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Ultrafast light targeting for high-throughput precise control of neuronal networks

Two-photon, single-cell resolution optogenetics based on holographic light-targeting approaches enables the generation of precise spatiotemporal neuronal activity patterns and thus a broad range of experimental applications, such as high throughput connectivity mapping and probing neural codes for p...

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Autores principales: Faini, Giulia, Tanese, Dimitrii, Molinier, Clément, Telliez, Cécile, Hamdani, Massilia, Blot, Francois, Tourain, Christophe, de Sars, Vincent, Del Bene, Filippo, Forget, Benoît C., Ronzitti, Emiliano, Emiliani, Valentina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10074378/
https://www.ncbi.nlm.nih.gov/pubmed/37019891
http://dx.doi.org/10.1038/s41467-023-37416-w
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author Faini, Giulia
Tanese, Dimitrii
Molinier, Clément
Telliez, Cécile
Hamdani, Massilia
Blot, Francois
Tourain, Christophe
de Sars, Vincent
Del Bene, Filippo
Forget, Benoît C.
Ronzitti, Emiliano
Emiliani, Valentina
author_facet Faini, Giulia
Tanese, Dimitrii
Molinier, Clément
Telliez, Cécile
Hamdani, Massilia
Blot, Francois
Tourain, Christophe
de Sars, Vincent
Del Bene, Filippo
Forget, Benoît C.
Ronzitti, Emiliano
Emiliani, Valentina
author_sort Faini, Giulia
collection PubMed
description Two-photon, single-cell resolution optogenetics based on holographic light-targeting approaches enables the generation of precise spatiotemporal neuronal activity patterns and thus a broad range of experimental applications, such as high throughput connectivity mapping and probing neural codes for perception. Yet, current holographic approaches limit the resolution for tuning the relative spiking time of distinct cells to a few milliseconds, and the achievable number of targets to 100-200, depending on the working depth. To overcome these limitations and expand the capabilities of single-cell optogenetics, we introduce an ultra-fast sequential light targeting (FLiT) optical configuration based on the rapid switching of a temporally focused beam between holograms at kHz rates. We used FLiT to demonstrate two illumination protocols, termed hybrid- and cyclic-illumination, and achieve sub-millisecond control of sequential neuronal activation and high throughput multicell illumination in vitro (mouse organotypic and acute brain slices) and in vivo (zebrafish larvae and mice), while minimizing light-induced thermal rise. These approaches will be important for experiments that require rapid and precise cell stimulation with defined spatio-temporal activity patterns and optical control of large neuronal ensembles.
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spelling pubmed-100743782023-04-05 Ultrafast light targeting for high-throughput precise control of neuronal networks Faini, Giulia Tanese, Dimitrii Molinier, Clément Telliez, Cécile Hamdani, Massilia Blot, Francois Tourain, Christophe de Sars, Vincent Del Bene, Filippo Forget, Benoît C. Ronzitti, Emiliano Emiliani, Valentina Nat Commun Article Two-photon, single-cell resolution optogenetics based on holographic light-targeting approaches enables the generation of precise spatiotemporal neuronal activity patterns and thus a broad range of experimental applications, such as high throughput connectivity mapping and probing neural codes for perception. Yet, current holographic approaches limit the resolution for tuning the relative spiking time of distinct cells to a few milliseconds, and the achievable number of targets to 100-200, depending on the working depth. To overcome these limitations and expand the capabilities of single-cell optogenetics, we introduce an ultra-fast sequential light targeting (FLiT) optical configuration based on the rapid switching of a temporally focused beam between holograms at kHz rates. We used FLiT to demonstrate two illumination protocols, termed hybrid- and cyclic-illumination, and achieve sub-millisecond control of sequential neuronal activation and high throughput multicell illumination in vitro (mouse organotypic and acute brain slices) and in vivo (zebrafish larvae and mice), while minimizing light-induced thermal rise. These approaches will be important for experiments that require rapid and precise cell stimulation with defined spatio-temporal activity patterns and optical control of large neuronal ensembles. Nature Publishing Group UK 2023-04-05 /pmc/articles/PMC10074378/ /pubmed/37019891 http://dx.doi.org/10.1038/s41467-023-37416-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Faini, Giulia
Tanese, Dimitrii
Molinier, Clément
Telliez, Cécile
Hamdani, Massilia
Blot, Francois
Tourain, Christophe
de Sars, Vincent
Del Bene, Filippo
Forget, Benoît C.
Ronzitti, Emiliano
Emiliani, Valentina
Ultrafast light targeting for high-throughput precise control of neuronal networks
title Ultrafast light targeting for high-throughput precise control of neuronal networks
title_full Ultrafast light targeting for high-throughput precise control of neuronal networks
title_fullStr Ultrafast light targeting for high-throughput precise control of neuronal networks
title_full_unstemmed Ultrafast light targeting for high-throughput precise control of neuronal networks
title_short Ultrafast light targeting for high-throughput precise control of neuronal networks
title_sort ultrafast light targeting for high-throughput precise control of neuronal networks
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10074378/
https://www.ncbi.nlm.nih.gov/pubmed/37019891
http://dx.doi.org/10.1038/s41467-023-37416-w
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