Behavioral Studies of the Olivocochlear Efferent System Learning to Listen in Noise
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ORIGINAL ARTICLE Behavioral Studies of the Olivocochlear Efferent System Learning to Listen in Noise Bradford J. May, PhD; Jennifer Budelis; John K. Niparko, MD Background: Olivocochlear (OC) neurons make up an Results: As predicted by the hypothesized function of efferent, descending auditory system that returns sound OC feedback systems, the lesioned cats exhibited sig- representations to the inner ear soon after they have en- nificantly elevated thresholds only when tested in back- tered the brain. Efferent inputs into the cochlea modu- ground noise. This initially poor performance returned late outer hair cell activity to improve the neural encod- to normal values after long-term exposure to the testing ing of auditory signals in background noise. Based on this procedure. physiological evidence, loss of efferent feedback is ex- pected to degrade perception in noise. Attempts to con- firm this prediction with long-term audiological assess- Conclusions: The results of our animal studies support ments have met with mixed results. the OC enhancement of sound localization behavior in background noise. Also, our behavioral observations Objective: To isolate procedural factors that may di- suggest the acquisition of alternate listening strategies minish the demonstration of long-term OC deficits in lis- that allowed lesioned cats to minimize the functional tening tasks. consequences of their auditory deficits by attending more closely to remaining directional cues. These Design: Operant conditioning procedures were used to learned compensatory behaviors were encouraged by train domestic cats to signal a change in the location of our present experimental design, which incorporated an auditory stimulus by responding on a lever. The small- long-term training under consistent stimulus condi- est detectable change in location was measured by ma- tions. These findings point out the potential limitations nipulating the distance between speakers under quiet con- of the highly routine audiological procedures that have ditions and in the presence of background noise. been used to assess the impact of OC feedback on Functional consequences of efferent feedback were evalu- human hearing. ated by comparing the sound localization thresholds of OC-lesioned cats with normal controls. Arch Otolaryngol Head Neck Surg. 2004;130:660-664 HE PERIPHERAL AUDITORY system, which links the superior olivary system distributes the complex to the cochlea.1 These efferent physical dimensions of an projections constitute a reflex arc that has acoustic stimulus across the capacity to modify the neural repre- large populations of neu- sentations of sound at the earliest stages Trons. The extraction of elemental percep- of auditory processing (Figure 1A). Al- tual attributes, such as loudness, pitch, and though 2 separate OC systems are im- location, from this highly encoded repre- plied by anatomical differences between sentation demands intensive neural com- efferent neurons in the medial and lateral putations that involve no less than 9 sub- brainstem,2 current physiological descrip- cortical nuclei. Information does not tions are limited to medial OC (MOC) neu- simply ascend the processing levels of the rons.3,4 The present study investigated the central auditory system. Within each behavioral consequences of MOC influ- nucleus, ascending representations are ences that are inferred from these physi- From the Department of transformed by descending influences from ological results. Otolaryngology–Head and Neck Surgery, The Johns higher-order neurons to emphasize the Olivocochlear projections termi- Hopkins University, Baltimore, specific parameters that characterize a nate within the cochlear nucleus and in- Md. The authors have no sound. ner ear (Figure 1B). The MOC fibers in- relevant financial interest in The most widely studied efferent au- fluence cochlear sensitivity and frequency this article. ditory pathway is the olivocochlear (OC) tuning by altering the sound-driven elec- (REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 130, MAY 2004 WWW.ARCHOTO.COM 660 ©2004 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/25/2021 tromotile responses of outer hair cells.5 This mecha- nism for automatic gain control may protect the ear from A damaging sounds and also enhance hearing in back- Brain 6-8 ground noise. Because outer hair cells play a pivotal Ear role in MOC feedback, common forms of sensorineural hearing loss compromise not only ascending auditory rep- Olivary Complex resentations but also the principal effectors of the de- scending OC system. It is possible to manipulate OC neurons indepen- Cochlea dently of the ascending auditory pathways because ef- ferent axons follow a separate course through the brain- B Cochlea stem and into the cochlea. In most animal studies, the OC fibers are exposed along the floor of the fourth ven- tricle (Figure 2A), where the neurons may be acti- vated by electrical stimulation or silenced by surgical le- 9,10 Afferent sions. These interventions most effectively address the Axons extensively crossed pathway of the MOC system. Outer On exiting the lateral brainstem, OC axons enter the Hair Cells 11 Inner cochlea via the inferior branch of the vestibular nerve. Efferent Hair Cells This anatomical detail has important clinical implica- Axons tions. When the vestibular nerve is sectioned to allevi- Figure 1. The reflex arc of medial olivocochlear neurons. A, The auditory ate intractable balance disorders, patients maintain af- brainstem of the cat in frontal section. Sound representations from the ear ferent function but lose all efferent feedback to the affected ascend to the olivary complex via the ventral afferent pathway and project ear (Figure 2B). back to the ear via the dorsal efferent pathway. B, Cross-sectional view of the inner ear. The major ascending afferent pathway arises from inner hair cells. Previous clinical studies have attempted to associ- Descending medial olivocochlear projections terminate on outer hair cells. 12-14 ate OC lesions with a unique pattern of hearing loss. Adapted from Hearing Research (Liberman MC. Effects of chronic cochlear These audiological assessments have investigated tone de-differentiation on auditory-nerve response. Hear Res. 1990;49:209-224) detection, intensity and frequency discrimination, ©1990, with permission from Elsevier. loudness adaptation, frequency selectivity, and spatial lateralization. Although an emphasis has been placed on stimulus conditions that maximize OC influences A in physiological preparations,14 demonstrations of auditory deficits in patient populations have been SC equivocal. IC Electrical Stimulation CBL Brainstem Lesions Based on clinical outcomes, it was hypothesized that Fourth conventional audiological procedures may fail to assess Ventricle OC function. To test this hypothesis, an animal behav- Lesion Crossed Site ior study was conducted to evaluate the effects of bilat- CN eral OC lesions on the sound localization behaviors of Uncrossed AN domestic cats. As predicted by previous behavioral and VN LSO physiological results, lesioned cats showed poor perfor- MSO mance when directional acuity was measured in the pres- ence of continuous background noise. Initially robust per- Vestibular Nerve Section ceptual deficits diminished after repeated testing under B constant stimulus conditions. These findings suggest that Figure 2. Functional manipulations of the olivocochlear pathways. A, Most low-uncertainty audiological procedures may obscure the laboratory studies involve electrical stimulation or surgical lesions along the functional significance of efferent feedback by promot- floor of the fourth ventricle. Brainstem lesions are most effective if they are ing compensatory listening strategies. made bilaterally. B, Vestibular nerve (VN) sections eliminate olivocochlear projections in route to the ear. AN, auditory nerve; CBL, cerebellum; CN, cochlear nucleus; IC, inferior colliculus; LSO, lateral superior olive; MSO, METHODS medial superior olive; SC, superior colliculus. Adapted from Hearing Research (Liberman MC. Effects of chronic cochlear de-differentiation on All surgical and behavioral procedures were approved by the auditory-nerve response. Hear Res. 1990;49:209-224) ©1990, with permission from Elsevier. Institutional Animal Care and Use Committee of The Johns Hop- kins School of Medicine, Baltimore, Md. Detailed descriptions of training methods for sound localization testing in cats are tained clean ears, good general health, and normal adult weights provided in previous publications.15,16 for the course of experiments. Experiments were performed on 6 adult male cats. The cats Experimental trials were designed to test the subject’s were individually caged and fed a restricted diet of dry chow. ability to detect changes in the elevation of a sound source in The feeding regimen was supplemented by liquefied meat paste quiet and in background noise. The cats were trained to that served as rewards for correct responses during behavioral release a response lever when auditory stimuli shifted from a testing sessions. Cats showed a strong appetite for meat paste reference speaker directly in front of the subject (0° elevation) and only moderate food deprivation was needed to motivate to a randomly selected comparison speaker at a higher eleva- subjects to work continuously for hourly sessions. Each cat main- tion in the median plane. After correct releases, a peristaltic (REPRINTED) ARCH OTOLARYNGOL