Spatially precise activation of the mouse cochlea with a multi-channel hybrid cochlear implant

Abstract Objective. Cochlear implants are among the few clinical interventions for people with severe or profound hearing loss. However, current spread during monopolar electrical stimulation results in poor spectral resolution, prompting the exploration of optical stimulation as an alternative approach. Enabled by introducing light-sensitive ion channels into auditory neurons (optogenetics), optical stimulation has been shown to activate a more discrete neural area with minimal overlap between each frequency channel during simultaneous stimulation. However, the utility of optogenetic approaches is uncertain due to the low fidelity of responses to light and high-power requirements compared to electrical stimulation. Approach. Hybrid stimulation, combining sub-threshold electrical and optical pulses, has been shown to improve fidelity and use less light, but the impact on spread of activation and channel summation using a translatable, multi-channel hybrid implant is unknown. This study examined these factors during single channel and simultaneous multi-channel hybrid stimulation in transgenic mice expressing the ChR2/H134R opsin. Acutely deafened mice were implanted with a hybrid cochlear array containing alternating light emitting diodes and platinum electrode rings. Spiking activity in the inferior colliculus was recorded during electrical-only or hybrid stimulation in which optical and electrical stimuli were both at sub-threshold intensities. Thresholds, spread of activation, and threshold shifts during simultaneous hybrid stimulation were compared to electrical-only stimulation. Main results. The electrical current required to reach activation threshold during hybrid stimulation was reduced by 7.3 dB compared to electrical-only stimulation (p<0.001). The activation width measured at two levels of discrimination above threshold and channel summation during simultaneous hybrid stimulation were significantly lower compared to electrical-only stimulation (p<0.05), but there was no spatial advantage of hybrid stimulation at higher electrical stimulation levels. Significance. Reduced channel interaction would facilitate multi-channel simultaneous stimulation, thereby enhancing the perception of temporal fine structure which is crucial for music and speech in noise.