The Journal of Neuroscience, December 15, 2002, 22(24):10871-10882
Confocal Analysis of Reciprocal Feedback at Rod Bipolar Terminals
in the Rabbit Retina
Jian
Zhang,
Wei
Li,
E. Brady
Trexler, and
Stephen C.
Massey
Department of Ophthalmology and Visual Science, University
of Texas-Houston Medical School, Houston, Texas 77030
Amacrine cells in the mammalian retina are famously diverse in
shape and function. Here, we show that two wide-field GABA amacrine
cells, S1 and S2, have stereotyped synaptic contacts with the
appropriate morphology and distribution to perform specific functions.
S1 and S2 both supply negative feedback to rod bipolar terminals and
thus provide a substrate for lateral inhibition in the rod pathway.
Synapses are specialized structures, and the presynaptic compartment is
normally characterized by a swelling or varicosity. Each S1 amacrine
cell has ~280 varicosities, whereas an S2 cell has even more, ~500
per cell. Confocal analysis shows that essentially all varicosities
aggregate around rod bipolar terminals where they are apposed by
postsynaptic GABA receptors. Each rod bipolar terminal is contacted by
varicosities from ~25 different S1 and 50 different S2 amacrine
cells. In fact, rod bipolar cells are the only synaptic target for S1
and S2 amacrine cells: all of the output from these two wide-field GABA
amacrine cells goes to rod bipolar terminals. It has long been a puzzle why two amacrine cells, apparently with the same connections, are
required. However, an analysis of the distribution of varicosities suggests that S1 and S2 amacrine cells provide different signals. S2
amacrine cells dominate within 200 µ from a rod bipolar terminal and
can provide an inhibitory input with spatial characteristics that match
the size of the surround signal recorded from AII amacrine cells in the
rod pathway. In contrast, the larger, better-coupled S1 amacrine cells
may provide a more distant network signal.
Key words:
retina; S1 amacrine cell; S2 amacrine cell; rod bipolar
cell; AII amacrine cell; confocal microscopy; Neurobiotin
Copyright © 2002 Society for Neuroscience 0270-6474/02/222410871-12$05.00/0