Utility of red-light ultrafast optogenetic stimulation of the auditory pathway.

channelrhodopsin cochlear implant dynamic range gating spiral ganglion temporal coding

Journal

EMBO molecular medicine
ISSN: 1757-4684
Titre abrégé: EMBO Mol Med
Pays: England
ID NLM: 101487380

Informations de publication

Date de publication:
07 06 2021
Historique:
revised: 22 03 2021
received: 04 09 2020
accepted: 23 03 2021
pubmed: 8 5 2021
medline: 26 10 2021
entrez: 7 5 2021
Statut: ppublish

Résumé

Optogenetic stimulation of spiral ganglion neurons (SGNs) in the ear provides a future alternative to electrical stimulation used in current cochlear implants. Here, we employed fast and very fast variants of the red-light-activated channelrhodopsin (ChR) Chrimson (f-Chrimson and vf-Chrimson) to study their utility for optogenetic stimulation of SGNs in mice. The light requirements were higher for vf-Chrimson than for f-Chrimson, even when optimizing membrane expression of vf-Chrimson by adding potassium channel trafficking sequences. Optogenetic time and intensity coding by single putative SGNs were compared with coding of acoustic clicks. vf-Chrimson enabled putative SGNs to fire at near-physiological rates with good temporal precision up to 250 Hz of stimulation. The dynamic range of SGN spike rate coding upon optogenetic stimulation was narrower than for acoustic clicks but larger than reported for electrical stimulation. The dynamic range of spike timing, on the other hand, was more comparable for optogenetic and acoustic stimulation. In conclusion, f-Chrimson and vf-Chrimson are promising candidates for optogenetic stimulation of SGNs in auditory research and future cochlear implants.

Identifiants

pubmed: 33960685
doi: 10.15252/emmm.202013391
pmc: PMC8185542
doi:

Substances chimiques

Channelrhodopsins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13391

Informations de copyright

© 2021 The Authors. Published under the terms of the CC BY 4.0 license.

Références

Nat Commun. 2018 May 1;9(1):1750
pubmed: 29717130
Nat Protoc. 2006;1(3):1412-28
pubmed: 17406430
J Acoust Soc Am. 1988 Jul;84(1):172-8
pubmed: 3411045
J Neurophysiol. 2016 Aug 1;116(2):844-58
pubmed: 27281743
Gene Ther. 2012 Feb;19(2):169-75
pubmed: 21993174
Methods Mol Biol. 2021;2191:261-285
pubmed: 32865750
Nat Neurosci. 2017 Aug;20(8):1172-1179
pubmed: 28671695
Nat Biotechnol. 2016 Feb;34(2):204-9
pubmed: 26829320
J Acoust Soc Am. 1974 Dec;56(6):1835-47
pubmed: 4443483
J Neurophysiol. 1986 Aug;56(2):261-86
pubmed: 3760921
J Neurophysiol. 2005 Jan;93(1):557-69
pubmed: 15456804
Hear Res. 1998 Jul;121(1-2):11-28
pubmed: 9682804
Mol Ther. 2018 Aug 1;26(8):1931-1939
pubmed: 30017876
Sci Transl Med. 2020 Jul 22;12(553):
pubmed: 32718992
FEBS Lett. 2001 Mar 30;493(2-3):129-33
pubmed: 11287009
J Neurophysiol. 2013 Aug;110(3):577-86
pubmed: 23596328
Hear Res. 1990 May;45(3):191-202
pubmed: 2358413
Hear Res. 1987;25(2-3):233-48
pubmed: 3558132
Nature. 2018 May;557(7705):359-367
pubmed: 29769667
EMBO Mol Med. 2020 Apr 7;12(4):e11618
pubmed: 32227585
Curr Protoc Neurosci. 2011 Oct;Chapter 4:Unit 4.17
pubmed: 21971848
J Clin Invest. 2014 Mar;124(3):1114-29
pubmed: 24509078
J Neural Eng. 2011 Oct;8(5):056006
pubmed: 21828906
Nat Commun. 2019 Apr 29;10(1):1962
pubmed: 31036812
J Neurosci. 2009 Nov 4;29(44):13797-808
pubmed: 19889991
Ear Hear. 1999 Feb;20(1):60-74
pubmed: 10037066
Front Mol Neurosci. 2021 Mar 11;14:635897
pubmed: 33776648
Physiol Rev. 2020 Oct 1;100(4):1467-1525
pubmed: 32191560
Cell. 2010 Apr 2;141(1):154-165
pubmed: 20303157
J Acoust Soc Am. 1991 Jul;90(1):274-87
pubmed: 1652601
J Neurophysiol. 2014 Sep 1;112(5):1025-39
pubmed: 24848461
Network. 2016;27(2-3):212-236
pubmed: 27644125
Hear Res. 2016 Aug;338:32-9
pubmed: 27220483
Gene Ther. 1996 Jul;3(7):588-92
pubmed: 8818645
J Cell Sci. 2005 May 1;118(Pt 9):1935-43
pubmed: 15827083
EMBO J. 2018 Dec 14;37(24):
pubmed: 30396994
Commun Biol. 2021 Jan 27;4(1):125
pubmed: 33504896
J Acoust Soc Am. 1978 Feb;63(2):442-55
pubmed: 670542
Gene Ther. 1999 Jun;6(6):973-85
pubmed: 10455399
GMS Curr Top Otorhinolaryngol Head Neck Surg. 2018 Feb 19;16:Doc04
pubmed: 29503669
J Neurophysiol. 1969 Jul;32(4):613-36
pubmed: 5810617
J Neurophysiol. 2012 Jul;108(1):69-82
pubmed: 22457465
J Neurosci. 2018 Jun 20;38(25):5727-5738
pubmed: 29793977
Sci Transl Med. 2018 Jul 11;10(449):
pubmed: 29997248
Cold Spring Harb Perspect Med. 2019 Aug 1;9(8):
pubmed: 30323016
Audiol Neurootol. 2011;16(2):113-23
pubmed: 20639631
IEEE Trans Biomed Eng. 2017 Aug;64(8):1662-1664
pubmed: 28650803
EMBO Mol Med. 2021 Jun 7;13(6):e13391
pubmed: 33960685
J Assoc Res Otolaryngol. 2006 Sep;7(3):195-210
pubmed: 16708257

Auteurs

Burak Bali (B)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Göttingen Graduate School for Neurosciences and Molecular Biosciences, University of Göttingen, Göttingen, Germany.
Restorative Cochlear Genomics Group, Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen, Germany.

David Lopez de la Morena (D)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Göttingen Graduate School for Neurosciences and Molecular Biosciences, University of Göttingen, Göttingen, Germany.
Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen, Germany.
Auditory Neuroscience Group, Max-Planck-Institute for Experimental Medicine, Göttingen, Germany.

Artur Mittring (A)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Auditory Circuit Lab, Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.

Thomas Mager (T)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Cluster of Excellence "Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC), University of Göttingen, Göttingen, Germany.

Vladan Rankovic (V)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Restorative Cochlear Genomics Group, Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen, Germany.

Antoine Tarquin Huet (AT)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen, Germany.
Auditory Circuit Lab, Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Cluster of Excellence "Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC), University of Göttingen, Göttingen, Germany.

Tobias Moser (T)

Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen, Göttingen, Germany.
Auditory Neuroscience and Optogenetics Laboratory, German Primate Center, Göttingen, Germany.
Auditory Neuroscience Group, Max-Planck-Institute for Experimental Medicine, Göttingen, Germany.
Cluster of Excellence "Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells" (MBExC), University of Göttingen, Göttingen, Germany.

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