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Fast two-photon volumetric imaging of an improved voltage indicator reveals electrical activity in deeply located neurons in the awake brain

View ORCID ProfileMariya Chavarha, View ORCID ProfileVincent Villette, Ivan K. Dimov, Lagnajeet Pradhan, Stephen W. Evans, Dongqing Shi, Renzhi Yang, Simon Chamberland, Jonathan Bradley, Benjamin Mathieu, View ORCID ProfileFrancois St-Pierre, Mark J. Schnitzer, Guoqiang Bi, Katalin Toth, View ORCID ProfileJun Ding, Stéphane Dieudonné, View ORCID ProfileMichael Z. Lin
doi: https://doi.org/10.1101/445064
Mariya Chavarha
Department of Bioengineering, Stanford University, Stanford, California, USADepartment of Neurobiology, Stanford University, Stanford, California, USA
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Vincent Villette
Institut de Biologie de l′École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, Paris, France
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Ivan K. Dimov
Department of Neurobiology, Stanford University, Stanford, California, USACNC Program, Stanford University, Stanford, California, USA
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Lagnajeet Pradhan
Department of Neurobiology, Stanford University, Stanford, California, USACNC Program, Stanford University, Stanford, California, USA
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Stephen W. Evans
Department of Neurobiology, Stanford University, Stanford, California, USA
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Dongqing Shi
Department of Neurobiology, Stanford University, Stanford, California, USASchool of Life Sciences, University of Science and Technology of China, Hefei, China
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Renzhi Yang
Department of Neurosurgey, Stanford University, Stanford, California, USA
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Simon Chamberland
Department of Psychiatry and Neuroscience, Quebec Mental Health Institute, Université Laval, Québec, Canada
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Jonathan Bradley
Institut de Biologie de l′École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, Paris, France
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Benjamin Mathieu
Institut de Biologie de l′École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, Paris, France
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Francois St-Pierre
Baylor College of Medicine, Houston, Texas, USA
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Mark J. Schnitzer
CNC Program, Stanford University, Stanford, California, USA
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Guoqiang Bi
School of Life Sciences, University of Science and Technology of China, Hefei, ChinaCAS Center for Excellence in Brain Science and Intelligence Technology, Shanghai, China
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Katalin Toth
Department of Psychiatry and Neuroscience, Quebec Mental Health Institute, Université Laval, Québec, Canada
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Jun Ding
Department of Neurosurgey, Stanford University, Stanford, California, USA
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Stéphane Dieudonné
Institut de Biologie de l′École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, PSL Research University, Paris, France
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Michael Z. Lin
Department of Bioengineering, Stanford University, Stanford, California, USADepartment of Neurobiology, Stanford University, Stanford, California, USA
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ABSTRACT

Imaging of transmembrane voltage deep in brain tissue with cellular resolution has the potential to reveal information processing by neuronal circuits in living animals with minimal perturbation. Multi-photon voltage imaging in vivo, however, is currently limited by speed and sensitivity of both indicators and imaging methods. Here, we report the engineering of an improved genetically encoded voltage indicator, ASAP3, which exhibits up to 51% fluorescence responses in the physiological voltage range, sub-millisecond activation kinetics, and full responsivity under two-photon illumination. We also introduce an ultrafast local volume excitation (ULOVE) two-photon scanning method to sample ASAP3 signals in awake mice at kilohertz rates with increased stability and sensitivity. ASAP3 and ULOVE allowed continuous single-trial tracking of spikes and subthreshold events for minutes in deep locations, with subcellular resolution, and with repeated sampling over multiple days. By imaging voltage in visual cortex neurons, we found evidence for cell type-dependent subthreshold modulation by locomotion. Thus, ASAP3 and ULOVE enable continuous high-speed high-resolution imaging of electrical activity in deeply located genetically defined neurons during awake behavior.

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Posted October 17, 2018.
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Fast two-photon volumetric imaging of an improved voltage indicator reveals electrical activity in deeply located neurons in the awake brain
Mariya Chavarha, Vincent Villette, Ivan K. Dimov, Lagnajeet Pradhan, Stephen W. Evans, Dongqing Shi, Renzhi Yang, Simon Chamberland, Jonathan Bradley, Benjamin Mathieu, Francois St-Pierre, Mark J. Schnitzer, Guoqiang Bi, Katalin Toth, Jun Ding, Stéphane Dieudonné, Michael Z. Lin
bioRxiv 445064; doi: https://doi.org/10.1101/445064
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Fast two-photon volumetric imaging of an improved voltage indicator reveals electrical activity in deeply located neurons in the awake brain
Mariya Chavarha, Vincent Villette, Ivan K. Dimov, Lagnajeet Pradhan, Stephen W. Evans, Dongqing Shi, Renzhi Yang, Simon Chamberland, Jonathan Bradley, Benjamin Mathieu, Francois St-Pierre, Mark J. Schnitzer, Guoqiang Bi, Katalin Toth, Jun Ding, Stéphane Dieudonné, Michael Z. Lin
bioRxiv 445064; doi: https://doi.org/10.1101/445064

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