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Thermogenetic neurostimulation with single-cell resolution

Yulia G. Ermakova, Aleksandr A. Lanin, Ilya V. Fedotov, Matvey Roshchin, Ilya V. Kelmanson, Dmitry Kulik, Yulia A. Bogdanova, Arina G. Shokhina, Dmitry S. Bilan, Dmitry B. Staroverov, Pavel M. Balaban, Andrei B. Fedotov, Dmitry A. Sidorov-Biryukov, Evgeny S. Nikitin, Aleksei M. Zheltikov () and Vsevolod V. Belousov ()
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Yulia G. Ermakova: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Aleksandr A. Lanin: International Laser Center, M.V. Lomonosov Moscow State University
Ilya V. Fedotov: International Laser Center, M.V. Lomonosov Moscow State University
Matvey Roshchin: Institute of Higher Nervous Activity and Neurophysiology
Ilya V. Kelmanson: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Dmitry Kulik: International Laser Center, M.V. Lomonosov Moscow State University
Yulia A. Bogdanova: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Arina G. Shokhina: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Dmitry S. Bilan: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Dmitry B. Staroverov: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences
Pavel M. Balaban: Institute of Higher Nervous Activity and Neurophysiology
Andrei B. Fedotov: International Laser Center, M.V. Lomonosov Moscow State University
Dmitry A. Sidorov-Biryukov: International Laser Center, M.V. Lomonosov Moscow State University
Evgeny S. Nikitin: Institute of Higher Nervous Activity and Neurophysiology
Aleksei M. Zheltikov: International Laser Center, M.V. Lomonosov Moscow State University
Vsevolod V. Belousov: Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

Nature Communications, 2017, vol. 8, issue 1, 1-15

Abstract: Abstract Thermogenetics is a promising innovative neurostimulation technique, which enables robust activation of neurons using thermosensitive transient receptor potential (TRP) cation channels. Broader application of this approach in neuroscience is, however, hindered by a limited variety of suitable ion channels, and by low spatial and temporal resolution of neuronal activation when TRP channels are activated by ambient temperature variations or chemical agonists. Here, we demonstrate rapid, robust and reproducible repeated activation of snake TRPA1 channels heterologously expressed in non-neuronal cells, mouse neurons and zebrafish neurons in vivo by infrared (IR) laser radiation. A fibre-optic probe that integrates a nitrogen−vacancy (NV) diamond quantum sensor with optical and microwave waveguide delivery enables thermometry with single-cell resolution, allowing neurons to be activated by exceptionally mild heating, thus preventing the damaging effects of excessive heat. The neuronal responses to the activation by IR laser radiation are fully characterized using Ca2+ imaging and electrophysiology, providing, for the first time, a complete framework for a thermogenetic manipulation of individual neurons using IR light.

Date: 2017
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DOI: 10.1038/ncomms15362

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