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Population imaging of neural activity in awake behaving mice

Author

Listed:
  • Kiryl D. Piatkevich

    (MIT
    MIT McGovern Institute for Brain Research, MIT)

  • Seth Bensussen

    (Boston University)

  • Hua-an Tseng

    (Boston University)

  • Sanaya N. Shroff

    (Boston University)

  • Violeta Gisselle Lopez-Huerta

    (Broad Institute of MIT and Harvard)

  • Demian Park

    (MIT
    MIT McGovern Institute for Brain Research, MIT)

  • Erica E. Jung

    (MIT
    University of Illinois)

  • Or A. Shemesh

    (MIT
    MIT McGovern Institute for Brain Research, MIT)

  • Christoph Straub

    (Harvard Medical School)

  • Howard J. Gritton

    (Boston University)

  • Michael F. Romano

    (Boston University)

  • Emma Costa

    (MIT)

  • Bernardo L. Sabatini

    (Harvard Medical School)

  • Zhanyan Fu

    (Broad Institute of MIT and Harvard)

  • Edward S. Boyden

    (MIT
    MIT McGovern Institute for Brain Research, MIT
    Department of Biological Engineering, MIT
    MIT Center for Neurobiological Engineering, MIT)

  • Xue Han

    (Boston University)

Abstract

A longstanding goal in neuroscience has been to image membrane voltage across a population of individual neurons in an awake, behaving mammal. Here we describe a genetically encoded fluorescent voltage indicator, SomArchon, which exhibits millisecond response times and is compatible with optogenetic control, and which increases the sensitivity, signal-to-noise ratio, and number of neurons observable several-fold over previously published fully genetically encoded reagents1–8. Under conventional one-photon microscopy, SomArchon enables the routine population analysis of around 13 neurons at once, in multiple brain regions (cortex, hippocampus, and striatum) of head-fixed, awake, behaving mice. Using SomArchon, we detected both positive and negative responses of striatal neurons during movement, as previously reported by electrophysiology but not easily detected using modern calcium imaging techniques9–11, highlighting the power of voltage imaging to reveal bidirectional modulation. We also examined how spikes relate to the subthreshold theta oscillations of individual hippocampal neurons, with SomArchon showing that the spikes of individual neurons are more phase-locked to their own subthreshold theta oscillations than to local field potential theta oscillations. Thus, SomArchon reports both spikes and subthreshold voltage dynamics in awake, behaving mice.

Suggested Citation

  • Kiryl D. Piatkevich & Seth Bensussen & Hua-an Tseng & Sanaya N. Shroff & Violeta Gisselle Lopez-Huerta & Demian Park & Erica E. Jung & Or A. Shemesh & Christoph Straub & Howard J. Gritton & Michael F., 2019. "Population imaging of neural activity in awake behaving mice," Nature, Nature, vol. 574(7778), pages 413-417, October.
  • Handle: RePEc:nat:nature:v:574:y:2019:i:7778:d:10.1038_s41586-019-1641-1
    DOI: 10.1038/s41586-019-1641-1
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    Cited by:

    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. Sanaya N. Shroff & Eric Lowet & Sudiksha Sridhar & Howard J. Gritton & Mohammed Abumuaileq & Hua-An Tseng & Cyrus Cheung & Samuel L. Zhou & Krishnakanth Kondabolu & Xue Han, 2023. "Striatal cholinergic interneuron membrane voltage tracks locomotor rhythms in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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