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Dual polarity voltage imaging reveals subthreshold dynamics and concurrent spiking patterns of multiple neuron-types

View ORCID ProfileMadhuvanthi Kannan, View ORCID ProfileGanesh Vasan, View ORCID ProfileSimon Haziza, Cheng Huang, Radek Chrapkiewicz, Junjie Luo, Jessica A. Cardin, View ORCID ProfileMark J. Schnitzer, View ORCID ProfileVincent A. Pieribone
doi: https://doi.org/10.1101/2021.10.13.463730
Madhuvanthi Kannan
1The John B. Pierce Laboratory, 290 Congress Ave, New Haven, CT 06519, USA
2Department of Cellular and Molecular Physiology, Yale University, 333 Cedar St., New Haven, CT 06520, USA
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  • ORCID record for Madhuvanthi Kannan
Ganesh Vasan
1The John B. Pierce Laboratory, 290 Congress Ave, New Haven, CT 06519, USA
2Department of Cellular and Molecular Physiology, Yale University, 333 Cedar St., New Haven, CT 06520, USA
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  • For correspondence: g.vasan@yale.edu mschnitz@stanford.edu v.pieribone@yale.edu
Simon Haziza
4James H. Clark Center, Stanford University, 318 Campus Dr., Stanford, CA 94305, USA
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Cheng Huang
4James H. Clark Center, Stanford University, 318 Campus Dr., Stanford, CA 94305, USA
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Radek Chrapkiewicz
4James H. Clark Center, Stanford University, 318 Campus Dr., Stanford, CA 94305, USA
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Junjie Luo
4James H. Clark Center, Stanford University, 318 Campus Dr., Stanford, CA 94305, USA
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Jessica A. Cardin
3Department of Neuroscience, Yale University, 333 Cedar St., New Haven, CT 06520, USA
7Kavli Institute of Neuroscience, Yale University, 333 Cedar St., New Haven, CT 06520, USA
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Mark J. Schnitzer
4James H. Clark Center, Stanford University, 318 Campus Dr., Stanford, CA 94305, USA
5CNC Program, Stanford University, Stanford, CA, USA
6Howard Hughes Medical Institute, Stanford University, Stanford, CA, USA
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  • For correspondence: g.vasan@yale.edu mschnitz@stanford.edu v.pieribone@yale.edu
Vincent A. Pieribone
1The John B. Pierce Laboratory, 290 Congress Ave, New Haven, CT 06519, USA
2Department of Cellular and Molecular Physiology, Yale University, 333 Cedar St., New Haven, CT 06520, USA
3Department of Neuroscience, Yale University, 333 Cedar St., New Haven, CT 06520, USA
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  • ORCID record for Vincent A. Pieribone
  • For correspondence: g.vasan@yale.edu mschnitz@stanford.edu v.pieribone@yale.edu
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Abstract

Genetically encoded fluorescent voltage indicators are ideally suited to reveal the millisecond-scale interactions among and between distinct, targeted cell populations. However, current indicator families lack the requisite sensitivity for in vivo multipopulation imaging. We describe high-performance green and red sensors, Ace-mNeon2 and VARNAM2, and their reverse response-polarity variants, pAce and pAceR. Our indicators enable 0.4-1 kHz voltage recordings from >50 neurons per field-of-view in awake mice and ∼30-min continuous imaging in flies. Using dual-polarity multiplexed imaging, we uncovered behavioral state-dependent interactions between distinct neocortical subclasses, as well as contributions to hippocampal field potentials from non-overlapping projection neuronal ensembles. By combining three mutually compatible indicators, we demonstrate concurrent triple-population voltage imaging. Our approach will empower investigations of the dynamic interplay between neuronal subclasses at single-spike resolution.

One Sentence Summary A new suite of voltage sensors enables simultaneous cellular-resolution activity imaging from multiple, targeted neuron-types in awake animals.

Competing Interest Statement

MK, GV and VAP are co-inventors on a patent application describing dual-polarity multiplexing; the other authors declare no competing interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 15, 2021.
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Dual polarity voltage imaging reveals subthreshold dynamics and concurrent spiking patterns of multiple neuron-types
Madhuvanthi Kannan, Ganesh Vasan, Simon Haziza, Cheng Huang, Radek Chrapkiewicz, Junjie Luo, Jessica A. Cardin, Mark J. Schnitzer, Vincent A. Pieribone
bioRxiv 2021.10.13.463730; doi: https://doi.org/10.1101/2021.10.13.463730
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Dual polarity voltage imaging reveals subthreshold dynamics and concurrent spiking patterns of multiple neuron-types
Madhuvanthi Kannan, Ganesh Vasan, Simon Haziza, Cheng Huang, Radek Chrapkiewicz, Junjie Luo, Jessica A. Cardin, Mark J. Schnitzer, Vincent A. Pieribone
bioRxiv 2021.10.13.463730; doi: https://doi.org/10.1101/2021.10.13.463730

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