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The Journal of Neuroscience, March 28, 2007, 27(13):3540-3547; doi:10.1523/JNEUROSCI.0372-07.2007

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Behavioral/Systems/Cognitive
Afferent Control of Horizontal Cell Morphology Revealed by Genetic Respecification of Rods and Cones

Mary A. Raven,¹ Edwin C. T. Oh,^3,4 Anand Swaroop,^3,4,5 and Benjamin E. Reese^1,2

¹Neuroscience Research Institute and ²Department of Psychology, University of California at Santa Barbara, Santa Barbara, California 93106, and ³Program in Neuroscience and ⁴Departments of Ophthalmology and Visual Sciences and ⁵Human Genetics, University of Michigan, Ann Arbor, Michigan 48105

Correspondence should be addressed to Benjamin E. Reese, Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060. Email: breese{at}psych.ucsb.edu

The first inhibitory interneurons of the retina, the horizontal cells, stratify within the outer plexiform layer, extending dendritic terminals that connect to the pedicles of cone photoreceptors and an axon terminal system contacting the spherules of rod photoreceptors. How the horizontal cells acquire this morphology is unknown, but instructive interactions with afferents are suggested to play a role in the development of synaptic circuits. Here, we show that the morphology of the axon terminal system and the dendritic field are selectively regulated by innervation from their respective afferents: genetic respecification of all cones to become rods, in Crxp-Nrl transgenic mice, produces an atrophic dendritic field yet leaves the axon terminal system largely intact. In contrast, in the retinas of Nrl^–/– mice, in which the population of rod photoreceptors is respecified to adopt a cone fate, the dendritic field is hypertrophic, whereas the axon terminal system is underdeveloped. Our studies reveal that, although cell-intrinsic mechanisms drive the formation of independent dendritic versus axonal domains, the afferents play a selectively instructive role in defining their respective morphologies.

Key words: differentiation; cone pedicle; rod spherule; outer plexiform layer; Nrl; axon terminal

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Received Jan. 26, 2007; revised Feb. 21, 2007; accepted March 2, 2007.

Correspondence should be addressed to Benjamin E. Reese, Neuroscience Research Institute, University of California, Santa Barbara, CA 93106-5060. Email: breese{at}psych.ucsb.edu

This article has been cited by other articles:

				P. W. Keeley and B. E. Reese Role of Afferents in the Differentiation of Bipolar Cells in the Mouse Retina J. Neurosci., February 3, 2010; 30(5): 1677 - 1685. [Abstract] [Full Text] [PDF]

				R. A. Poche and B. E. Reese Retinal horizontal cells: challenging paradigms of neural development and cancer biology Development, July 1, 2009; 136(13): 2141 - 2151. [Abstract] [Full Text] [PDF]

				R. A. Poche, K. M. Kwan, M. A. Raven, Y. Furuta, B. E. Reese, and R. R. Behringer Lim1 Is Essential for the Correct Laminar Positioning of Retinal Horizontal Cells J. Neurosci., December 19, 2007; 27(51): 14099 - 14107. [Abstract] [Full Text] [PDF]

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