Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity

Abstract

Mechanosensation - by which mechanical stimuli are converted into a neuronal signal - is the basis for the sensory systems of hearing, balance, and touch. Mechanosensation is unmatched in speed and its diverse range of sensitivities, reaching its highest temporal limits with the sense of hearing; however, hair cells (HCs) and the auditory nerve (AN) serve as obligatory bottlenecks for sounds to engage the brain. Like other sensory neurons, auditory neurons use the canonical pathway for neurotransmission and millisecond-duration action potentials (APs). How the auditory system utilizes the relatively slow transmission mechanisms to achieve ultrafast speed, and high audio-frequency hearing remains an enigma. Here, we address this paradox and report that the mouse, and chinchilla, AN are mechanically sensitive, and minute mechanical displacement profoundly affects its response properties. Sound-mimicking sinusoidal mechanical and electrical current stimuli affect phase-locked responses. In a phase-dependent manner, the two stimuli can also evoke suppressive responses. We propose that mechanical sensitivity interacts with synaptic responses to shape responses in the AN, including frequency tuning and temporal phase-locking. Combining neurotransmission and mechanical sensation to control spike patterns gives the mammalian AN a secondary receptor role, an emerging theme in primary neuronal functions.

Demyelination and Na+Channel Redistribution Underlie Auditory and Vestibular Dysfunction in PMP22-Null Mice

“…Among the essentials for speed is nonquantal neurotransmission in the calyceal synapse between vestibular HCs and first-order neurons ( Eatock, 2018 ). A recently identified phenomenon wherein primary auditory neurons are directly, mechanically sensitive at the non-myelinated synaptic terminals may also shape the speed of auditory temporal coding ( Perez-Flores et al, 2022 ). The peripheral dendrites of the eighth nerve, which subserve the sound–balance–brain interphase, are furnished with compact myelin at the internodes to reduce membrane capacitance and facilitate AP speed propagation.…”

The Current State of Proteomics and Metabolomics for Inner Ear Health and Disease

“…Hearing and balance function is governed by mechanosensation—mechanical sounds and vibrations in the environment, which are the converted in the ear into all-or-none electrical signals, like binary code, which are sent to the brain for higher-order processing and perception or response. Mechanosensation relies on a well-controlled homeostatic environment involving hair cells, afferent neurons, supporting cells, and inner ear fluids containing potassium and sodium [ 6 ]. When the microenvironment of the inner ear changes, such as due to pathology, dysfunction of the sensory cells follows, resulting in debilitating hearing impairment and vestibular system disorders such as dizziness and vertigo.…”