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A fast rod photoreceptor signaling pathway in the mammalian retina
Wei Li1, Shan Chen1 & Steven H DeVries2
Rod photoreceptors were recently shown to contact Off cone bipolar cells, providing an alternative pathway for rod signal flow in the mammalian retina. By recording from pairs of rods and Off cone bipolar cells in the ground squirrel (Spermophilus tridecemlineatus), we measured the synaptic responses of mammalian rods unfiltered by the slow kinetics of the rod bipolar cell response. We show that vesicle fusion and turnover in mammalian rods is fast, and that this new pathway can mediate rapid signaling.
2010 Nature America, Inc. All rights reserved.
Rods signal over a ~105-fold range of light intensities and use two pathways to communicate with postsynaptic neurons. At the
dimmest intensities, small graded signals flow to rod bipolar cells, where a metabotropic glutamate receptorlinked cascade provides low-pass temporal and threshold filtering1. At brighter intensities, larger signals flow to cone photoreceptors over a second pathway mediated by rodcone gap junctions2. Anatomical evidence for a third rod pathway was obtained initially in the ground squirrel3 and subsequently in other mammals4,5. In this pathway, rod terminals, called spherules, directly contact a subset of Off cone bipolar cells. The function of the third pathway is unclear. Only 5%20% of the rods contact Off cone bipolar cells, and contacts are on the external surface of the spherule, away from vesicle release sites within invaginations4,5. If the third pathway is functional, then the rapidly responding AMPA- and kainate-type glutamate receptors on Off cone bipolar cells can be used to measure the properties of rod transmitter release. Measurements at the synapse between a rod and an Off bipolar cell in the amphibian retina suggest that release is dominated by a component with slow kinetics that is matched to the slow time course of the rod photoresponse6,7.
We first identified the cone bipolar cell types that contacted rods. Cone bipolar cells were labeled by injecting a fluorescent tracer.
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a,b: GluR4 GluR5 Rhod cf: GluR4 GluR5 NB g,h: Alexa 568 Rhod NB