Properties of Multivesicular Release from Mouse Rod Photoreceptors Support Transmission of Single-photon Responses

Overview

Journal Elife

Specialty Biology

Date 2021 Mar 26

PMID 33769285

Citations 10

Authors

Cassandra L Hays

Asia L Sladek

Greg D Field

Wallace B Thoreson

Affiliations

Soon will be listed here.

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.

Citing Articles

The architecture of invaginating rod synapses slows glutamate diffusion and shapes synaptic responses.

Thoreson W, Bartol T, Conoan N, Diamond J J Gen Physiol. 2025; 157(3).

PMID: 40019452 PMC: 11869902. DOI: 10.1085/jgp.202413746.

The Structural and Functional Integrity of Rod Photoreceptor Ribbon Synapses Depends on Redundant Actions of Dynamins 1 and 3.

Hanke-Gogokhia C, Zapadka T, Finkelstein S, Klingeborn M, Maugel T, Singer J J Neurosci. 2024; 44(25).

PMID: 38641407 PMC: 11209669. DOI: 10.1523/JNEUROSCI.1379-23.2024.

Origin of Discrete and Continuous Dark Noise in Rod Photoreceptors.

Bocchero U, Pahlberg J eNeuro. 2023; 10(11).

PMID: 37973380 PMC: 10687842. DOI: 10.1523/ENEURO.0390-23.2023.

EAAT5 glutamate transporter rapidly binds glutamate with micromolar affinity in mouse rods.

Thoreson W, Chhunchha B J Gen Physiol. 2023; 155(9).

PMID: 37477643 PMC: 10359920. DOI: 10.1085/jgp.202313349.

Rabconnectin-3α/DMXL2 Is Locally Enriched at the Synaptic Ribbon of Rod Photoreceptor Synapses.

Dittrich A, Ramesh G, Jung M, Schmitz F Cells. 2023; 12(12).

PMID: 37371135 PMC: 10297199. DOI: 10.3390/cells12121665.

References

Van Rossum M, Smith R . Noise removal at the rod synapse of mammalian retina. Vis Neurosci. 1998; 15(5):809-21. DOI: 10.1017/s0952523898155037. View

Gross O, Pugh Jr E, Burns M . cGMP in mouse rods: the spatiotemporal dynamics underlying single photon responses. Front Mol Neurosci. 2015; 8:6. PMC: 4349151. DOI: 10.3389/fnmol.2015.00006. View

Fu Y, Kefalov V, Luo D, Xue T, Yau K . Quantal noise from human red cone pigment. Nat Neurosci. 2008; 11(5):565-71. PMC: 2774794. DOI: 10.1038/nn.2110. View

Malagon G, Miki T, Llano I, Neher E, Marty A . Counting Vesicular Release Events Reveals Binomial Release Statistics at Single Glutamatergic Synapses. J Neurosci. 2016; 36(14):4010-25. PMC: 6705515. DOI: 10.1523/JNEUROSCI.4352-15.2016. View

Okawa H, Miyagishima K, Arman A, Hurley J, Field G, Sampath A . Optimal processing of photoreceptor signals is required to maximize behavioural sensitivity. J Physiol. 2010; 588(Pt 11):1947-60. PMC: 2901982. DOI: 10.1113/jphysiol.2010.188573. View

Kavalali E . Spontaneous neurotransmission: A form of neural communication comes of age. J Neurosci Res. 2017; 96(3):331-334. PMC: 5766395. DOI: 10.1002/jnr.24207. View

Cork K, Van Hook M, Thoreson W . Mechanisms, pools, and sites of spontaneous vesicle release at synapses of rod and cone photoreceptors. Eur J Neurosci. 2016; 44(3):2015-27. PMC: 4969212. DOI: 10.1111/ejn.13288. View

Sampath A, Rieke F . Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron. 2004; 41(3):431-43. DOI: 10.1016/s0896-6273(04)00005-4. View

Hasegawa J, Obara T, Tanaka K, Tachibana M . High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron. 2006; 50(1):63-74. DOI: 10.1016/j.neuron.2006.02.022. View

10.

Field G, Rieke F . Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron. 2002; 34(5):773-85. DOI: 10.1016/s0896-6273(02)00700-6. View

11.

Trexler E, Casti A, Zhang Y . Nonlinearity and noise at the rod-rod bipolar cell synapse. Vis Neurosci. 2010; 28(1):61-8. PMC: 3058690. DOI: 10.1017/S0952523810000301. View

12.

Behrens C, Schubert T, Haverkamp S, Euler T, Berens P . Connectivity map of bipolar cells and photoreceptors in the mouse retina. Elife. 2016; 5. PMC: 5148610. DOI: 10.7554/eLife.20041. View

13.

Yue W, Frederiksen R, Ren X, Luo D, Yamashita T, Shichida Y . Spontaneous activation of visual pigments in relation to openness/closedness of chromophore-binding pocket. Elife. 2017; 6. PMC: 5302883. DOI: 10.7554/eLife.18492. View

14.

Schneeweis D, Schnapf J . Photovoltage of rods and cones in the macaque retina. Science. 1995; 268(5213):1053-6. DOI: 10.1126/science.7754386. View

15.

Zampighi G, Schietroma C, Zampighi L, Woodruff M, Wright E, Brecha N . Conical tomography of a ribbon synapse: structural evidence for vesicle fusion. PLoS One. 2011; 6(3):e16944. PMC: 3046965. DOI: 10.1371/journal.pone.0016944. View

16.

Schein S, Ahmad K . Efficiency of synaptic transmission of single-photon events from rod photoreceptor to rod bipolar dendrite. Biophys J. 2006; 91(9):3257-67. PMC: 1614493. DOI: 10.1529/biophysj.106.091744. View

17.

Arriza J, Eliasof S, Kavanaugh M, Amara S . Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci U S A. 1997; 94(8):4155-60. PMC: 20584. DOI: 10.1073/pnas.94.8.4155. View

18.

Kavalali E . The mechanisms and functions of spontaneous neurotransmitter release. Nat Rev Neurosci. 2014; 16(1):5-16. DOI: 10.1038/nrn3875. View

19.

Berntson A, Smith R, Taylor W . Transmission of single photon signals through a binary synapse in the mammalian retina. Vis Neurosci. 2005; 21(5):693-702. DOI: 10.1017/S0952523804215048. View

20.

Tsukamoto Y, Omi N . Functional allocation of synaptic contacts in microcircuits from rods via rod bipolar to AII amacrine cells in the mouse retina. J Comp Neurol. 2013; 521(15):3541-55. PMC: 4265793. DOI: 10.1002/cne.23370. View