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

Giulia Faini, Dimitrii Tanese, Clément Molinier, Cécile Telliez, Massilia Hamdani, Francois Blot, Christophe Tourain, Vincent Sars, Filippo Bene, Benoît C. Forget, Emiliano Ronzitti () and Valentina Emiliani ()
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Giulia Faini: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Dimitrii Tanese: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Clément Molinier: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Cécile Telliez: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Massilia Hamdani: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Francois Blot: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Christophe Tourain: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Vincent Sars: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Filippo Bene: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Benoît C. Forget: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Emiliano Ronzitti: Sorbonne Université, INSERM, CNRS, Institut de la Vision
Valentina Emiliani: Sorbonne Université, INSERM, CNRS, Institut de la Vision

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41467-023-37416-w

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