Optogenetics at the Presynapse

Overview

Journal Nat Neurosci

Date 2022 Jul 14

PMID 35835882

Authors

Benjamin R Rost

Jonas Wietek

Ofer Yizhar

Dietmar Schmitz

Affiliations

Soon will be listed here.

Abstract

Optogenetic actuators enable highly precise spatiotemporal interrogation of biological processes at levels ranging from the subcellular to cells, circuits and behaving organisms. Although their application in neuroscience has traditionally focused on the control of spiking activity at the somatodendritic level, the scope of optogenetic modulators for direct manipulation of presynaptic functions is growing. Presynaptically localized opsins combined with light stimulation at the terminals allow light-mediated neurotransmitter release, presynaptic inhibition, induction of synaptic plasticity and specific manipulation of individual components of the presynaptic machinery. Here, we describe presynaptic applications of optogenetic tools in the context of the unique cell biology of axonal terminals, discuss their potential shortcomings and outline future directions for this rapidly developing research area.

Citing Articles

Flexible electronic-photonic 3D integration from ultrathin polymer chiplets.

Huang Y, Li G, Bai T, Shin Y, Wang X, More A Npj Flex Electron. 2025; 8.

PMID: 39780990 PMC: 11709425. DOI: 10.1038/s41528-024-00344-w.

Distinct release properties of glutamate/GABA co-transmission serve as a frequency-dependent filtering of supramammillary inputs.

Hirai H, Konno K, Yamasaki M, Watanabe M, Sakaba T, Hashimotodani Y Elife. 2024; 13.

PMID: 39680436 PMC: 11649240. DOI: 10.7554/eLife.99711.

Sparsity of Population Activity in the Hippocampus Is Task-Invariant Across the Trisynaptic Circuit and Dorsoventral Axis.

Lee J, Nielsen M, McHugh R, Morgan E, Hong N, Sutherland R Hippocampus. 2024; 35(1):e23651.

PMID: 39620324 PMC: 11610716. DOI: 10.1002/hipo.23651.

Leptin-activated hypothalamic BNC2 neurons acutely suppress food intake.

Tan H, Yin L, Tan Y, Ivanov J, Plucinska K, Ilanges A Nature. 2024; 636(8041):198-205.

PMID: 39478220 PMC: 11618066. DOI: 10.1038/s41586-024-08108-2.

The Neural and Computational Architecture of Feedback Dynamics in Mouse Cortex during Stimulus Report.

Ciceri S, Oude Lohuis M, Rottschafer V, Pennartz C, Avitabile D, van Gaal S eNeuro. 2024; 11(9).

PMID: 39260892 PMC: 11444237. DOI: 10.1523/ENEURO.0191-24.2024.

References

Fenno L, Yizhar O, Deisseroth K . The development and application of optogenetics. Annu Rev Neurosci. 2011; 34:389-412. PMC: 6699620. DOI: 10.1146/annurev-neuro-061010-113817. View

Zhou X, Pan M, Lin M . Investigating neuronal function with optically controllable proteins. Front Mol Neurosci. 2015; 8:37. PMC: 4508517. DOI: 10.3389/fnmol.2015.00037. View

Kim C, Adhikari A, Deisseroth K . Integration of optogenetics with complementary methodologies in systems neuroscience. Nat Rev Neurosci. 2017; 18(4):222-235. PMC: 5708544. DOI: 10.1038/nrn.2017.15. View

Rost B, Schneider-Warme F, Schmitz D, Hegemann P . Optogenetic Tools for Subcellular Applications in Neuroscience. Neuron. 2017; 96(3):572-603. DOI: 10.1016/j.neuron.2017.09.047. View

Abbott L, Regehr W . Synaptic computation. Nature. 2004; 431(7010):796-803. DOI: 10.1038/nature03010. View

Rozenberg A, Inoue K, Kandori H, Beja O . Microbial Rhodopsins: The Last Two Decades. Annu Rev Microbiol. 2021; 75:427-447. DOI: 10.1146/annurev-micro-031721-020452. View

Govorunova E, Sineshchekov O, Li H, Spudich J . Microbial Rhodopsins: Diversity, Mechanisms, and Optogenetic Applications. Annu Rev Biochem. 2017; 86:845-872. PMC: 5747503. DOI: 10.1146/annurev-biochem-101910-144233. View

Kuhne J, Vierock J, Tennigkeit S, Dreier M, Wietek J, Petersen D . Unifying photocycle model for light adaptation and temporal evolution of cation conductance in channelrhodopsin-2. Proc Natl Acad Sci U S A. 2019; 116(19):9380-9389. PMC: 6510988. DOI: 10.1073/pnas.1818707116. View

Wietek J, Prigge M . Enhancing Channelrhodopsins: An Overview. Methods Mol Biol. 2016; 1408:141-65. DOI: 10.1007/978-1-4939-3512-3_10. View

10.

Vierock J, Grimm C, Nitzan N, Hegemann P . Molecular determinants of proton selectivity and gating in the red-light activated channelrhodopsin Chrimson. Sci Rep. 2017; 7(1):9928. PMC: 5577340. DOI: 10.1038/s41598-017-09600-8. View

11.

Wietek J, Wiegert J, Adeishvili N, Schneider F, Watanabe H, Tsunoda S . Conversion of channelrhodopsin into a light-gated chloride channel. Science. 2014; 344(6182):409-12. DOI: 10.1126/science.1249375. View

12.

Berndt A, Lee S, Ramakrishnan C, Deisseroth K . Structure-guided transformation of channelrhodopsin into a light-activated chloride channel. Science. 2014; 344(6182):420-4. PMC: 4096039. DOI: 10.1126/science.1252367. View

13.

Govorunova E, Sineshchekov O, Janz R, Liu X, Spudich J . NEUROSCIENCE. Natural light-gated anion channels: A family of microbial rhodopsins for advanced optogenetics. Science. 2015; 349(6248):647-50. PMC: 4764398. DOI: 10.1126/science.aaa7484. View

14.

Mahn M, Gibor L, Patil P, Malina K, Oring S, Printz Y . High-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins. Nat Commun. 2018; 9(1):4125. PMC: 6175909. DOI: 10.1038/s41467-018-06511-8. View

15.

Malyshev A, Roshchin M, Smirnova G, Dolgikh D, Balaban P, Ostrovsky M . Chloride conducting light activated channel GtACR2 can produce both cessation of firing and generation of action potentials in cortical neurons in response to light. Neurosci Lett. 2017; 640:76-80. DOI: 10.1016/j.neulet.2017.01.026. View

16.

Inoue K . Diversity, Mechanism, and Optogenetic Application of Light-Driven Ion Pump Rhodopsins. Adv Exp Med Biol. 2021; 1293:89-126. DOI: 10.1007/978-981-15-8763-4_6. View

17.

Mahn M, Prigge M, Ron S, Levy R, Yizhar O . Biophysical constraints of optogenetic inhibition at presynaptic terminals. Nat Neurosci. 2016; 19(4):554-6. PMC: 4926958. DOI: 10.1038/nn.4266. View

18.

Raimondo J, Kay L, Ellender T, Akerman C . Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission. Nat Neurosci. 2012; 15(8):1102-4. PMC: 3428858. DOI: 10.1038/nn.3143. View

19.

Gao S, Nagpal J, Schneider M, Kozjak-Pavlovic V, Nagel G, Gottschalk A . Optogenetic manipulation of cGMP in cells and animals by the tightly light-regulated guanylyl-cyclase opsin CyclOp. Nat Commun. 2015; 6:8046. PMC: 4569695. DOI: 10.1038/ncomms9046. View

20.

Scheib U, Broser M, Constantin O, Yang S, Gao S, Mukherjee S . Rhodopsin-cyclases for photocontrol of cGMP/cAMP and 2.3 Å structure of the adenylyl cyclase domain. Nat Commun. 2018; 9(1):2046. PMC: 5967339. DOI: 10.1038/s41467-018-04428-w. View