Albrecht, N.; Koert, E.; Vavakou, A.; Roos, L.; Jablonski, L.; Marcoleta, J. P.; Cardona Audi, J.; Alfken, J.; Aakhte, M.; Klein, E.; Salditt, T.; Huisken, J.; Ruther, P.; Mager, T.; Kusch, K.; Moser, T.

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, J oCI stimulation achieves near-physiological spectral resolution.