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GlyRα2, not GlyRα3, modulates the receptive field surround of OFF retinal ganglion cells

Published online by Cambridge University Press:  30 October 2015

CHI ZHANG ,
REGINA D. NOBLES  and
MAUREEN A. McCALL
CHI ZHANG
Affiliation:
Department of Anatomical Sciences & Neurobiology, University of Louisville, Louisville, Kentucky
REGINA D. NOBLES
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky
MAUREEN A. McCALL*
Affiliation:
Department of Anatomical Sciences & Neurobiology, University of Louisville, Louisville, Kentucky Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, Kentucky
*
*Address correspondence to: Maureen A. McCall, Department of Ophthalmology & Visual Sciences, University of Louisville, Louisville, KY 40202. E-mail: Mo.mccall@louisville.edu
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Abstract

Receptive fields (RFs) of most retinal ganglion cells (RGCs) consist of an excitatory center and suppressive surround. The RF center arises from the summation of excitatory bipolar cell glutamatergic inputs, whereas the surround arises from lateral inhibitory inputs. In the retina, both gamma amino butyric acid (GABA) and glycine are inhibitory neurotransmitters. A clear role for GABAergic inhibition modulating the RGC RF surround has been demonstrated across species. Glycinergic inhibition is more commonly associated with RF center modulation, although there is some evidence that it may contribute to the RF surround. The synaptic glycinergic chloride channels are formed by three homomeric β and two homomeric α subunits that can be glycine receptor (GlyR) α1, α2, α3, or α4. GlyRα composition is responsible for currents with distinct decay kinetics. Their expression within the inner plexiform laminae and neuronal subtypes also differ. We studied the role of GlyR subunit selective modulation of RGC RF surrounds, using mice lacking GlyRα2 (Glra2−/−), GlyRα3 (Glra3−/−), or both (Glra2/3−/−). We chose this molecular genetic approach instead of pharmacological manipulation because there are no subunit selective antagonists and strychnine blocks all GlyRs. Comparisons of annulus-evoked responses among wild type (WT) and GlyRα knockouts (Glra2−/−, Glra3−/− and Glra2/3−/−) show that GlyRα2 inhibition enhances RF surround suppression and post-stimulus excitation in only WT OFF RGCs. Similarities in the responses in Glra2−/− and Glra2/3−/− RGCs verify these conclusions. Based on previous and current data, we propose that GlyRα2-mediated input uses a crossover inhibitory circuit. Further, we suggest that GlyRα2 modulates the OFF RGC RF center and surround independently. In summary, our results define a selective GlyR subunit-specific control of RF surround suppression in OFF RGCs.

Keywords

Subunit selective inhibitionCrossover inhibitionVisionGlycineRetinal ON ganglion cellsOFF ganglion cellsReceptive fieldSurround suppression
Type
Research Article
Information
Visual Neuroscience , Volume 32 , 2015 , E026
Copyright
Copyright © Cambridge University Press 2015 

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