Population imaging of neural activity in awake behaving mice

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 () and Xue Han ()
Additional contact information
Kiryl D. Piatkevich: 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
Erica E. Jung: MIT
Or A. Shemesh: 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
Xue Han: Boston University

Nature, 2019, vol. 574, issue 7778, 413-417

Abstract: 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.

Date: 2019
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DOI: 10.1038/s41586-019-1641-1

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