Optogenetic stimulation of the auditory pathway
Victor H. Hernandez, … , Nicola Strenzke, Tobias Moser
Victor H. Hernandez, … , Nicola Strenzke, Tobias Moser
Published March 3, 2014; First published February 10, 2014
Citation Information: J Clin Invest. 2014;124(3):1114-1129. https://doi.org/10.1172/JCI69050.
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Technical Advance Otology

Optogenetic stimulation of the auditory pathway

Abstract

Auditory prostheses can partially restore speech comprehension when hearing fails. Sound coding with current prostheses is based on electrical stimulation of auditory neurons and has limited frequency resolution due to broad current spread within the cochlea. In contrast, optical stimulation can be spatially confined, which may improve frequency resolution. Here, we used animal models to characterize optogenetic stimulation, which is the optical stimulation of neurons genetically engineered to express the light-gated ion channel channelrhodopsin-2 (ChR2). Optogenetic stimulation of spiral ganglion neurons (SGNs) activated the auditory pathway, as demonstrated by recordings of single neuron and neuronal population responses. Furthermore, optogenetic stimulation of SGNs restored auditory activity in deaf mice. Approximation of the spatial spread of cochlear excitation by recording local field potentials (LFPs) in the inferior colliculus in response to suprathreshold optical, acoustic, and electrical stimuli indicated that optogenetic stimulation achieves better frequency resolution than monopolar electrical stimulation. Virus-mediated expression of a ChR2 variant with greater light sensitivity in SGNs reduced the amount of light required for responses and allowed neuronal spiking following stimulation up to 60 Hz. Our study demonstrates a strategy for optogenetic stimulation of the auditory pathway in rodents and lays the groundwork for future applications of cochlear optogenetics in auditory research and prosthetics.

Authors

Victor H. Hernandez, Anna Gehrt, Kirsten Reuter, Zhizi Jing, Marcus Jeschke, Alejandro Mendoza Schulz, Gerhard Hoch, Matthias Bartels, Gerhard Vogt, Carolyn W. Garnham, Hiromu Yawo, Yugo Fukazawa, George J. Augustine, Ernst Bamberg, Sebastian Kügler, Tim Salditt, Livia de Hoz, Nicola Strenzke, Tobias Moser

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Figure 3

Microelectrode recordings from individual neurons of the auditory pathway reveal activation by cochlear optogenetics.

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Microelectrode recordings from individual neurons of the auditory pathwa...
(A) Relatively short latencies and remarkably high reliability and temporal precision of single-neuron spiking near the internal auditory canal, presumably representing SGNs in response to intracochlear laser light stimulation. Simultaneously recorded oABRs are shown above the associated single-neuron traces. Bottom panel: poststimulus time histograms of several neurons, distinguished by grayscale values. (B) Single neuron responses encountered within the posterior part of the cochlear nucleus, showing slightly longer latencies, lower reliability, and increased jitter, likely representing principal neurons. Upper panels: average corresponding oABR and individual trials with responses of a single neuron. Bottom panel: PSTH of putative principal neurons of the cochlear nucleus. PSTH, peristimulus time histrogram.