IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41975-3.html
   My bibliography  Save this article

Widefield imaging of rapid pan-cortical voltage dynamics with an indicator evolved for one-photon microscopy

Author

Listed:
  • Xiaoyu Lu

    (Systems, Synthetic, and Physical Biology Program, Rice University
    Department of Neuroscience, Baylor College of Medicine)

  • Yunmiao Wang

    (Neuroscience Graduate Program, Emory University
    Biology Department, Emory University)

  • Zhuohe Liu

    (Department of Electrical and Computer Engineering, Rice University
    The University of Texas MD Anderson Cancer Center)

  • Yueyang Gou

    (Department of Neuroscience, Baylor College of Medicine)

  • Dieter Jaeger

    (Biology Department, Emory University)

  • François St-Pierre

    (Systems, Synthetic, and Physical Biology Program, Rice University
    Department of Electrical and Computer Engineering, Rice University
    Department of Neuroscience, Baylor College of Medicine
    Department of Biochemistry and Molecular Biology, Baylor College of Medicine)

Abstract

Widefield imaging with genetically encoded voltage indicators (GEVIs) is a promising approach for understanding the role of large cortical networks in the neural coding of behavior. However, the limited performance of current GEVIs restricts their deployment for single-trial imaging of rapid neuronal voltage dynamics. Here, we developed a high-throughput platform to screen for GEVIs that combine fast kinetics with high brightness, sensitivity, and photostability under widefield one-photon illumination. Rounds of directed evolution produced JEDI-1P, a green-emitting fluorescent indicator with enhanced performance across all metrics. Next, we optimized a neonatal intracerebroventricular delivery method to achieve cost-effective and wide-spread JEDI-1P expression in mice. We also developed an approach to correct optical measurements from hemodynamic and motion artifacts effectively. Finally, we achieved stable brain-wide voltage imaging and successfully tracked gamma-frequency whisker and visual stimulations in awake mice in single trials, opening the door to investigating the role of high-frequency signals in brain computations.

Suggested Citation

  • Xiaoyu Lu & Yunmiao Wang & Zhuohe Liu & Yueyang Gou & Dieter Jaeger & François St-Pierre, 2023. "Widefield imaging of rapid pan-cortical voltage dynamics with an indicator evolved for one-photon microscopy," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41975-3
    DOI: 10.1038/s41467-023-41975-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41975-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41975-3?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. Nicholas A. Steinmetz & Peter Zatka-Haas & Matteo Carandini & Kenneth D. Harris, 2019. "Distributed coding of choice, action and engagement across the mouse brain," Nature, Nature, vol. 576(7786), pages 266-273, December.
    2. 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.
    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. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Evan S. Schaffer & Neeli Mishra & Matthew R. Whiteway & Wenze Li & Michelle B. Vancura & Jason Freedman & Kripa B. Patel & Venkatakaushik Voleti & Liam Paninski & Elizabeth M. C. Hillman & L. F. Abbot, 2023. "The spatial and temporal structure of neural activity across the fly brain," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    4. Kenneth W. Latimer & David J. Freedman, 2023. "Low-dimensional encoding of decisions in parietal cortex reflects long-term training history," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    5. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Masashi Hasegawa & Ziyan Huang & Ricardo Paricio-Montesinos & Jan Gründemann, 2024. "Network state changes in sensory thalamus represent learned outcomes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Jérémie Sibille & Carolin Gehr & Jonathan I. Benichov & Hymavathy Balasubramanian & Kai Lun Teh & Tatiana Lupashina & Daniela Vallentin & Jens Kremkow, 2022. "High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Gal Atlan & Noa Matosevich & Noa Peretz-Rivlin & Idit Marsh-Yvgi & Noam Zelinger & Eden Chen & Timna Kleinman & Noa Bleistein & Efrat Sheinbach & Maya Groysman & Yuval Nir & Ami Citri, 2024. "Claustrum neurons projecting to the anterior cingulate restrict engagement during sleep and behavior," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Guo, Lei & Guo, Minxin & Wu, Youxi & Xu, Guizhi, 2023. "Specific neural coding of fMRI spiking neural network based on time coding," Chaos, Solitons & Fractals, Elsevier, vol. 174(C).
    10. Frank Gelens & Juho Äijälä & Louis Roberts & Misako Komatsu & Cem Uran & Michael A. Jensen & Kai J. Miller & Robin A. A. Ince & Max Garagnani & Martin Vinck & Andres Canales-Johnson, 2024. "Distributed representations of prediction error signals across the cortical hierarchy are synergistic," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Drew C. Schreiner & Christian Cazares & Rafael Renteria & Christina M. Gremel, 2022. "Information normally considered task-irrelevant drives decision-making and affects premotor circuit recruitment," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. 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.
    13. João D. Semedo & Anna I. Jasper & Amin Zandvakili & Aravind Krishna & Amir Aschner & Christian K. Machens & Adam Kohn & Byron M. Yu, 2022. "Feedforward and feedback interactions between visual cortical areas use different population activity patterns," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Christopher M. Kim & Arseny Finkelstein & Carson C. Chow & Karel Svoboda & Ran Darshan, 2023. "Distributing task-related neural activity across a cortical network through task-independent connections," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    15. 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.
    16. Christopher F. Angeloni & Wiktor Młynarski & Eugenio Piasini & Aaron M. Williams & Katherine C. Wood & Linda Garami & Ann M. Hermundstad & Maria N. Geffen, 2023. "Dynamics of cortical contrast adaptation predict perception of signals in noise," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    17. Kotaro Ishizu & Shosuke Nishimoto & Yutaro Ueoka & Akihiro Funamizu, 2024. "Localized and global representation of prior value, sensory evidence, and choice in male mouse cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. Yina Wei & Anirban Nandi & Xiaoxuan Jia & Joshua H. Siegle & Daniel Denman & Soo Yeun Lee & Anatoly Buchin & Werner Geit & Clayton P. Mosher & Shawn Olsen & Costas A. Anastassiou, 2023. "Associations between in vitro, in vivo and in silico cell classes in mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    19. Yue Liu & Xiao-Jing Wang, 2024. "Flexible gating between subspaces in a neural network model of internally guided task switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    20. Pierre-Marie Gardères & Sébastien Gal & Charly Rousseau & Alexandre Mamane & Dan Alin Ganea & Florent Haiss, 2024. "Coexistence of state, choice, and sensory integration coding in barrel cortex LII/III," Nature Communications, Nature, vol. 15(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_s41467-023-41975-3. 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.