The Olivocochlear Reflex Strength and Cochlear Sensitivity are Independently Modulated by Auditory Cortex Microstimulation

Abstract

In mammals, efferent projections to the cochlear receptor are constituted by olivocochlear (OC) fibers that originate in the superior olivary complex. Medial and lateral OC neurons make synapses with outer hair cells and with auditory nerve fibers, respectively. In addition to the OC system, there are also descending projections from the auditory cortex that are directed towards the thalamus, inferior colliculus, cochlear nucleus, and superior olivary complex. Olivocochlear function can be assessed by measuring a brainstem reflex mediated by auditory nerve fibers, cochlear nucleus neurons, and OC fibers. Although it is known that the OC reflex is activated by contralateral acoustic stimulation and produces a suppression of cochlear responses, the influence of cortical descending pathways in the OC reflex is largely unknown. Here, we used auditory cortex electrical microstimulation in chinchillas to study a possible cortical modulation of cochlear and auditory nerve responses to tones in the absence and presence of contralateral noise. We found that cortical microstimulation produces two different peripheral modulations: (i) changes in cochlear sensitivity evidenced by amplitude modulation of cochlear microphonics and auditory nerve compound action potentials and (ii) enhancement or suppression of the OC reflex strength as measured by auditory nerve responses, which depended on the intersubject variability of the OC reflex. Moreover, both corticofugal effects were not correlated, suggesting the presence of two functionally different efferent pathways. These results demonstrate that auditory cortex electrical microstimulation independently modulates the OC reflex strength and cochlear sensitivity.

Cochlear activity in silent cue-target intervals shows a theta-rhythmic pattern and is correlated to attentional alpha modulations

“…In the current study we show power modulations of OOA in frequencies that in the cortical literature have been repeatedly reported to be related to various attentional task demands Fries et al, 2001;Klimesch, 2012;Wutz et al, 2018). Electrical stimulation of the auditory cortex in bats and chinchillas shows that cochlear responses can be modulated in a frequency specific manner (Dragicevic et al, 2015;León et al, 2012;Xiao & Suga, 2002). The current results imply that the modulation of cochlear low-frequency oscillatory power putatively is driven by top-down attentional processes (note that the frequency is unchanged).…”

Effect of Auditory Predictability on the Human Peripheral Auditory System

“…Efferent MOC fibers project to outer hair cells (OHCs) in the cochlea and activation of these fibers alters OHC activity, effectively reducing cochlear gain (reviews: Guinan, 2006Guinan, , 2018. 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).…”

Corticofugal modulation of peripheral auditory responses

“…Only a few physiological studies have assessed the corticofugal effects of auditory cortex manipulations on the most peripheral auditory structures, including, auditory nerve responses (León et al, 2012 ; Dragicevic et al, 2015 ), cochlear electrical responses (Xiao and Suga, 2002 ; León et al, 2012 ; Dragicevic et al, 2015 ) and otoacoustic emissions (OAE; Khalfa et al, 2001 ; Perrot et al, 2006 ). In a seminal work, Xiao and Suga ( 2002 ) demonstrated that the auditory cortex activity modulates the amplitude and frequency tuning of cochlear microphonics (CM) responses near the echolocalizing frequency of the mustached bat (61 kHz).…”