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J Neurophysiol 99: 25-36, 2008. First published November 7, 2007; doi:10.1152/jn.00737.2007
0022-3077/08 $8.00
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Mechanisms Contributing to Tonic Release at the Cone Photoreceptor Ribbon Synapse

Barbara Innocenti1,2 and Ruth Heidelberger1,2,3

1The W. M. Keck Center for the Neurobiology of Learning and Memory, 2Department of Neurobiology and Anatomy, and 3Graduate School of Biomedical Sciences, University of Texas Medical School at Houston, Houston, Texas

Submitted 2 July 2007; accepted in final form 25 October 2007

Time-resolved capacitance measurements in combination with fluorescence measurements of internal calcium suggested three kinetic components of release in acutely isolated cone photoreceptors of the tiger salamander. A 45-fF releasable pool, corresponding to about 1,000 vesicles, was identified. This pool could be depleted with a time constant of a few hundred milliseconds and its recovery from depletion was quite rapid ({tau} {approx} 1 s). The fusion of vesicles in this pool was blocked by low-millimolar EGTA. Endocytosis was sufficiently slow that it is likely that refilling of the releasable pool occurred from preformed vesicles. A second, slower component of release ({tau}depletion {approx} 3 s) was identified that was approximately twice the size of the releasable pool. This pool may serve as a first reserve pool that replenishes the releasable pool. Computer simulations indicate that the properties of the releasable and first reserve pools are sufficient to maintain synaptic signaling for several seconds in the face of near-maximal stimulations and in the absence of other sources of vesicles. Along with lower rates of depletion, additional mechanisms, such as replenishment from distal reserve pools and the fast recycling of vesicles, may further contribute to the maintenance of graded, tonic release from cone photoreceptors.

Address for reprint requests and other correspondence: R. Heidelberger, Department of Neurobiology and Anatomy, MSB 7.046, University of Texas Medical School at Houston, 6431 Fannin Street, Houston, TX 77025 (E-mail: ruth.heidelberger{at}uth.tmc.edu)






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