Medial olivocochlear bundle activation and perceived auditory intensity in humans

Abstract

In order to test the hypothesis of a role of cochlear efferent activity in intensity perception in humans, loudness functions, loudness integration, and loudness summation were measured in the absence and in the presence of contralateral noise in normal-hearing subjects. Additionally, relationships with the effect of the noise on evoked otoacoustic emissions (EOAEs) were tested, and comparisons with vestibular neurotomy patients were performed. Overall, the results failed to demonstrate significant effects of contralateral noise stimulation on loudness functions and loudness integration. Furthermore, no significant differences were found in vestibular neurotomy patients. A significant effect of contralateral noise on loudness summation was noted, but was not related to the effect on otoacoustic emissions. The present results fail to support the notion that efferent influences onto the cochlear compression have a significant perceptual effect.

Introduction

The mammalian cochlea is the target of numerous efferent nervous projections named the olivocochlear bundle (OCB), which originates from the superior olivary complex [37]. The existence of OCB-mediated effects on the auditory periphery has been clearly established [8], [10], [15], [20], [28], [30], [41], [45], [50]. The detailed mechanisms underlying these effects and their relevance in the processing of auditory information remain, however, a current matter of debate. Three main hypotheses concerning the functional role of the OCB have been stated.

First, it has been proposed, based on the suppressive effects of OCB stimulation on peripheral auditory responses, that the main role of the OCB is to protect the inner ear from acoustic overstimulation [23], [36].

Second, it has been proposed that OCB activity makes more accurate the encoding of the signals in noisy backgrounds, leading to lower (better) detection and discrimination thresholds in noise. Some studies with the efferents cut have provided equivocal results [9], [18], [19], [24], [42], [43], [47] but this second hypothesis is, however, sustained by both electrophysiological and behavioral data. Electrophysiological results in animals indicate an unmasking effect of OCB stimulation on auditory nerve fiber responses to signals in noise [20], [21] and recent behavioral measurements collected in animals after section of the OCB showed a thresholds degradation in binaural background noise [24]. The unmasking effect of the OCB is also evidenced by the strong relationships between detection or intensity discrimination thresholds of tones presented in binaural noise, and suppression of the amplitude of evoked otoacoustic emissions (EOAEs) by a contralateral broadband noise [25], [26], which is assumed to reflect OCB functioning. The notion that this contralateral EOAE suppression effect is indeed a reflect of OCB functioning relies on: (1) anatomical data showing that the MOCB projects onto the outer hair cells of the organ of Corti [37]; (2) that these cells have motile properties which are likely to provide the basis for the generation of otoacoustic emissions [5]; and (3) that the OCB can be excited by a contralateral acoustic stimulus [6].

The third hypothesis about the functional role of the medial olivocochlear bundle (MOCB) has been inspired by Russell and Murugasu's study [40] evidencing that the OCB reduces cochlear compression. Because cochlear compression constitutes an essential aspect of intensity encoding by the peripheral auditory system, if cochlear functioning is altered by OCB activity, then intensity perception is likely to be also affected.

The aim of the present study was to test further this latter hypothesis. Advantage was taken of the three different approaches that have been successfully used in previous studies to investigate the role of the OCB in human hearing [16], [25], [26], [42], [43], namely: (1) comparing psychoacoustic measurements obtained in the absence and in the presence of a contralateral broadband noise known to produce substantial activation of the MOCB in the tested ear; (2) testing for relationships between the contralateral noise effect on both psychoacoustic performances and amplitude of EOAEs; and (3) testing whether contralateral noise effects which are supposed to be mediated by OCB activity remain in subjects with cut efferents (i.e. subjects operated for vestibular neurotomy).

Three aspects of intensity perception are investigated, namely: loudness functions, temporal loudness integration, and loudness summation.

Loudness functions provide a straightforward means to track changes in loudness perception upon contralateral noise stimulation or after section of the OCB. Based on the hypothesis that OCB activity reduces cochlear compression, we might expect changes in the shape of the loudness functions upon contralateral stimulation in the control, but not in the vestibular neurotomy subjects.

Temporal loudness integration refers to the fact that loudness increases with duration over about 200–300 ms [11], [29], [35], [46]. Penner [34] first assumed that compression and loudness integration were closely related: the stronger the compression, the larger the integration. Additional lines of evidence for this relationship have been provided over the last decades. In particular, this is consistent with the observed reduced temporal integration for hearing-impaired subjects with reduced cochlear compression [7], [14]. It is also in agreement with recent findings indicating that loudness integration [13], along with compression [38], [51], is more marked at midstimulus intensities. In this context, if OCB activity contributes to reduce cochlear compression [40], less temporal integration should be observed when the OCB is activated. This effect is tested in the present study by measuring loudness integration in a single ear in the presence and in the absence of a contralateral acoustic stimulation.

Loudness summation refers to the fact that loudness is related to stimulus bandwidth independently to the overall physical energy: assuming an equal energy, the wider is the bandwidth of the sound, the louder it sounds [52]. This has been interpreted by considering that the amount of loudness due to spectral components falling in the same auditory filter—i.e. the so-called specific loudness—is a compressive function of the summed intensity of these components. Consequently, the overall loudness of a sound, which is the sum of the specific loudness values, will increase along with the number of filters excited, even if the overall energy is kept constant. The amount of loudness summation, which is equal to the loudness difference between two equal-energy sounds with different bandwidths, will depend on the amount of cochlear compression: the stronger the compression, the larger the loudness summation effect. This is in harmony with the fact that loudness summation has generally been found to be smaller for neurosensorial hearing-impaired people [3], [12], [44] with reduced cochlear compression [27], [31], [32], [33]. If MOC feedback reduces cochlear compression as suggested by electrophysiological data, less loudness summation should be observed when the efferent system is activated by a contralateral noise.