Dual-polarity voltage imaging of the concurrent dynamics of multiple neuron types.

Publisher: American Association for the Advancement of Science Country of Publication: United States NLM ID: 0404511 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1095-9203 (Electronic) Linking ISSN: 00368075 NLM ISO Abbreviation: Science Subsets: MEDLINE

Publication: : Washington, DC : American Association for the Advancement of Science
Original Publication: New York, N.Y. : [s.n.] 1880-

Action Potentials*/physiology ; Hippocampus*/cytology ; Hippocampus*/physiology ; Neurons*/classification ; Neurons*/physiology ; Molecular Imaging*/methods ; Visual Cortex*/cytology ; Visual Cortex*/physiology; Animals ; Mice ; Interneurons/physiology ; Vasoactive Intestinal Peptide/metabolism ; Rhodopsin/chemistry ; Rhodopsin/genetics ; Luminescent Proteins/chemistry ; Luminescent Proteins/genetics ; Fluorescence ; Luminescent Measurements

Genetically encoded fluorescent voltage indicators are ideally suited to reveal the millisecond-scale interactions among and between targeted cell populations. However, current indicators lack the requisite sensitivity for in vivo multipopulation imaging. We describe next-generation green and red voltage sensors, Ace-mNeon2 and VARNAM2, and their reverse response-polarity variants pAce and pAceR. Our indicators enable 0.4- to 1-kilohertz voltage recordings from >50 spiking neurons per field of view in awake mice and ~30-minute continuous imaging in flies. Using dual-polarity multiplexed imaging, we uncovered brain state-dependent antagonism between neocortical somatostatin-expressing (SST ⁺ ) and vasoactive intestinal peptide-expressing (VIP ⁺ ) interneurons and contributions to hippocampal field potentials from cell ensembles with distinct axonal projections. By combining three mutually compatible indicators, we performed simultaneous triple-population imaging. These approaches will empower investigations of the dynamic interplay between neuronal subclasses at single-spike resolution.

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P30 EY026878 United States EY NEI NIH HHS; U01 NS103517 United States NS NINDS NIH HHS; UF1 NS107610 United States NS NINDS NIH HHS; U19 MH114830 United States MH NIMH NIH HHS; U19 NS104590 United States NS NINDS NIH HHS; U01 NS120822 United States NS NINDS NIH HHS

37221-79-7 (Vasoactive Intestinal Peptide)
9009-81-8 (Rhodopsin)
0 (Luminescent Proteins)

Date Created: 20221115 Date Completed: 20221123 Latest Revision: 20230601

20240829

PMC9703638

10.1126/science.abm8797

36378956