The Journal of Neurophysiology Vol. 80 No. 6 December 1998, pp. 3163-3172
Copyright ©1998 The American Physiological Society

Transmitter Concentration at a Three-Dimensional Synapse

Rukmini Rao-Mirotznik², Gershon Buchsbaum², and Peter Sterling¹

¹ Department of Neuroscience and ² Department of Bioengineering, University of Pennsylvania, Philadelphia, Pennsylvania 19104

Rao-Mirotznik, Rukmini, Gershon Buchsbaum, and Peter Sterling. Transmitter concentration at a three-dimensional synapse. J. Neurophysiol. 80: 3163-3172, 1998. At intensities from starlight to 1000-fold brighter, the mammalian rod synapse transmits a binary signal, the capture of 0 or 1 photon. Zero is signified by tonic exocytosis, and 1 is signified by a brief pause. The synapse is three dimensional: vesicles discharge at the apex of a deep cleft created by the invagination of four postsynaptic processes. Two horizontal cell spines bearing -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors reach near to the release sites (16 nm), and two bipolar dendrites bearing mGluR6 receptors end far from the release sites (up to 640 nm). We considered two hypotheses for signal transfer: transmitter quanta might be integrated in the cleft and sensed as a steady concentration (high for 0 and low for 1); or quanta might be sensed at the postsynaptic membrane as discrete postsynaptic potentials (PSPs) and integrated within the dendrite. We calculate from a passive diffusion model that the invagination empties rapidly ( ~ 1.7 ms). Further calculations suggest that a glutamate concentration high enough to hold a bipolar cell in darkness at one end of its response range would require ~4,000 vesicles/s. On the other hand, the glutamate pulse from a single vesicle would reach both nearby AMPA receptors (low affinity) and distant mGluR6 receptors (high affinity) at spatiotemporal concentrations matched to their apparent binding affinities. Thus one vesicle could evoke a discrete PSP in all four postsynaptic processes. We calculate from a stochastic model that PSPs could transfer the binary signal at ~100 vesicles/s. Thus dendritic integration of unitary PSPs is both plausible and 40-fold more efficient than the alternative mechanism. The rod's deep invagination, rather than serving to pool transmitter, may serve to prevent "spillover" of transmitter to neighboring rods. Spillover, by pooling the noise from neighboring rods, would impair transmission of their binary signals.

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