Rapid and reversible optogenetic silencing of synaptic transmission by clustering of synaptic vesicles

Dennis Vettkötter, Martin Schneider, Brady D. Goulden, Holger Dill, Jana Liewald, Sandra Zeiler, Julia Guldan, Yilmaz Arda Ateş, Shigeki Watanabe and Alexander Gottschalk ()
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Dennis Vettkötter: Goethe University
Martin Schneider: Goethe University
Brady D. Goulden: Johns Hopkins University
Holger Dill: Goethe University
Jana Liewald: Goethe University
Sandra Zeiler: Goethe University
Julia Guldan: Goethe University
Yilmaz Arda Ateş: Goethe University
Shigeki Watanabe: Johns Hopkins University
Alexander Gottschalk: Goethe University

Nature Communications, 2022, vol. 13, issue 1, 1-17

Abstract: Abstract Acutely silencing specific neurons informs about their functional roles in circuits and behavior. Existing optogenetic silencers include ion pumps, channels, metabotropic receptors, and tools that damage the neurotransmitter release machinery. While the former hyperpolarize the cell, alter ionic gradients or cellular biochemistry, the latter allow only slow recovery, requiring de novo synthesis. Thus, tools combining fast activation and reversibility are needed. Here, we use light-evoked homo-oligomerization of cryptochrome CRY2 to silence synaptic transmission, by clustering synaptic vesicles (SVs). We benchmark this tool, optoSynC, in Caenorhabditis elegans, zebrafish, and murine hippocampal neurons. optoSynC clusters SVs, observable by electron microscopy. Locomotion silencing occurs with tauon ~7.2 s and recovers with tauoff ~6.5 min after light-off. optoSynC can inhibit exocytosis for several hours, at very low light intensities, does not affect ion currents, biochemistry or synaptic proteins, and may further allow manipulating different SV pools and the transfer of SVs between them.

Date: 2022
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DOI: 10.1038/s41467-022-35324-z

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