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The Journal of Neuroscience, July 4, 2007, 27(27):7275-7283; doi:10.1523/JNEUROSCI.1143-07.2007

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Development/Plasticity/Repair
Inhibitory Plasticity Facilitates Recovery of Stimulus Velocity Tuning in the Superior Colliculus after Chronic NMDA Receptor Blockade

Khaleel A. Razak and Sarah L. Pallas

Department of Biology, Georgia State University, Atlanta, Georgia 30303

Correspondence should be addressed to Sarah L. Pallas, Department of Biology, Georgia State University, 24 Peachtree Center Avenue, Atlanta, GA 30303. Email: bioslp{at}langate.gsu.edu

The developing nervous system is shaped in important ways by spontaneous and stimulus-driven neural activity. Perturbation of normal activity patterns can profoundly affect the development of some neural response properties, whereas others are preserved through mechanisms that either compensate for or are unaffected by the perturbation. Most studies have examined the role of excitation in activity-dependent plasticity of response properties. Here, we examine the role of inhibition within the context of response selectivity for moving stimuli. The spatial extent of retinal input to the developing hamster superior colliculus (SC) can be experimentally increased by chronic NMDA receptor (NMDAR) blockade. Remarkably, stimulus velocity tuning is intact despite the increase in excitatory inputs. The goal of this study was to investigate whether plasticity in surround inhibition might provide the mechanism underlying this preservation of velocity tuning. Surround inhibition shapes velocity tuning in the majority of superficial layer SC neurons in normal hamsters. We show that despite the NMDAR blockade-induced increase in feedforward excitatory convergence from the retina, stimulus velocity tuning in the SC is maintained via compensatory plasticity in surround inhibition. The inhibitory surround increased in strength and spatial extent, and surround inhibition made a larger contribution to velocity tuning in the SC after chronic NMDAR blockade. These results show that inhibitory plasticity can preserve the balance between excitation and inhibition that is necessary to preserve response properties after developmental manipulations of neural activity. Understanding these compensatory mechanisms may permit their use to facilitate recovery from trauma or sensory deprivation.

Key words: traumatic brain injury; rodent; retinotectal; homeostatic plasticity; inhibitory plasticity; visual development

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Received Sept. 29, 2006; revised May 18, 2007; accepted May 22, 2007.

Correspondence should be addressed to Sarah L. Pallas, Department of Biology, Georgia State University, 24 Peachtree Center Avenue, Atlanta, GA 30303. Email: bioslp{at}langate.gsu.edu

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