IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37622-6.html
   My bibliography  Save this article

All-optical closed-loop voltage clamp for precise control of muscles and neurons in live animals

Author

Listed:
  • Amelie C. F. Bergs

    (Goethe University
    Goethe University)

  • Jana F. Liewald

    (Goethe University
    Goethe University)

  • Silvia Rodriguez-Rozada

    (University Medical Center Hamburg-Eppendorf)

  • Qiang Liu

    (The Rockefeller University
    City University of Hong Kong)

  • Christin Wirt

    (Goethe University
    Goethe University)

  • Artur Bessel

    (Independent Researcher)

  • Nadja Zeitzschel

    (Goethe University
    Goethe University)

  • Hilal Durmaz

    (Goethe University
    Goethe University)

  • Adrianna Nozownik

    (University Medical Center Hamburg-Eppendorf)

  • Holger Dill

    (Goethe University
    Goethe University)

  • Maëlle Jospin

    (Université Claude Bernard Lyon 1, Institut NeuroMyoGène)

  • Johannes Vierock

    (Humboldt University)

  • Cornelia I. Bargmann

    (The Rockefeller University
    Chan Zuckerberg Initiative)

  • Peter Hegemann

    (Humboldt University)

  • J. Simon Wiegert

    (University Medical Center Hamburg-Eppendorf
    University of Heidelberg)

  • Alexander Gottschalk

    (Goethe University
    Goethe University)

Abstract

Excitable cells can be stimulated or inhibited by optogenetics. Since optogenetic actuation regimes are often static, neurons and circuits can quickly adapt, allowing perturbation, but not true control. Hence, we established an optogenetic voltage-clamp (OVC). The voltage-indicator QuasAr2 provides information for fast, closed-loop optical feedback to the bidirectional optogenetic actuator BiPOLES. Voltage-dependent fluorescence is held within tight margins, thus clamping the cell to distinct potentials. We established the OVC in muscles and neurons of Caenorhabditis elegans, and transferred it to rat hippocampal neurons in slice culture. Fluorescence signals were calibrated to electrically measured potentials, and wavelengths to currents, enabling to determine optical I/V-relationships. The OVC reports on homeostatically altered cellular physiology in mutants and on Ca2+-channel properties, and can dynamically clamp spiking in C. elegans. Combining non-invasive imaging with control capabilities of electrophysiology, the OVC facilitates high-throughput, contact-less electrophysiology in individual cells and paves the way for true optogenetic control in behaving animals.

Suggested Citation

  • Amelie C. F. Bergs & Jana F. Liewald & Silvia Rodriguez-Rozada & Qiang Liu & Christin Wirt & Artur Bessel & Nadja Zeitzschel & Hilal Durmaz & Adrianna Nozownik & Holger Dill & Maëlle Jospin & Johannes, 2023. "All-optical closed-loop voltage clamp for precise control of muscles and neurons in live animals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37622-6
    DOI: 10.1038/s41467-023-37622-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37622-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37622-6?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. Peng Zou & Yongxin Zhao & Adam D. Douglass & Daniel R. Hochbaum & Daan Brinks & Christopher A. Werley & D. Jed Harrison & Robert E. Campbell & Adam E. Cohen, 2014. "Bright and fast multicoloured voltage reporters via electrochromic FRET," Nature Communications, Nature, vol. 5(1), pages 1-10, December.
    2. Yiyang Gong & Mark J. Wagner & Jin Zhong Li & Mark J. Schnitzer, 2014. "Imaging neural spiking in brain tissue using FRET-opsin protein voltage sensors," Nature Communications, Nature, vol. 5(1), pages 1-11, May.
    3. Mathias Mahn & Lihi Gibor & Pritish Patil & Katayun Cohen-Kashi Malina & Shir Oring & Yoav Printz & Rivka Levy & Ilan Lampl & Ofer Yizhar, 2018. "High-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    4. Nicholas C. Flytzanis & Claire N. Bedbrook & Hui Chiu & Martin K. M. Engqvist & Cheng Xiao & Ken Y. Chan & Paul W. Sternberg & Frances H. Arnold & Viviana Gradinaru, 2014. "Archaerhodopsin variants with enhanced voltage-sensitive fluorescence in mammalian and Caenorhabditis elegans neurons," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    5. Feng Zhang & Li-Ping Wang & Martin Brauner & Jana F. Liewald & Kenneth Kay & Natalie Watzke & Phillip G. Wood & Ernst Bamberg & Georg Nagel & Alexander Gottschalk & Karl Deisseroth, 2007. "Multimodal fast optical interrogation of neural circuitry," Nature, Nature, vol. 446(7136), pages 633-639, April.
    6. Johannes Vierock & Silvia Rodriguez-Rozada & Alexander Dieter & Florian Pieper & Ruth Sims & Federico Tenedini & Amelie C. F. Bergs & Imane Bendifallah & Fangmin Zhou & Nadja Zeitzschel & Joachim Ahlb, 2021. "BiPOLES is an optogenetic tool developed for bidirectional dual-color control of neurons," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    7. Kazumasa Oda & Johannes Vierock & Satomi Oishi & Silvia Rodriguez-Rozada & Reiya Taniguchi & Keitaro Yamashita & J. Simon Wiegert & Tomohiro Nishizawa & Peter Hegemann & Osamu Nureki, 2018. "Crystal structure of the red light-activated channelrhodopsin Chrimson," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    8. Ping Liu & Bojun Chen & Zhao-Wen Wang, 2020. "GABAergic motor neurons bias locomotor decision-making in C. elegans," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    9. Yoav Adam & Jeong J. Kim & Shan Lou & Yongxin Zhao & Michael E. Xie & Daan Brinks & Hao Wu & Mohammed A. Mostajo-Radji & Simon Kheifets & Vicente Parot & Selmaan Chettih & Katherine J. Williams & Benj, 2019. "Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics," Nature, Nature, vol. 569(7756), pages 413-417, May.
    Full references (including those not matched with items on IDEAS)

    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. Lizhu Li & Lihui Lu & Yuqi Ren & Guo Tang & Yu Zhao & Xue Cai & Zhao Shi & He Ding & Changbo Liu & Dali Cheng & Yang Xie & Huachun Wang & Xin Fu & Lan Yin & Minmin Luo & Xing Sheng, 2022. "Colocalized, bidirectional optogenetic modulations in freely behaving mice with a wireless dual-color optoelectronic probe," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Dennis Vettkötter & Martin Schneider & Brady D. Goulden & Holger Dill & Jana Liewald & Sandra Zeiler & Julia Guldan & Yilmaz Arda Ateş & Shigeki Watanabe & Alexander Gottschalk, 2022. "Rapid and reversible optogenetic silencing of synaptic transmission by clustering of synaptic vesicles," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. David Eriksson & Artur Schneider & Anupriya Thirumalai & Mansour Alyahyay & Brice Crompe & Kirti Sharma & Patrick Ruther & Ilka Diester, 2022. "Multichannel optogenetics combined with laminar recordings for ultra-controlled neuronal interrogation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Stanislav Ott & Sangyu Xu & Nicole Lee & Ivan Hong & Jonathan Anns & Danesha Devini Suresh & Zhiyi Zhang & Xianyuan Zhang & Raihanah Harion & Weiying Ye & Vaishnavi Chandramouli & Suresh Jesuthasan & , 2024. "Kalium channelrhodopsins effectively inhibit neurons," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    5. Jianian Lin & Zongyue Cheng & Guang Yang & Meng Cui, 2022. "Optical gearbox enabled versatile multiscale high-throughput multiphoton functional imaging," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    6. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. 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.
    8. C. Nicolas & A. Ju & Y. Wu & H. Eldirdiri & S. Delcasso & Y. Couderc & C. Fornari & A. Mitra & L. Supiot & A. Vérité & M. Masson & S. Rodriguez-Rozada & D. Jacky & J. S. Wiegert & A. Beyeler, 2023. "Linking emotional valence and anxiety in a mouse insula-amygdala circuit," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    9. Eric Lowet & Krishnakanth Kondabolu & Samuel Zhou & Rebecca A. Mount & Yangyang Wang & Cara R. Ravasio & Xue Han, 2022. "Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Yihan Wang & Qian-Quan Sun, 2024. "A prefrontal motor circuit initiates persistent movement," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    11. Xu Zhan & Chao Chen & Longgang Niu & Xinran Du & Ying Lei & Rui Dan & Zhao-Wen Wang & Ping Liu, 2023. "Locomotion modulates olfactory learning through proprioception in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    12. Yide Zhang & Binglin Shen & Tong Wu & Jerry Zhao & Joseph C. Jing & Peng Wang & Kanomi Sasaki-Capela & William G. Dunphy & David Garrett & Konstantin Maslov & Weiwei Wang & Lihong V. Wang, 2022. "Ultrafast and hypersensitive phase imaging of propagating internodal current flows in myelinated axons and electromagnetic pulses in dielectrics," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Huee Ru Chong & Yadollah Ranjbar-Slamloo & Malcolm Zheng Hao Ho & Xuan Ouyang & Tsukasa Kamigaki, 2023. "Functional alterations of the prefrontal circuit underlying cognitive aging in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Paul J. Lamothe-Molina & Andreas Franzelin & Lennart Beck & Dong Li & Lea Auksutat & Tim Fieblinger & Laura Laprell & Joachim Alhbeck & Christine E. Gee & Matthias Kneussel & Andreas K. Engel & Claus , 2022. "ΔFosB accumulation in hippocampal granule cells drives cFos pattern separation during spatial learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Gaoxiang Mei & Natalia Mamaeva & Srividya Ganapathy & Peng Wang & Willem J DeGrip & Kenneth J Rothschild, 2018. "Raman spectroscopy of a near infrared absorbing proteorhodopsin: Similarities to the bacteriorhodopsin O photointermediate," PLOS ONE, Public Library of Science, vol. 13(12), pages 1-24, December.
    16. Arita Silapetere & Songhwan Hwang & Yusaku Hontani & Rodrigo G. Fernandez Lahore & Jens Balke & Francisco Velazquez Escobar & Martijn Tros & Patrick E. Konold & Rainer Matis & Roberta Croce & Peter J., 2022. "QuasAr Odyssey: the origin of fluorescence and its voltage sensitivity in microbial rhodopsins," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    17. Zhenrui Liao & Kevin C. Gonzalez & Deborah M. Li & Catalina M. Yang & Donald Holder & Natalie E. McClain & Guofeng Zhang & Stephen W. Evans & Mariya Chavarha & Jane Simko & Christopher D. Makinson & M, 2024. "Functional architecture of intracellular oscillations in hippocampal dendrites," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Changjia Cai & Johannes Friedrich & Amrita Singh & M Hossein Eybposh & Eftychios A Pnevmatikakis & Kaspar Podgorski & Andrea Giovannucci, 2021. "VolPy: Automated and scalable analysis pipelines for voltage imaging datasets," PLOS Computational Biology, Public Library of Science, vol. 17(4), pages 1-28, April.
    19. Yuki Bando & Michael Wenzel & Rafael Yuste, 2021. "Simultaneous two-photon imaging of action potentials and subthreshold inputs in vivo," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    20. Saurabh Thapliyal & Isabel Beets & Dominique A. Glauser, 2023. "Multisite regulation integrates multimodal context in sensory circuits to control persistent behavioral states in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, 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_s41467-023-37622-6. 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.