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The Journal of Neuroscience, May 27, 2009, 29(21):6917-6925; doi:10.1523/JNEUROSCI.3125-08.2009

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Behavioral/Systems/Cognitive
Cortical Lesion-Induced Visual Hemineglect Is Prevented by NMDA Antagonist Pretreatment

Huai Jiang, Barry E. Stein, and John G. McHaffie

Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, North Carolina 27157-1010

Correspondence should be addressed to John G. McHaffie, Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC 27157. Email: mchaffie{at}wfubmc.edu

Large unilateral visual cortex lesions produce enduring contralesional visual orientation deficits. To examine whether glutamate excitotoxicity is involved in establishing these deficits, cats were pretreated with the NMDA receptor antagonist dizocilpine (MK-801) 30 min before unilateral visual cortex ablation. Pretreated MK-801 animals were trained first in an orientation task in which they were required to fixate directly ahead and then orient to stimuli introduced at various eccentricities throughout the visual field. They did not display the characteristic ipsilesional head and neck asymmetries and/or spontaneous ipsiversive rotational behaviors or show the profound contralesional visual neglect seen postoperatively in nonpretreated control animals. Rather, pretreated animals were able to orient to visual stimuli in the contralesional hemifield immediately following surgical recovery. Postmortem histology revealed severe retrograde degeneration of the ipsilesional lateral geniculate nucleus in both experimental groups, suggesting that postlesion visuomotor behavioral competencies in pretreated animals are attributable to preserved function in nongeniculocortical visual pathways. These observations are consistent with the hypothesis that visual cortex lesions normally induce secondary alterations via NMDA-mediated excitotoxicity in these other pathways that prevents them from supporting visuomotor behaviors. The similar behavioral competencies of MK-801-pretreated animals and those whose lesion-induced deficits are ameliorated by removing basal ganglia afferents to the ipsilesional superior colliculus are consistent with this hypothesis and highlight the normal functional capabilities of this circuit. It is likely that MK-801 pretreatment acts, at least in part, by preserving the normal interhemispheric control dynamics with which the basal ganglia influence superior colliculus-mediated orientation behaviors.

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Received July 5, 2008; revised March 10, 2009; accepted April 20, 2009.

Correspondence should be addressed to John G. McHaffie, Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, NC 27157. Email: mchaffie{at}wfubmc.edu

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