Specific Influences of Early Acoustic Environments on Cochlear Hair Cells in Postnatal Mice

Abstract

The auditory function develops and matures after birth in many mammalian species. After hearing onset, environmental sounds exert profound and long-term effects on auditory functions. However, the effects of the acoustic environment on the functional development of the peripheral auditory system, especially the cochlear sensory hair cells, are still unclear. In the present study, we exposed mouse pups to frequency-enriched acoustic environments in postnatal days 0–14. The results indicated that the acoustic environment significantly decreased the threshold of the auditory brainstem response in a frequency-specific manner. Compared with controls, no difference was found in the number and alignment of inner and outer hair cells or in the length of hair bundles after acoustic overstimulation. The expression and function of prestin, the motor protein of outer hair cells (OHCs), were specifically increased in OHCs activated by acoustic stimulation at postnatal days 7–11. We analyzed the postnatal maturation of ribbon synapses in the hair cell areas. After acoustic stimulation, the number of ribbon synapses was closer to the mature stage than to the controls. Taken together, these data indicate that early acoustic exposure could promote the functional maturation of cochlear hair cells and the development of hearing.

Generating inner ear organoids containing putative cochlear hair cells from human pluripotent stem cells

“…For iPSC-derived cardiomyocytes, mechanical and or electrophysiological stimulation enhances their structural maturity in vitro 53 so it is conceivable that cochlear hair cells developing within otic organoids may require acoustic stimulation to become fully functional. This is consistent with the functional maturation of cochlear hair cells and the development of hearing in neonatal mice 54 , however to improve the utility of our inner ear organoid culture to the point where we can investigate the possible contribution of acoustic stimulation, we need to manipulate additional signalling molecules that could amplify the otic induction process. This could focus on various FGFs or retinoic acid (known to contribute to the control of location-specific aspects of hair cell phenotypes) 55 , 56 but a more tractable approach might be to extend the development of fluorescent reporter systems analogous to the ATOH-GFP cell line developed by Koehler et al 19…”

Cross-Talk of Low-Level Sensory and High-Level Cognitive Processing: Development, Mechanisms, and Relevance for Cross-Modal Abilities of the Brain

“…Auditory reflexes in pups were accelerated when the mothers were reared in an enriched environment during gestation. Moreover, exposure to frequencyenriched acoustic environments during the first 14 days after birth significantly decreased the threshold of auditory responses in a frequency-specific manner (Chang et al, 2018). Rearing in a disturbed acoustic environment impairs the development of the auditory system (Zhang et al, 2002;Chang and Merzenich, 2003;Nakahara et al, 2004;Speechley et al, 2007).…”

Earliest experience of a relatively rare sound but not a frequent sound causes long term changes in the adult auditory cortex

“…We show that the mouse auditory pathway, ACX and IC, is driven by sounds with ear canals closed as early as P7 and down to intensities of 60 dB SPL. The above result is perhaps not surprising as auditory brainstem responses (ABR) in mice have been shown before ECO 23 and that there are long term changes in prestin expression in mice when exposed to loud sounds at these early ages (P6-P11). Studies based on sound-evoked and spontaneous activity show that the central auditory pathway is functional before ECO.…”

“…Low threshold hearing onset coincides with ECO 5,22 in the mouse, with outer hair cell (OHC) based sensitivity allowing detection of near 0 dB SPL sounds. The developing auditory pathway is functional before ECO 23 as known from ACX sound driven responses obtained by surgically opening the ear canal 24 in mice. However, moderate-intensity sounds, for example, at conversational levels (~70 dB SPL) may drive spiking activity in the ACX before ECO without surgically opening the ear canal, through bone conduction 25 .…”