Multichannel optical cochlear implants enable spectrally distinct auditory activity

When hearing fails, cochlear implants (CIs) partially restore auditory perception. Yet, poor coding of spectral information remains a bottleneck as each electrode broadly activates the auditory nerve. As light can be more conveniently confined, optical (o)CIs present a promising alternative. Here, we combined expression of the potent channelrhodopsin ChReef in spiral ganglion neurons (SGNs) and oCIs based on 5-10 green LED in gerbils. We characterized the oCI encoding of intensity and spectral information by ChReef-SGNs using recordings from the central nucleus of the inferior colliculus (ICC). ChReef aligned light sensitivity of SGNs well with the radiant fluxes provided by individual LEDs: ICC-activity had thresholds <200 nJ and reached a maximum close to that achieved with 46 dB tones. Multichannel oCIs enabled tonotopically ordered and spectrally distinct stimulation indistinguishable from acoustic stimulation for up to moderate activity levels. Some LEDs elicited >1 spectral peaks for stronger intensities. Representational Similarity Analysis and Linear Discriminant Analysis of ICC activity indicated improved channel discriminability of optical over electrical stimulation. In summary, {micro}J oCI stimulation achieves near-physiological spectral resolution. The Paper ExplainedO_ST_ABSProblemC_ST_ABSElectrical cochlear implants (eCIs) partially restore speech comprehension in most of >1 million otherwise deaf users, who still face challenges hearing in daily situations. This is primarily due to poor spectral selectivity of electrical sound encoding. Spatially more confined optogenetic activation of the auditory nerve by optical cochlear implants (oCI) promises to overcome this limitation. However, a thorough characterization of bionic coding of sound information by multichannel oCI is needed to evaluate the potential for improved hearing restoration. ResultsHere, we combine the potent channelrhodopsin ChReef and 10-channel oCI based on green LEDs in gerbils and characterize their utility for encoding of spectral and intensity information by multielectrode array recordings from the midbrain. ChReef enabled activation of the auditory pathway with nano-joule thresholds and up to high levels of midbrain activity with low {micro}J radiant energy. The cochlear spread of excitation and channel discriminability for low to medium activity levels were close to what we observed with acoustic stimulation. ImpactOur work demonstrates great potential of multichannel optogenetic stimulation for encoding sound frequency information.