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Infrared light excites cells by changing their electrical capacitance

Shapiro, Mikhail G. and Homma, Kazuaki and Villarreal, Sebastian and Richter, Claus-Peter and Bezanilla, Francisco (2012) Infrared light excites cells by changing their electrical capacitance. Nature Communications, 3 . Art. No. 736. ISSN 2041-1723. PMCID PMC3316879; PMC5684604. https://resolver.caltech.edu/CaltechAUTHORS:20140423-134017519

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Abstract

Optical stimulation has enabled important advances in the study of brain function and other biological processes, and holds promise for medical applications ranging from hearing restoration to cardiac pace making. In particular, pulsed laser stimulation using infrared wavelengths >1.5 μm has therapeutic potential based on its ability to directly stimulate nerves and muscles without any genetic or chemical pre-treatment. However, the mechanism of infrared stimulation has been a mystery, hindering its path to the clinic. Here we show that infrared light excites cells through a novel, highly general electrostatic mechanism. Infrared pulses are absorbed by water, producing a rapid local increase in temperature. This heating reversibly alters the electrical capacitance of the plasma membrane, depolarizing the target cell. This mechanism is fully reversible and requires only the most basic properties of cell membranes. Our findings underscore the generality of pulsed infrared stimulation and its medical potential.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/ncomms1742DOIArticle
https://doi.org/10.1038/ncomms16148DOICorrigendum
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3316879PubMed CentralArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5684604PubMed CentralCorrigendum
ORCID:
AuthorORCID
Shapiro, Mikhail G.0000-0002-0291-4215
Additional Information:© 2012 Macmillan Publishers Limited. This work is licensed under a Creative Commons Attribution-NonCommercial-Share Alike 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/. Received 16 Nov 2011; Accepted 9 Feb 2012; Published 13 Mar 2012. We thank Brian Salzberg, Stuart McLaughlin and Robert Eisenberg for helpful discussions. We thank Lockheed Martin Aculight for providing the laser. Funding was provided by the NIH: GM030376 (F.B.) and DC011481-01A1 (C.-P.R.). Author contributions: M.G.S. and K.H. performed experiments with oocytes. S.V., M.G.S., F.B. and K.H. performed experiments with artificial bilayers. K.H. performed experiments with HEK cells. M.G.S., F.B., S.V. and K.H. implemented the models. M.G.S., S.V., K.H., C.-P.R. and F.B. analysed the data. M.G.S. wrote the manuscript with input from all authors. M.G.S., F.B. and S.V. provided analytical tools. M.G.S., C.-P.R. and F.B. initiated the study.
Errata:We have been alerted that the theoretical explanation proposed in the subheading ‘Capacitive effect is consistent with classical theory’ of the Results section, to explain the molecular events underlying the experimentally determined increase in cell membrane electrical capacitance by infrared light excitation, is not valid. This has been attributed to an error in the assignment of the sign convention of the transmembrane charge model used in the proposed theoretical explanation. This error does not invalidate the experimental findings and main conclusion of the work, namely that membrane capacitance changes underlie infrared light-induced electrical currents and action potentials. We thank Plaksin et al. for bringing this to our attention and direct readers to the Correspondence and our Reply, which details the exact nature of the error and includes an alternative explanation for the molecular mechanisms causing this experimental effect.
Funders:
Funding AgencyGrant Number
NIHGM030376
NIHDC011481-01A1
PubMed Central ID:PMC3316879; PMC5684604
Record Number:CaltechAUTHORS:20140423-134017519
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20140423-134017519
Official Citation:Shapiro, M.G. et al. Infrared light excites cells by changing their electrical capacitance. Nat. Commun. 3:736 doi: 10.1038/ncomms1742 (2012)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:45157
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Apr 2014 21:47
Last Modified:22 Nov 2019 20:37

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