Abstract
Cochlear implants (CIs) electrically stimulate spiral ganglion neurons (SGNs) and partially restore hearing to half a million CI users. However, wide current spread from intracochlear electrodes limits spatial selectivity (i.e. spectral resolution) of electrical CIs. Optogenetic stimulation might become an alternative, since light can be confined in space, promising artificial sound encoding with increased spectral selectivity. Here we compare spectral selectivity of optogenetic, electric, and acoustic stimulation by multi-channel recordings in the inferior colliculus (IC) of gerbils. When projecting light onto tonotopically distinct SGNs, we observe corresponding tonotopically ordered IC activity. An activity-based comparison reveals that spectral selectivity of optogenetic stimulation is indistinguishable from acoustic stimulation for modest intensities. Moreover, optogenetic stimulation outperforms bipolar electric stimulation at medium and high intensities and monopolar electric stimulation at all intensities. In conclusion, we demonstrate better spectral selectivity of optogenetic over electric SGN stimulation, suggesting the potential for improved hearing restoration by optical CIs.
Highlights
Cochlear implants (CIs) electrically stimulate spiral ganglion neurons (SGNs) and partially restore hearing to half a million CI users
Stimulation of the auditory system using fiber-based optical CIs (oCIs) has greatly advanced in the past years: a proof of principle study employing cochlear optogenetics in transgenic mice demonstrated optical activation of the auditory pathway up to the inferior colliculus (IC), where current source density analysis indicated a smaller spread of SGN excitation for optical than for monopolar electrical stimulation[8]
We scrutinized the spectral spread of excitation for optogenetic stimulation of SGNs and compared it to physiological hearing and hearing with eCI employing monopolar stimulation, used in the majority of clinical eCIs23, as well as bipolar stimulation
Summary
Cochlear implants (CIs) electrically stimulate spiral ganglion neurons (SGNs) and partially restore hearing to half a million CI users. Optical stimulation of SGNs represents a novel approach to overcome this limitation of eCIs: Light can be better confined in space and, optical CIs (oCIs) could activate SGNs along the tonotopic axis of the cochlea with higher spatial selectivity This promises improved spectral resolution of artificial sound coding and an increased number of independent stimulation channels[7,8,9,10]. We demonstrate spatially selective optical activation of the auditory system in a tonotopic manner with a spectrally more confined SGN excitation than the one found upon monopolar and bipolar electrical stimulation This indicates increased spectral resolution of artificial sound encoding when using optogenetic instead of electrical stimulation—and suggests that oCIs might overcome the major bottleneck of eCIs
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