IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37416-w.html
   My bibliography  Save this article

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

Author

Listed:
  • 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)

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.

Suggested Citation

  • Giulia Faini & Dimitrii Tanese & Clément Molinier & Cécile Telliez & Massilia Hamdani & Francois Blot & Christophe Tourain & Vincent Sars & Filippo Bene & Benoît C. Forget & Emiliano Ronzitti & Valent, 2023. "Ultrafast light targeting for high-throughput precise control of neuronal networks," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37416-w
    DOI: 10.1038/s41467-023-37416-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37416-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37416-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ofer Yizhar & Lief E. Fenno & Matthias Prigge & Franziska Schneider & Thomas J. Davidson & Daniel J. O’Shea & Vikaas S. Sohal & Inbal Goshen & Joel Finkelstein & Jeanne T. Paz & Katja Stehfest & Roman, 2011. "Neocortical excitation/inhibition balance in information processing and social dysfunction," Nature, Nature, vol. 477(7363), pages 171-178, September.
    2. Oscar Hernandez & Eirini Papagiakoumou & Dimitrii Tanese & Kevin Fidelin & Claire Wyart & Valentina Emiliani, 2016. "Three-dimensional spatiotemporal focusing of holographic patterns," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    3. Selmaan N. Chettih & Christopher D. Harvey, 2019. "Single-neuron perturbations reveal feature-specific competition in V1," Nature, Nature, vol. 567(7748), pages 334-340, March.
    4. Robert C. Froemke & Yang Dan, 2002. "Spike-timing-dependent synaptic modification induced by natural spike trains," Nature, Nature, vol. 416(6879), pages 433-438, March.
    5. Yoav Printz & Pritish Patil & Mathias Mahn & Asaf Benjamin & Anna Litvin & Rivka Levy & Max Bringmann & Ofer Yizhar, 2023. "Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Matt Udakis & Victor Pedrosa & Sophie E. L. Chamberlain & Claudia Clopath & Jack R. Mellor, 2020. "Interneuron-specific plasticity at parvalbumin and somatostatin inhibitory synapses onto CA1 pyramidal neurons shapes hippocampal output," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Caio Vaz Rimoli & Claudio Moretti & Fernando Soldevila & Enora Brémont & Cathie Ventalon & Sylvain Gigan, 2024. "Demixing fluorescence time traces transmitted by multimode fibers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Ruth R. Sims & Imane Bendifallah & Christiane Grimm & Aysha S. Mohamed Lafirdeen & Soledad Domínguez & Chung Yuen Chan & Xiaoyu Lu & Benoît C. Forget & François St-Pierre & Eirini Papagiakoumou & Vale, 2024. "Scanless two-photon voltage imaging," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Lloyd E. Russell & Mehmet Fişek & Zidan Yang & Lynn Pei Tan & Adam M. Packer & Henry W. P. Dalgleish & Selmaan N. Chettih & Christopher D. Harvey & Michael Häusser, 2024. "The influence of cortical activity on perception depends on behavioral state and sensory context," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Bettina Voelcker & Ravi Pancholi & Simon Peron, 2022. "Transformation of primary sensory cortical representations from layer 4 to layer 2," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Jan C. Frankowski & Alexa Tierno & Shreya Pavani & Quincy Cao & David C. Lyon & Robert F. Hunt, 2022. "Brain-wide reconstruction of inhibitory circuits after traumatic brain injury," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Alexandre Castonguay & Sébastien Thomas & Frédéric Lesage & Christian Casanova, 2014. "Repetitive and Retinotopically Restricted Activation of the Dorsal Lateral Geniculate Nucleus with Optogenetics," PLOS ONE, Public Library of Science, vol. 9(4), pages 1-8, April.
    5. Brandon W. Hughes & Jessica L. Huebschman & Evgeny Tsvetkov & Benjamin M. Siemsen & Kirsten K. Snyder & Rose Marie Akiki & Daniel J. Wood & Rachel D. Penrod & Michael D. Scofield & Stefano Berto & Mak, 2024. "NPAS4 supports cocaine-conditioned cues in rodents by controlling the cell type-specific activation balance in the nucleus accumbens," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Gregory Lepeu & Ellen Maren & Kristina Slabeva & Cecilia Friedrichs-Maeder & Markus Fuchs & Werner J. Z’Graggen & Claudio Pollo & Kaspar A. Schindler & Antoine Adamantidis & Timothée Proix & Maxime O., 2024. "The critical dynamics of hippocampal seizures," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Pan Xu & Yuanlei Yue & Juntao Su & Xiaoqian Sun & Hongfei Du & Zhichao Liu & Rahul Simha & Jianhui Zhou & Chen Zeng & Hui Lu, 2022. "Pattern decorrelation in the mouse medial prefrontal cortex enables social preference and requires MeCP2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Yu-Jun Wang & Gui-Ying Zan & Cenglin Xu & Xue-Ping Li & Xuelian Shu & Song-Yu Yao & Xiao-Shan Xu & Xiaoyun Qiu & Yexiang Chen & Kai Jin & Qi-Xin Zhou & Jia-Yu Ye & Yi Wang & Lin Xu & Zhong Chen & Jing, 2023. "The claustrum-prelimbic cortex circuit through dynorphin/κ-opioid receptor signaling underlies depression-like behaviors associated with social stress etiology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Yu, Haitao & Guo, Xinmeng & Wang, Jiang & Deng, Bin & Wei, Xile, 2015. "Spike coherence and synchronization on Newman–Watts small-world neuronal networks modulated by spike-timing-dependent plasticity," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 419(C), pages 307-317.
    10. Yanyun Ren & Xiaobo Bu & Ming Wang & Yue Gong & Junjie Wang & Yuyang Yang & Guijun Li & Meng Zhang & Ye Zhou & Su-Ting Han, 2022. "Synaptic plasticity in self-powered artificial striate cortex for binocular orientation selectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    11. Jung Ho Hyun & Kenichiro Nagahama & Ho Namkung & Neymi Mignocchi & Seung-Eon Roh & Patrick Hannan & Sarah Krüssel & Chuljung Kwak & Abigail McElroy & Bian Liu & Mingguang Cui & Seunghwan Lee & Dongmin, 2022. "Tagging active neurons by soma-targeted Cal-Light," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Gabriel Koch Ocker & Ashok Litwin-Kumar & Brent Doiron, 2015. "Self-Organization of Microcircuits in Networks of Spiking Neurons with Plastic Synapses," PLOS Computational Biology, Public Library of Science, vol. 11(8), pages 1-40, August.
    13. Henry W. Kietzman & Gracy Trinoskey-Rice & Sarah A. Blumenthal & Jidong D. Guo & Shannon L. Gourley, 2022. "Social incentivization of instrumental choice in mice requires amygdala-prelimbic cortex-nucleus accumbens connectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Noemi S Araújo & Selvin Z Reyes-Garcia & João A F Brogin & Douglas D Bueno & Esper A Cavalheiro & Carla A Scorza & Jean Faber, 2022. "Chaotic and stochastic dynamics of epileptiform-like activities in sclerotic hippocampus resected from patients with pharmacoresistant epilepsy," PLOS Computational Biology, Public Library of Science, vol. 18(4), pages 1-31, April.
    15. Barbara Feulner & Matthew G. Perich & Raeed H. Chowdhury & Lee E. Miller & Juan A. Gallego & Claudia Clopath, 2022. "Small, correlated changes in synaptic connectivity may facilitate rapid motor learning," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Can Tao & Guang-Wei Zhang & Wen-Jian Sun & Junxiang J. Huang & Li I. Zhang & Huizhong Whit Tao, 2024. "Excitation-inhibition imbalance in medial preoptic area circuits underlies chronic stress-induced depression-like states," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Ruth R. Sims & Imane Bendifallah & Christiane Grimm & Aysha S. Mohamed Lafirdeen & Soledad Domínguez & Chung Yuen Chan & Xiaoyu Lu & Benoît C. Forget & François St-Pierre & Eirini Papagiakoumou & Vale, 2024. "Scanless two-photon voltage imaging," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    18. Qingtao Sun & Jianping Zhang & Anan Li & Mei Yao & Guangcai Liu & Siqi Chen & Yue Luo & Zhi Wang & Hui Gong & Xiangning Li & Qingming Luo, 2022. "Acetylcholine deficiency disrupts extratelencephalic projection neurons in the prefrontal cortex in a mouse model of Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    19. Pfaffelhuber, P. & Rotter, S. & Stiefel, J., 2022. "Mean-field limits for non-linear Hawkes processes with excitation and inhibition," Stochastic Processes and their Applications, Elsevier, vol. 153(C), pages 57-78.
    20. Luye Qin & Jamal B. Williams & Tao Tan & Tiaotiao Liu & Qing Cao & Kaijie Ma & Zhen Yan, 2021. "Deficiency of autism risk factor ASH1L in prefrontal cortex induces epigenetic aberrations and seizures," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37416-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.