Hearing the light: how artificial hearing could become more natural

In a recently published study, scientists led by Prof. Tobias Moser, Director of the Institute for Auditory Neuroscience at the University Medical Center Göttingen (UMG) and Head of the Auditory Neuroscience and Optogenetics research group at the German Primate Center – Leibniz Institute for Primate Research (DPZ), have characterized the spectral resolution of natural and artificial hearing.

In Mongolian gerbils, they compared optogenetic excitation of the auditory nerve – a technique which was recently developed in Göttingen – with acoustic hearing and with clinically used electrical stimulation of the auditory nerve.

To stimulate the auditory nerve optically, light-sensitive ion channels were introduced into the nerve cells of the inner ear using viral gene transfer. By studying neuronal activity in the midbrain, the spectral resolution of acoustic, optical and electrical hearing was compared.

The results demonstrate that the artificial excitation of the auditory pathway by light allows a much higher spectral resolution than the excitation by electric current. At low levels of activity in the midbrain, the spectral resolution was even as good as that of acoustic hearing.

These results spur hope that future optical cochlear implants will improve the ability of hearing impaired to hear more naturally, improve speech understanding in noise and music perception.

Original publication:
Dieter A, Duque-Afonso CJ, Rankovic V, Jeschke M, Moser T (2019): Near physiological spectral selectivity of cochlear optogenetics. Nature Communications (doi: 10.1038/s41467-019-09980-7).

BACKGROUND

Hearing is more than just the perception of acoustic signals from our surroundings which facilitate our daily navigation in everyday life: it forms the basis for communication and thus enables us to exchange information with our fellow human beings and actively participate in social life. For many of the approximately 460 million people affected worldwide, a hearing impairment or even deafness means not only the inability to perceive acoustic signals, but also social isolation and the resulting impairment of quality of life. Hearing impairment is often caused by the loss of hair cells in the cochlea of the inner ear, which in normal hearing people convert the sound waves of acoustic signals into electrical signals that are then sent to the brain via the auditory nerve.

Up to today, hearing prostheses, so-called cochlear implants (CI), are used to restore hearing in people with severe hearing loss or deafness. These CIs are inserted into the cochlea and stimulate the auditory nerve using electrical current. Cochlear implants provide more than 500,000 patients worldwide with an artificial sense of hearing, which in the majority of cases enables open speech understanding. However, electrical CIs are limited in the precise transmission of fine gradations of pitch (frequency). For CI users, this means e.g. difficulties in speech perception in environments with background noise and in recognizing melodies. The limited spectral resolution of today's cochlear implants is caused by the relatively wide spread of electrical current in the cochlea. This activates large sections of the auditory nerve at the same time, hampering the representation of different pitches by artificial hearing. The problem can nicely be illustrated by a piano: “While natural hearing can follow pressing individual keys, the sound perception by means of a cochlear implant is more comparable to simultaneously pressing many piano keys. In order to restore more natural hearing, it has to be possible to distinguish between individual pitches,” explains Tobias Moser. This could be achieved by stimulating the auditory nerve with light: “Since light can be focused better than electric current, it allows more precise stimulation of the auditory nerve.” Together with his Göttingen team and cooperation partners, Moser is pursuing the development of optical cochlear implants. Since the auditory nerve is not light-sensitive, genetically encoded light sensors have to be inserted into the neurons of the auditory nerve. This approach, known as optogenetics, was developed recently in deafened rodents whose auditory pathway was subsequently stimulated by light to restore hearing. However, the question of spectral resolution remained largely unaddressed.

In their latest study, the researchers around Professor Moser have now characterized the spectral resolution of the optogenetic excitation of the auditory nerve and compared it to the frequency resolution of electrical and acoustic stimulation. While the inner ear of the Mongolian gerbils was stimulated optically, electrically, or acoustically, the researchers recorded neuronal activity in the auditory midbrain. The spectral resolution of the different excitation modes was determined by an activity-based analysis of the excitation width. The results show that the frequency resolution of artificial hearing can be significantly improved by optical compared to electrical stimulation. At low and moderate levels of activity, the frequency resolution of optogenetic excitation was indistinguishable from the resolution of acoustic stimulation. “Our results demonstrate for the first time that the spectral resolution of optogenetic stimulation of the auditory nerve is higher than the electrical stimulation used clinically,” says Alexander Dieter, PhD student at the Institute of Auditory Neuroscience and first author of the study: “This lets us hope that the restoration of hearing with a future optical cochlear implant will enable patients to hear more naturally.”

Before optogenetic hearing restoration can be tested in clinical trials on patients, how-ever, many more studies need to be conducted. “A logical next step is to extend single-channel stimulation, as in the current study, to multi-channel stimulation using, for example, microLED arrays,” says Marcus Jeschke, head of a junior research group at the DPZ and one of the senior authors of the study. “We hope to use these to investigate whether the activations of LEDs located close to each other can be discriminated and how and whether the activations of the individual LEDs interact,” continues Jeschke. “If future experiments in marmoset monkeys confirm our results, and the biosafety of our technology can be demonstrated, we have great hope that optical cochlear implants will also work in humans.”

The scientists are still a long way from their goal of an improved cochlear implant for the hearing impaired, but the demonstration of improved frequency resolution in the rodent model is an important milestone on this path. Preclinical research was supported by the “OptoHear” project of the European Research Council.

FIGURE: Spread of neural activity in the auditory midbrain for acoustic (top), optical (mid) and electrical (bottom) stimulation of different strength. Activity (from low: blue to strong: yellow) upon different stimulation levels (horizontal axis) spreads little (area covered along the vertical axis) for acoustic and optical stimulation: high spectral resolution. In contrast, activity spreads massively for electrical stimulation: low spectral resolution. Figure by Alexander Dieter, Institute for Auditory Neuroscience/umg

FURTHER INFORMATIONEN:
University Medical Center Göttingen
Prof. Dr. Tobias Moser
Institute for Auditory Neuroscience and InnerEarLab
Telefon +49 (0)551 / 39-63070; Email: tmoser@gwdg.de
www.auditory-neuroscience.uni-goettingen.de
http://www.innerearlab.uni-goettingen.de/
http://www.auditory-neuroscience.uni-goettingen.de/OptoHear.html
https://www.dpz.eu/de/abteilung/auditorische-neurowissenschaften-und-optogenetik…

University Medical Center Göttingen
Prof. Dr. Tobias Moser
Institute for Auditory Neuroscience and InnerEarLab
Telefon +49 (0)551 / 39-63070; Email: tmoser@gwdg.de

www.auditory-neuroscience.uni-goettingen.de
http://www.innerearlab.uni-goettingen.de/
http://www.auditory-neuroscience.uni-goettingen.de/OptoHear.html
https://www.dpz.eu/de/abteilung/auditorische-neurowissenschaften-und-optogenetik…

Dieter A, Duque-Afonso CJ, Rankovic V, Jeschke M, Moser T (2019): Near physiological spectral selectivity of cochlear optogenetics. Nature Communications (doi: 10.1038/s41467-019-09980-7).