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The Journal of Neuroscience, February 14, 2007, 27(7):1746-1755; doi:10.1523/JNEUROSCI.4383-06.2007

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Development/Plasticity/Repair
Developmental Homeostasis of Mouse Retinocollicular Synapses

Anand R. Chandrasekaran,1 * Ruchir D. Shah,1 * and Michael C. Crair1,2

1Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030, and 2Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510

Correspondence should be addressed to Michael C. Crair, Department of Neurobiology, Yale University School of Medicine, P.O. Box 208001, New Haven, CT 06520-8001. Email: michael.crair{at}yale.edu

Spontaneous retinal waves during development are thought to provide an instructive signal for precise retinotopic mapping by correlating the activity of neighboring retinal ganglion cells. In mutant mice (ß2–/–) that lack correlated waves, retinocollicular map refinement is impaired. In vivo recordings reveal that neurons in the superior colliculus of ß2–/– mice have large receptive fields and low peak visual responses, resulting in a conservation of total integrated response. We find that this "response homeostasis" is maintained on a cell-by-cell basis, and argue that it does not depend on regulation from the visual cortex during adulthood. Instead, in vitro recordings show that homeostasis arises from the conservation of total synaptic input from the retina, and that it is maintained via different mechanisms over development. In the absence of correlated retinal waves, ß2–/– neurons sample a larger number of weaker retinal inputs relative to controls after the first postnatal week. Once retinal waves are restored, developmental learning rules and homeostasis drive refinement so that fewer, stronger synapses are retained, as in wild-type mice, but from a larger retinal area. Homeostasis in neurons has been shown previously to regulate the gain of synaptic transmission in response to perturbations of activity. Our results suggest that during the development of sensory maps, a unique consequence of homeostatic mechanisms is the precise shaping of neuronal receptive fields in conjunction with activity-dependent competition.

Key words: retinal waves; superior colliculus; activity-dependent; homeostasis; development; mouse


Received Oct. 7, 2006; revised Jan. 4, 2007; accepted Jan. 8, 2007.

Correspondence should be addressed to Michael C. Crair, Department of Neurobiology, Yale University School of Medicine, P.O. Box 208001, New Haven, CT 06520-8001. Email: michael.crair{at}yale.edu




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