Olivocochlear Efferents in Animals and Humans: From Anatomy to Clinical Relevance

Abstract

Olivocochlear efferents allow the central auditory system to adjust the functioning of the inner ear during active and passive listening. While many aspects of efferent anatomy, physiology and function are well established, others remain controversial. This article reviews the current knowledge on olivocochlear efferents, with emphasis on human medial efferents. The review covers (1) the anatomy and physiology of olivocochlear efferents in animals; (2) the methods used for investigating this auditory feedback system in humans, their limitations and best practices; (3) the characteristics of medial-olivocochlear efferents in humans, with a critical analysis of some discrepancies across human studies and between animal and human studies; (4) the possible roles of olivocochlear efferents in hearing, discussing the evidence in favor and against their role in facilitating the detection of signals in noise and in protecting the auditory system from excessive acoustic stimulation; and (5) the emerging association between abnormal olivocochlear efferent function and several health conditions. Finally, we summarize some open issues and introduce promising approaches for investigating the roles of efferents in human hearing using cochlear implants.

Altered cochlear innervation in developing and mature naked and Damaraland mole rats

“…Specifically, medial efferent innervation provides inhibitory input to the OHCs and, thereby, regulates the cochlear amplifier. In this way, medial efferent innervation is believed to improve signal transduction, enhance signal detection, and protect the cochlea from noise‐induced injury (reviewed in both Guinan, ; Lopez‐Poveda, ). Thus, our findings of reduced medial efferent innervation density are consistent with previous reports of reduced cochlear tuning in a related mole rat species, F. anselli (Kössl et al, ).…”

Effect of Auditory Predictability on the Human Peripheral Auditory System

“…Our study shows that intramodal top-down attention may modulate the processing of predictable spectral input in the peripheral auditory system, thereby adding support to current debate on the sensitivity of the human auditory peripheral system to top-down modulation (e.g., Beim et al, 2018;Lopez-Poveda, 2018). Our observations further indicate that predictability may affect auditory processing in the peripheral auditory system.…”

“…Efferent MOC signals may alter the amplitudes and phases of the two DPOAE components (primaries) by different amounts, which can result in either positive or negative DPOAE-level changes depending on the specific primary frequencies (Guinan, 2006)an ambiguity that might explain why some previous DPOAE studies observed opposite effects of auditory attention (Smith et al, 2012;Srinivasan et al, 2012Srinivasan et al, , 2014Wittekindt et al, 2014). Future studies may disambiguate the direction of peripheral predictability effects by measuring, e.g., stimulus-frequency OAEs (SFOAEs), which require only a single test frequency but otherwise more sophisticated methods (Guinan, 2006;Lopez-Poveda, 2018). In sum, our DPOAE results suggest that OHCs may be sensitive to auditory predictability when the listener is paying top-down attention to the acoustic input.…”

“…It is still unclear whether predictive processing occurs also at the lowest stage of auditory processing, in the peripheral auditory system. The peripheral auditory system receives top-down feedback from the central auditory system via the medial olivocochlear (MOC) efferent system (Huffman and Henson, 1990;Lopez-Poveda, 2018). The MOC system is a network of neurons located in the medial part of the superior olivary complex in the brainstem that receives ascending input from the cochlear nucleus and descending input via corticofugal projections.…”

“…Efferent MOC-fiber activity can be modulated in a 'topdown' manner: electric microstimulation or deactivation of the auditory cortex alters OHC activity as measured with cochlear microphonics or otoacoustic emissions (OAEs) (Perrot et al, 2006;Dragicevic et al, 2015;Terreros and Delano, 2015;Jager and Kossl, 2016). Similarly, changes in arousal or endogenous (interor intramodal) attention may lead to OHC-activity changes as measured with OAEs (Puel et al, 1988;Froehlich et al, 1990Froehlich et al, , 1993Giard et al, 1994;Ferber-Viart et al, 1995;Maison et al, 2001;de Boer and Thornton, 2007;Harkrider and Bowers, 2009;Smith et al, 2012;Srinivasan et al, 2012Srinivasan et al, , 2014Walsh et al, 2014Walsh et al, , 2015Wittekindt et al, 2014;Smith and Cone, 2015), although the existence and direction of these top-down attention effects are still debated (Picton et al, 1971;Avan and Bonfils, 1992;Michie et al, 1996;Beim et al, 2018Beim et al, , 2019Francis et al, 2018;Lopez-Poveda, 2018).…”