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Development of excitatory and inhibitory neurotransmitters in transitory cholinergic neurons, starburst amacrine cells, and GABAergic amacrine cells of rabbit retina, with implications for previsual and visual development of retinal ganglion cells

Published online by Cambridge University Press:  15 April 2010

EDWARD V. FAMIGLIETTI  and
SARAH J. SUNDQUIST
EDWARD V. FAMIGLIETTI*
Affiliation:
Department of Surgery (Ophthalmology), Brown University, Providence, Rhode Island Division of Ophthalmology, Rhode Island Hospital, Providence, Rhode Island
SARAH J. SUNDQUIST
Affiliation:
Neuroscience Discovery Research, Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana 46285-0438.
*
*Address correspondence and reprint requests to: Edward V. Famiglietti, P. O. Box 252, Narragansett, RI 02882. E-mail: edward_famiglietti@brown.edu
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Abstract

Starburst amacrine cells (SACs), the only acetylcholine (ACh)-releasing amacrine cells (ACs) in adult rabbit retina, contain GABA and are key elements in the retina’s directionally selective (DS) mechanism. Unlike many other GABAergic ACs, they use glutamic acid decarboxlyase (GAD)67, not GAD65, to synthesize GABA. Using immunocytochemistry, we demonstrate the apoptosis at birth (P0) of transitory putative ACs that exhibit immunoreactivity (IR) for the ACh-synthetic enzyme choline acetyltransferase (ChAT), GAD67, and the GABA transporter, GAT1. Only a few intact, displaced ChAT-immunoreactive SAC bodies are detected at P0. At P2, ChAT-IR is detected in the two narrowly stratified substrata of starburst dendrites in the inner plexiform layer (IPL). Quantitative analysis reveals that in the first postnatal week, only a small fraction of SACs cells express ChAT- and GABA-IR. Not until the end of the second week are they expressed in all SACs. At P0, a three-tiered stratification of GABA-IR is present in the IPL, entirely different from the adult pattern of seven substrata, emerging at P3–P4, and optimally visualized at P13. At P0, GAD65 is detectable in normally placed AC bodies. At P1, GAD65-IR appears in dendrites of nonstarburst GABAergic ACs, and by P5 is robust in the adult pattern of four substrata in the IPL. GAD65-IR never co-localizes with ChAT-IR. In a temporal comparison of our data with physiological, pharmacological, and ultrastructural studies, we suggest that transitory ChAT-immunoreactive cells share with SACs production of stage II (nicotinic) waves of previsual synchronous activity in ganglion cells (GCs). Further, we conclude that (1) GAD65-immunoreactive, non-SAC GABAergic ACs are the most likely candidates responsible for the suppression of stage III (muscarinic/AMPA-kainate) waves and (2) DS responses first appear in DS GCs, when about 50% of SACs express ChAT- and GABA-IR, and in 100% of DS GCs, when expression occurs in all SACs.

Keywords

AChCholine acetyltransferaseGABAGlutamic acid decarboxylaseGAT1ChATGAD65GAD67Retinal waves
Type
Research Articles
Information
Visual Neuroscience , Volume 27 , Issue 1-2 , March 2010 , pp. 19 - 42
Copyright
Copyright © Cambridge University Press 2010

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