Vision under starlight requires rod photoreceptors to transduce and transmit single photon responses to the visual system. This remarkable sensitivity depends on a small voltage change reliably reducing glutamate release such that post-synaptic rod bipolar cells can robustly detect the signal. To transmit this small signal, we have found that rod vesicle release deviates strongly from a Poisson process under conditions that mimic darkness. Specifically, at their resting membrane potential in darkness, rods exhibit coordinated and regularly timed multivesicular release events. Each release event consisted of ~17 vesicles and occurred 2-3 times more regularly than expected from a Poisson process. Hyperpolarizing rods to mimic the voltage change produced by a single photon response abruptly reduced the probability of multivesicular release nearly to zero with a rebound increase in release probability at stimulus offset. Simulations of these release dynamics indicate that this regularly timed, multivesicular release promotes transmission of single photon responses to post-synaptic neurons. Furthermore, the mechanism is efficient, requiring fewer vesicles to be released per second than uniquantal release governed by Poisson statistics.
bioRxiv Subject Collection: Neuroscience