Abstract
The dynamic adjustment of hearing sensitivity and frequency selectivity is mediated by the medial olivocochlear efferent reflex, which suppresses the gain of the ‘cochlear amplifier' in each ear. Such efferent feedback is important for promoting discrimination of sounds in background noise, sound localization and protecting the cochleae from acoustic overstimulation. However, the sensory driver for the olivocochlear reflex is unknown. Here, we resolve this longstanding question using a mouse model null for the gene encoding the type III intermediate filament peripherin (Prph). Prph(−/−) mice lacked type II spiral ganglion neuron innervation of the outer hair cells, whereas innervation of the inner hair cells by type I spiral ganglion neurons was normal. Compared with Prph(+/+) controls, both contralateral and ipsilateral olivocochlear efferent-mediated suppression of the cochlear amplifier were absent in Prph(−/−) mice, demonstrating that outer hair cells and their type II afferents constitute the sensory drive for the olivocochlear efferent reflex.
Highlights
The dynamic adjustment of hearing sensitivity and frequency selectivity is mediated by the medial olivocochlear efferent reflex, which suppresses the gain of the ‘cochlear amplifier’ in each ear
The type II spiral ganglion neurons (SGNs) fibres turn basally at the Deiters’ cell level to form the outer spiral bundle (OSB) that innervates multiple OHCs19,22. This was most evident in the neonatal cochlea (Supplementary Fig. 1a,c–f), whereas PRPH immunolabelling in the adult cochlear type II SGN fibres diminished beyond the inner spiral plexus (Supplementary Fig. 1b,g,h), compared with resolution of the OSB with neurofilament 200 kDa (NF200) immunolabelling (Fig. 1a,c)
Our findings determine that the outer hair cell (OHC)—type II SGN sensory pathway drives the medial olivocochlear (MOC) efferent reflex-mediated control of the cochlear amplifier
Summary
The dynamic adjustment of hearing sensitivity and frequency selectivity is mediated by the medial olivocochlear efferent reflex, which suppresses the gain of the ‘cochlear amplifier’ in each ear. The relative levels of sound transduced by IHCs between the two ears is principally regulated by a sensorimotor reflex pathway, which responds to elevation of sound in one ear by rapidly reducing the gain of the cochlear amplifier in the opposite cochlea[5,6,7] This ‘contralateral suppression’ is produced by medial olivocochlear (MOC) efferent neurons located in the superior olivary complex of the brainstem, whose myelinated axons approach the floor of the fourth ventricle from both sides before migrating laterally to join the ipsilateral auditory nerve and terminate on the OHCs8. MOC reflex control of hearing sensitivity utilizes a closed-loop negative-feedback pathway with the OHCs operating as both the sensor and effector
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