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The Journal of Neuroscience, April 19, 2006, 26(16):4206-4215; doi:10.1523/JNEUROSCI.0496-06.2006

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Behavioral/Systems/Cognitive
Light-Induced Changes in Spike Synchronization between Coupled ON Direction Selective Ganglion Cells in the Mammalian Retina

Jessica M. Ackert,¹ Synphen H. Wu,² Jacob C. Lee,¹ Joseph Abrams,¹ Edward H. Hu,^1,2 Ido Perlman,³ and Stewart A. Bloomfield^1,2

¹Departments of Ophthalmology and ²Physiology and Neuroscience, New York University School of Medicine, New York, New York 10016, and ³Department of Physiology and Biophysics, Technion-Israel Institute of Technology, Technion City, Haifa 3200, Israel

Correspondence should be addressed to Dr. Stewart A. Bloomfield, Department of Ophthalmology, New York University School of Medicine, 550 First Avenue, New York, NY 10016. Email: blooms01{at}med.nyu.edu

Although electrical coupling via gap junctions is prevalent among ganglion cells in the vertebrate retina, there have been few direct studies of their influence on the light-evoked signaling of these cells. Here, we describe the pattern and function of coupling between the ON direction selective (DS) ganglion cells, a unique subtype whose signals are transmitted to the accessory optic system (AOS) where they initiate the optokinetic response. ON DS cells are coupled indirectly via gap junctions made with a subtype of polyaxonal amacrine cell. This coupling underlies synchronization of the spontaneous and light-evoked spike activity of neighboring ON DS cells. However, we find that ON DS cell pairs show robust synchrony for all directions of stimulus movement, except for the null direction. Null stimulus movement evokes a GABAergic inhibition that temporally shifts firing of ON DS cell neighbors, resulting in a desynchronization of spike activity. Thus, detection of null stimulus movement appears key to the direction selectivity of ON DS cells, evoking both an attenuation of spike frequency and a desynchronization of neighbors. We posit that active desynchronization reduces summation of synaptic potentials at target AOS cells and thus provides a secondary mechanism by which ON DS cell ensembles can signal direction of stimulus motion to the brain.

Key words: retina; synchrony; gap junctions; coupling; ganglion cells; inhibition

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Received Nov. 1, 2005; revised March 6, 2006; accepted March 14, 2006.

Correspondence should be addressed to Dr. Stewart A. Bloomfield, Department of Ophthalmology, New York University School of Medicine, 550 First Avenue, New York, NY 10016. Email: blooms01{at}med.nyu.edu

This article has been cited by other articles:

				J. Shlens, G. D. Field, J. L. Gauthier, M. Greschner, A. Sher, A. M. Litke, and E. J. Chichilnisky The Structure of Large-Scale Synchronized Firing in Primate Retina J. Neurosci., April 15, 2009; 29(15): 5022 - 5031. [Abstract] [Full Text] [PDF]

				W. Sun, Q. Deng, W. R. Levick, and S. He ON direction-selective ganglion cells in the mouse retina J. Physiol., October 1, 2006; 576(1): 197 - 202. [Abstract] [Full Text] [PDF]

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