Membrane water for probing neuronal membrane potentials and ionic fluxes at the single cell level

M. E.P. Didier; O. B. Tarun; P. Jourdain; P. Magistretti; S. Roke

doi:10.1038/s41467-018-07713-w

Membrane water for probing neuronal membrane potentials and ionic fluxes at the single cell level

M. E.P. Didier, O. B. Tarun, P. Jourdain, P. Magistretti, S. Roke^*

^*Corresponding author for this work

Biological, Environmental Sciences and Engineering

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

28 Scopus citations

Abstract

Neurons communicate through electrochemical signaling within a complex network. These signals are composed of changes in membrane potentials and are traditionally measured with the aid of (toxic) fluorescent labels or invasive electrical probes. Here, we demonstrate an improvement in label-free second harmonic neuroimaging sensitivity by ~3 orders of magnitude using a wide-field medium repetition rate illumination. We perform a side-by-side patch-clamp and second harmonic imaging comparison to demonstrate the theoretically predicted linear correlation between whole neuron membrane potential changes and the square root of the second harmonic intensity. We assign the ion induced changes to the second harmonic intensity to changes in the orientation of membrane interfacial water, which is used to image spatiotemporal changes in the membrane potential and K⁺ ion flux. We observe a non-uniform spatial distribution and temporal activity of ion channels in mouse brain neurons.

Original language	English (US)
Article number	5287
Journal	Nature Communications
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41467-018-07713-w
State	Published - Dec 1 2018

Bibliographical note

Funding Information:
This work was supported by the Julia Jacobi Foundation and the Swiss National Foundation (grant number 200021_146884). The authors would like to thank E. Ruchti, E. Gasparetto and M. Wirth for providing the neuronal cultures, B.S. Sermet for help with the patch-clamp measurements and P. Marquet and I. Allaman for discussions.

Publisher Copyright:
© 2018, The Author(s).

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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title = "Membrane water for probing neuronal membrane potentials and ionic fluxes at the single cell level",

abstract = "Neurons communicate through electrochemical signaling within a complex network. These signals are composed of changes in membrane potentials and are traditionally measured with the aid of (toxic) fluorescent labels or invasive electrical probes. Here, we demonstrate an improvement in label-free second harmonic neuroimaging sensitivity by ~3 orders of magnitude using a wide-field medium repetition rate illumination. We perform a side-by-side patch-clamp and second harmonic imaging comparison to demonstrate the theoretically predicted linear correlation between whole neuron membrane potential changes and the square root of the second harmonic intensity. We assign the ion induced changes to the second harmonic intensity to changes in the orientation of membrane interfacial water, which is used to image spatiotemporal changes in the membrane potential and K+ ion flux. We observe a non-uniform spatial distribution and temporal activity of ion channels in mouse brain neurons.",

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AU - Magistretti, P.

AU - Roke, S.

N1 - Funding Information: This work was supported by the Julia Jacobi Foundation and the Swiss National Foundation (grant number 200021_146884). The authors would like to thank E. Ruchti, E. Gasparetto and M. Wirth for providing the neuronal cultures, B.S. Sermet for help with the patch-clamp measurements and P. Marquet and I. Allaman for discussions. Publisher Copyright: © 2018, The Author(s).

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N2 - Neurons communicate through electrochemical signaling within a complex network. These signals are composed of changes in membrane potentials and are traditionally measured with the aid of (toxic) fluorescent labels or invasive electrical probes. Here, we demonstrate an improvement in label-free second harmonic neuroimaging sensitivity by ~3 orders of magnitude using a wide-field medium repetition rate illumination. We perform a side-by-side patch-clamp and second harmonic imaging comparison to demonstrate the theoretically predicted linear correlation between whole neuron membrane potential changes and the square root of the second harmonic intensity. We assign the ion induced changes to the second harmonic intensity to changes in the orientation of membrane interfacial water, which is used to image spatiotemporal changes in the membrane potential and K+ ion flux. We observe a non-uniform spatial distribution and temporal activity of ion channels in mouse brain neurons.

AB - Neurons communicate through electrochemical signaling within a complex network. These signals are composed of changes in membrane potentials and are traditionally measured with the aid of (toxic) fluorescent labels or invasive electrical probes. Here, we demonstrate an improvement in label-free second harmonic neuroimaging sensitivity by ~3 orders of magnitude using a wide-field medium repetition rate illumination. We perform a side-by-side patch-clamp and second harmonic imaging comparison to demonstrate the theoretically predicted linear correlation between whole neuron membrane potential changes and the square root of the second harmonic intensity. We assign the ion induced changes to the second harmonic intensity to changes in the orientation of membrane interfacial water, which is used to image spatiotemporal changes in the membrane potential and K+ ion flux. We observe a non-uniform spatial distribution and temporal activity of ion channels in mouse brain neurons.

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Membrane water for probing neuronal membrane potentials and ionic fluxes at the single cell level

Abstract

Bibliographical note

ASJC Scopus subject areas

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