooth pursuit, or fixation. In addition, the magnitude of the offset depended on the eccentricity of the inactivated site as well as the degree of spatial uncertainty associated with the behavioral goal. These results indicate that gaze control depends on the balance of activity across a map of goal locations in the SC, and that by silencing some of the neurons in the normally active population representing the behavioral goal, focal inactivation causes a biased estimate of where to look.

Key words: superior colliculus; pursuit; voluntary eye movement; stimulus–response; reversible inactivation; muscimol

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Received March 27, 2008; revised July 3, 2008; accepted July 7, 2008.

Correspondence should be addressed to Ziad M. Hafed, Systems Neurobiology Laboratory, Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: zhafed{at}salk.edu

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Tracking an Invisible Target Reveals Spatial Tuning of Neurons in the Rostral Superior Colliculus Is Not Dependent on Visual Stimuli

Marion R. Van Horn
J. Neurosci. 2009 29: 589-590. [Full Text]  

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