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The Journal of Neuroscience, May 9, 2007, 27(19):5033-5042; doi:10.1523/JNEUROSCI.5386-06.2007

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Cellular/Molecular
Synaptic Ca²⁺ in Darkness Is Lower in Rods than Cones, Causing Slower Tonic Release of Vesicles

Zejuan Sheng,¹ Sue-Yeon Choi,¹ Ajay Dharia,¹ Jian Li,² Peter Sterling,² and Richard H. Kramer¹

¹Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, and ²Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Correspondence should be addressed to Dr. Richard H. Kramer, Department of Molecular and Cell Biology, 121 Life Sciences Addition, University of California, Berkeley, CA 94720-3200. Email: rhkramer{at}berkeley.edu

Rod and cone photoreceptors use specialized biochemistry to generate light responses that differ in their sensitivity and kinetics. However, it is unclear whether there are also synaptic differences that affect the transmission of visual information. Here, we report that in the dark, rods tonically release synaptic vesicles at a much slower rate than cones, as measured by the release of the fluorescent vesicle indicator FM1-43. To determine whether slower release results from a lower Ca²⁺ sensitivity or a lower dark concentration of Ca²⁺, we imaged fluorescent indicators of synaptic vesicle cycling and intraterminal Ca²⁺. We report that the Ca²⁺ sensitivity of release is indistinguishable in rods and cones, consistent with their possessing similar release machinery. However, the dark intraterminal Ca²⁺ concentration is lower in rods than in cones, as determined by two-photon Ca²⁺ imaging. The lower level of dark Ca²⁺ ensures that rods encode intensity with a slower vesicle release rate that is better matched to the lower information content of dim light.

Key words: retina; photoreceptor; neurotransmitter release; ribbon synapse; exocytosis; Ca²⁺ imaging

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Received Dec. 13, 2006; revised March 7, 2007; accepted April 1, 2007.

Correspondence should be addressed to Dr. Richard H. Kramer, Department of Molecular and Cell Biology, 121 Life Sciences Addition, University of California, Berkeley, CA 94720-3200. Email: rhkramer{at}berkeley.edu

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