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The Journal of Neuroscience, June 18, 2008, 28(25):6526-6536; doi:10.1523/JNEUROSCI.1533-08.2008

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Neurobiology of Disease
Functional Stability of Retinal Ganglion Cells after Degeneration-Induced Changes in Synaptic Input

David J. Margolis,¹ Gregory Newkirk,¹ Thomas Euler,² and Peter B. Detwiler¹

¹Department of Physiology and Biophysics and Program in Neurobiology and Behavior, University of Washington, Seattle, Washington 98195, and ²Department of Biomedical Optics, Max Planck Institute for Medical Research, 69120 Heidelberg, Germany

Correspondence should be addressed to either of the following: Peter B. Detwiler, Department of Physiology and Biophysics, University of Washington, Box 357290, Seattle, WA 98195, Email: detwiler{at}u.washington.edu; or David J. Margolis at his present address, Department of Neurophysiology, Brain Research Institute, University of Zurich, CH-8057 Zurich, Switzerland, Email: margolis{at}hifo.uzh.ch

Glutamate released from photoreceptors controls the activity and output of parallel pathways in the retina. When photoreceptors die because of degenerative diseases, surviving retinal networks are left without their major source of input, but little is known about how photoreceptor loss affects ongoing synaptic activity and retinal output. Here, we use patch-clamp recording and two-photon microscopy to investigate morphological and physiological properties of identified types of ON and OFF retinal ganglion cells (RGCs) in the adult (36–210 d old) retinal degeneration rd-1/rd-1 mouse. We find that strong rhythmic synaptic input drives ongoing oscillatory spike activity in both ON and OFF RGCs at a fundamental "beating" frequency of 10 Hz. Despite this aberrant activity, ON and OFF cells maintain their characteristic dendritic stratification, intrinsic firing properties, including rebound firing in OFF cells, balance of synaptic excitation and inhibition, and dendritic calcium signaling. Thus, RGCs are inherently stable during degeneration-induced retinal activity.

Key words: retinal degeneration; photoreceptor; blindness; ganglion cells; dendrites; calcium

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Received Sept. 18, 2007; revised May 14, 2008; accepted May 14, 2008.

Correspondence should be addressed to either of the following: Peter B. Detwiler, Department of Physiology and Biophysics, University of Washington, Box 357290, Seattle, WA 98195, Email: detwiler{at}u.washington.edu; or David J. Margolis at his present address, Department of Neurophysiology, Brain Research Institute, University of Zurich, CH-8057 Zurich, Switzerland, Email: margolis{at}hifo.uzh.ch

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