Abstract
Vision under starlight requires rod photoreceptors to transduce and transmit single-photon responses to the visual system. Small single-photon voltage changes must therefore cause detectable reductions in glutamate release. We found that rods achieve this by employing mechanisms that enhance release regularity and its sensitivity to small voltage changes. At the resting membrane potential in darkness, mouse rods exhibit coordinated and regularly timed multivesicular release events, each consisting of ~17 vesicles and occurring two to three times more regularly than predicted by Poisson statistics. Hyperpolarizing rods to mimic the voltage change produced by a single photon abruptly reduced the probability of multivesicular release nearly to zero with a rebound increase at stimulus offset. Simulations of these release dynamics indicate that this regularly timed, multivesicular release promotes transmission of single-photon responses to post-synaptic rod-bipolar cells. Furthermore, the mechanism is efficient, requiring lower overall release rates than uniquantal release governed by Poisson statistics.
Highlights
One of the most impressive features of the visual system is the ability to detect single photons
Synaptic vesicle release is an intrinsically noisy process that is typically described by Poisson statistics (Malagon et al, 2016; Miki, 2019; Zhang and Peskin, 2015), posing a problem for post-synaptic bipolar cells to distinguish a genuine decrease in vesicle release caused by the absorption of a photon from a stochastic pause in vesicle release
When rods were held for many seconds at À60 or À70 mV, similar to the membrane potential achieved in bright light, we observed occasional inward currents arising from activation of glutamate transporters on the rod terminal (Figure 1; Grassmeyer et al, 2019)
Summary
One of the most impressive features of the visual system is the ability to detect single photons. Pioneering psychophysical studies showed that humans can detect flashes consisting of a few photons hitting the retina, indicating that individual rods can respond to the absorption of single photons and reliably signal these events to post-synaptic neurons (Barlow, 1956; Hecht et al, 1942; Sakitt, 1972; Tinsley et al, 2016). Rods signal the absorption of a photon to post-synaptic rod-bipolar cells by decreasing the rate of glutamate release. Synaptic vesicle release is an intrinsically noisy process that is typically described by Poisson statistics (Malagon et al, 2016; Miki, 2019; Zhang and Peskin, 2015), posing a problem for post-synaptic bipolar cells to distinguish a genuine decrease in vesicle release caused by the absorption of a photon from a stochastic pause in vesicle release. How does the rod transform a small voltage change into a sufficiently large and reliable change in vesicle release?
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