Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics

Yoav Adam; Jeong J. Kim; Shan Lou; Yongxin Zhao; Michael E. Xie; Daan Brinks; Hao Wu; Mohammed A. Mostajo-Radji; Simon Kheifets; Vicente Parot; Selmaan Chettih; Katherine J. Williams; Benjamin Gmeiner; Samouil L. Farhi; Linda Madisen; E. Kelly Buchanan; Ian Kinsella; Ding Zhou; Liam Paninski; Christopher D. Harvey; Hongkui Zeng; Paola Arlotta; Robert E. Campbell; Adam E. Cohen

doi:10.1038/s41586-019-1166-7

Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics

Yoav Adam, Jeong J. Kim, Shan Lou, Yongxin Zhao, Michael E. Xie, Daan Brinks, Hao Wu, Mohammed A. Mostajo-Radji, Simon Kheifets, Vicente Parot, Selmaan Chettih, Katherine J. Williams, Benjamin Gmeiner, Samouil L. Farhi, Linda Madisen, E. Kelly Buchanan, Ian Kinsella, Ding Zhou, Liam Paninski, Christopher D. HarveyHongkui Zeng, Paola Arlotta, Robert E. Campbell, Adam E. Cohen^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

221 Scopus citations

Abstract

A technology that simultaneously records membrane potential from multiple neurons in behaving animals will have a transformative effect on neuroscience research^1,2. Genetically encoded voltage indicators are a promising tool for these purposes; however, these have so far been limited to single-cell recordings with a marginal signal-to-noise ratio in vivo^3–5. Here we developed improved near-infrared voltage indicators, high-speed microscopes and targeted gene expression schemes that enabled simultaneous in vivo recordings of supra- and subthreshold voltage dynamics in multiple neurons in the hippocampus of behaving mice. The reporters revealed subcellular details of back-propagating action potentials and correlations in subthreshold voltage between multiple cells. In combination with stimulation using optogenetics, the reporters revealed changes in neuronal excitability that were dependent on the behavioural state, reflecting the interplay of excitatory and inhibitory synaptic inputs. These tools open the possibility for detailed explorations of network dynamics in the context of behaviour.[Figure not available: see fulltext.]

Original language	English
Pages (from-to)	413-417
Number of pages	5
Journal	Nature
Volume	569
Issue number	7756
DOIs	https://doi.org/10.1038/s41586-019-1166-7
State	Published - 16 May 2019
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2019, The Author(s), under exclusive licence to Springer Nature Limited.

Access to Document

10.1038/s41586-019-1166-7

Cite this

Adam, Y., Kim, J. J., Lou, S., Zhao, Y., Xie, M. E., Brinks, D., Wu, H., Mostajo-Radji, M. A., Kheifets, S., Parot, V., Chettih, S., Williams, K. J., Gmeiner, B., Farhi, S. L., Madisen, L., Buchanan, E. K., Kinsella, I., Zhou, D., Paninski, L., ... Cohen, A. E. (2019). Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics. Nature, 569(7756), 413-417. https://doi.org/10.1038/s41586-019-1166-7

@article{f9c6dd7cd06d47ce81f443ad8454603b,

title = "Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics",

abstract = "A technology that simultaneously records membrane potential from multiple neurons in behaving animals will have a transformative effect on neuroscience research1,2. Genetically encoded voltage indicators are a promising tool for these purposes; however, these have so far been limited to single-cell recordings with a marginal signal-to-noise ratio in vivo3–5. Here we developed improved near-infrared voltage indicators, high-speed microscopes and targeted gene expression schemes that enabled simultaneous in vivo recordings of supra- and subthreshold voltage dynamics in multiple neurons in the hippocampus of behaving mice. The reporters revealed subcellular details of back-propagating action potentials and correlations in subthreshold voltage between multiple cells. In combination with stimulation using optogenetics, the reporters revealed changes in neuronal excitability that were dependent on the behavioural state, reflecting the interplay of excitatory and inhibitory synaptic inputs. These tools open the possibility for detailed explorations of network dynamics in the context of behaviour.[Figure not available: see fulltext.]",

author = "Yoav Adam and Kim, {Jeong J.} and Shan Lou and Yongxin Zhao and Xie, {Michael E.} and Daan Brinks and Hao Wu and Mostajo-Radji, {Mohammed A.} and Simon Kheifets and Vicente Parot and Selmaan Chettih and Williams, {Katherine J.} and Benjamin Gmeiner and Farhi, {Samouil L.} and Linda Madisen and Buchanan, {E. Kelly} and Ian Kinsella and Ding Zhou and Liam Paninski and Harvey, {Christopher D.} and Hongkui Zeng and Paola Arlotta and Campbell, {Robert E.} and Cohen, {Adam E.}",

note = "Publisher Copyright: {\textcopyright} 2019, The Author(s), under exclusive licence to Springer Nature Limited.",

year = "2019",

month = may,

day = "16",

doi = "10.1038/s41586-019-1166-7",

language = "אנגלית",

volume = "569",

pages = "413--417",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Research",

number = "7756",

}

Adam, Y, Kim, JJ, Lou, S, Zhao, Y, Xie, ME, Brinks, D, Wu, H, Mostajo-Radji, MA, Kheifets, S, Parot, V, Chettih, S, Williams, KJ, Gmeiner, B, Farhi, SL, Madisen, L, Buchanan, EK, Kinsella, I, Zhou, D, Paninski, L, Harvey, CD, Zeng, H, Arlotta, P, Campbell, RE & Cohen, AE 2019, 'Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics', Nature, vol. 569, no. 7756, pp. 413-417. https://doi.org/10.1038/s41586-019-1166-7

TY - JOUR

T1 - Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics

AU - Adam, Yoav

AU - Kim, Jeong J.

AU - Lou, Shan

AU - Zhao, Yongxin

AU - Xie, Michael E.

AU - Brinks, Daan

AU - Wu, Hao

AU - Mostajo-Radji, Mohammed A.

AU - Kheifets, Simon

AU - Parot, Vicente

AU - Chettih, Selmaan

AU - Williams, Katherine J.

AU - Gmeiner, Benjamin

AU - Farhi, Samouil L.

AU - Madisen, Linda

AU - Buchanan, E. Kelly

AU - Kinsella, Ian

AU - Zhou, Ding

AU - Paninski, Liam

AU - Harvey, Christopher D.

AU - Zeng, Hongkui

AU - Arlotta, Paola

AU - Campbell, Robert E.

AU - Cohen, Adam E.

PY - 2019/5/16

Y1 - 2019/5/16

N2 - A technology that simultaneously records membrane potential from multiple neurons in behaving animals will have a transformative effect on neuroscience research1,2. Genetically encoded voltage indicators are a promising tool for these purposes; however, these have so far been limited to single-cell recordings with a marginal signal-to-noise ratio in vivo3–5. Here we developed improved near-infrared voltage indicators, high-speed microscopes and targeted gene expression schemes that enabled simultaneous in vivo recordings of supra- and subthreshold voltage dynamics in multiple neurons in the hippocampus of behaving mice. The reporters revealed subcellular details of back-propagating action potentials and correlations in subthreshold voltage between multiple cells. In combination with stimulation using optogenetics, the reporters revealed changes in neuronal excitability that were dependent on the behavioural state, reflecting the interplay of excitatory and inhibitory synaptic inputs. These tools open the possibility for detailed explorations of network dynamics in the context of behaviour.[Figure not available: see fulltext.]

AB - A technology that simultaneously records membrane potential from multiple neurons in behaving animals will have a transformative effect on neuroscience research1,2. Genetically encoded voltage indicators are a promising tool for these purposes; however, these have so far been limited to single-cell recordings with a marginal signal-to-noise ratio in vivo3–5. Here we developed improved near-infrared voltage indicators, high-speed microscopes and targeted gene expression schemes that enabled simultaneous in vivo recordings of supra- and subthreshold voltage dynamics in multiple neurons in the hippocampus of behaving mice. The reporters revealed subcellular details of back-propagating action potentials and correlations in subthreshold voltage between multiple cells. In combination with stimulation using optogenetics, the reporters revealed changes in neuronal excitability that were dependent on the behavioural state, reflecting the interplay of excitatory and inhibitory synaptic inputs. These tools open the possibility for detailed explorations of network dynamics in the context of behaviour.[Figure not available: see fulltext.]

UR - http://www.scopus.com/inward/record.url?scp=85065234582&partnerID=8YFLogxK

U2 - 10.1038/s41586-019-1166-7

DO - 10.1038/s41586-019-1166-7

M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???

C2 - 31043747

AN - SCOPUS:85065234582

SN - 0028-0836

VL - 569

SP - 413

EP - 417

JO - Nature

JF - Nature

IS - 7756

ER -

Voltage imaging and optogenetics reveal behaviour-dependent changes in hippocampal dynamics

Abstract

Bibliographical note

Access to Document

Other files and links

Fingerprint

Cite this