Direct optogenetic activation of inner hair cells improves the efficiency and fidelity of auditory encoding

Severe hearing impairment affects approximately 5% of the global population, with a prevalence projected to increase over the coming decades. Cochlear implant devices pose a neuroprosthetic treatment option to allow sound perception and speech comprehension. However, users are limited in the spectrum of auditory information they can regain because electrical stimulation of the auditory nerve generates a broad spread of current and limits the transmission of sound frequency information. Recently, optogenetic stimulation of the cochlear nerve has emerged as a promising alternative for hearing restoration. Because light can be precisely confined in space, optogenetic stimulation of the cochlea permits to activate auditory neurons within smaller tonotopic regions, thereby improving the encoding of sound frequencies compared to electrical stimulation. However, this approach is limited in terms of dynamic range and ability to follow rapidly varying inputs, thus preventing faithful transmission of auditory information. Here, we developed an alternative approach targeting directly sensory inner hair cells with optogenetics. We demonstrate that this approach decreases the amount of light energy necessary to evoke auditory responses. Direct stimulation of hair cells increases the dynamic range of intensities encoded by neurons in subcortical auditory areas and improves the temporal fidelity of optogenetic responses. Finally, a biophysical model of the auditory system suggests that preserving the synapses between inner hair cells and auditory neurons greatly improves the encoding performance of an optical cochlear implant. Together, our results suggest that targeting sensory inner hair cells is a promising approach for hearing restoration through an optical implant.