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Population imaging of neural activity in awake behaving mice in multiple brain regions

Kiryl D. Piatkevich, Seth Bensussen, Hua-an Tseng, View ORCID ProfileSanaya N. Shroff, Violeta Gisselle Lopez-Huerta, Demian Park, Erica E. Jung, Or A. Shemesh, Christoph Straub, Howard J. Gritton, Michael F. Romano, Emma Costa, Bernardo L. Sabatini, Zhanyan Fu, Edward S. Boyden, Xue Han
doi: https://doi.org/10.1101/616094
Kiryl D. Piatkevich
1Media Lab, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
2MIT McGovern Institute for Brain Research, MIT, Cambridge, MA, USA
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Seth Bensussen
3Department of Biomedical Engineering, Boston University, Boston, MA, USA
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Hua-an Tseng
3Department of Biomedical Engineering, Boston University, Boston, MA, USA
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Sanaya N. Shroff
3Department of Biomedical Engineering, Boston University, Boston, MA, USA
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  • ORCID record for Sanaya N. Shroff
Violeta Gisselle Lopez-Huerta
4Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, USA
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Demian Park
1Media Lab, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
2MIT McGovern Institute for Brain Research, MIT, Cambridge, MA, USA
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Erica E. Jung
1Media Lab, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
5Department of Mechanical and Industrial Engineering, University of Illinois, Chicago, USA
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Or A. Shemesh
1Media Lab, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
2MIT McGovern Institute for Brain Research, MIT, Cambridge, MA, USA
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Christoph Straub
6Howard Hughes Medical Institute, Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Howard J. Gritton
3Department of Biomedical Engineering, Boston University, Boston, MA, USA
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Michael F. Romano
3Department of Biomedical Engineering, Boston University, Boston, MA, USA
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Emma Costa
1Media Lab, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
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Bernardo L. Sabatini
6Howard Hughes Medical Institute, Department of Neurobiology, Harvard Medical School, Boston, MA, USA
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Zhanyan Fu
4Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, USA
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Edward S. Boyden
1Media Lab, Massachusetts Institute of Technology (MIT), Cambridge, MA, USA
2MIT McGovern Institute for Brain Research, MIT, Cambridge, MA, USA
7Department of Biological Engineering, MIT, Cambridge, MA, USA
8MIT Center for Neurobiological Engineering, MIT, Cambridge, MA, USA
9Department of Brain and Cognitive Sciences, MIT, Cambridge, MA, USA
10Koch Institute, MIT, Cambridge, MA, USA
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  • For correspondence: xuehan@bu.edu esb@media.mit.edu
Xue Han
3Department of Biomedical Engineering, Boston University, Boston, MA, USA
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  • For correspondence: xuehan@bu.edu esb@media.mit.edu
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Abstract

A longstanding goal in neuroscience has been to image membrane voltage, with high temporal precision and sensitivity, in awake behaving mammals. Here, we report a genetically encoded voltage indicator, SomArchon, which exhibits millisecond response times and compatibility with optogenetic control, and which increases the sensitivity, signal-to-noise ratio, and number of neurons observable, by manyfold over previous reagents. SomArchon only requires conventional one-photon microscopy to achieve these high performance characteristics. These improvements enable population analysis of neural activity, both at the subthreshold and spiking levels, in multiple brain regions – cortex, hippocampus, and striatum – of awake behaving mice. Using SomArchon, we detect both positive and negative responses of striatal neurons during movement, highlighting the power of voltage imaging to reveal bidirectional modulation. We also examine how the intracellular subthreshold theta oscillations of hippocampal neurons govern spike output, finding that nearby cells can exhibit highly correlated subthreshold activities, even as they generate highly divergent spiking patterns.

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Posted April 23, 2019.
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Population imaging of neural activity in awake behaving mice in multiple brain regions
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. Romano, Emma Costa, Bernardo L. Sabatini, Zhanyan Fu, Edward S. Boyden, Xue Han
bioRxiv 616094; doi: https://doi.org/10.1101/616094
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Population imaging of neural activity in awake behaving mice in multiple brain regions
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. Romano, Emma Costa, Bernardo L. Sabatini, Zhanyan Fu, Edward S. Boyden, Xue Han
bioRxiv 616094; doi: https://doi.org/10.1101/616094

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