Efferent-mediated control of basilar membrane motion

Abstract

Medial olivocochlear efferent (MOCE) neurones innervate the outer hair cells (OHCs) of the mammalian cochlea, and convey signals that are capable of controlling the sensitivity of the peripheral auditory system in a frequency-specific manner. Recent methodological developments have allowed the effects of the MOCE system to be observed in vivo at the level of the basilar membrane (BM). These observations have confirmed earlier theories that at least some of the MOCE's effects are mediated via the cochlea's mechanics, with the OHCs acting as the mechanical effectors. However, the new observations have also provided some unexpected twists: apparently, the MOCEs can enhance the BM's responses to some sounds while inhibiting its responses to others, and they can alter the BM's response to a single sound using at least two separate mechanisms. Such observations put new constraints on the way in which the cochlea's mechanics, and the OHCs in particular, are thought to operate.

Figure 1. Simplified circuitry, and experimental approaches to the medial olivocochlear efferent system

A, schematic section of the mammalian brainstem illustrating bilateral origins of MOCE neurones in the medial regions of the superior olivary complex. Electrical stimulation of the MOCE system is facilitated by exposing the floor of the fourth ventricle at the midline, where both uncrossed (red) and crossed (cyan) MOCE fibres lie close to the surface of the brainstem. B, schematic section of organ of Corti illustrating MOCE innervation of the outer hair cells. Interferometric recording of sound-evoked motion (white arrows) is facilitated by placing reflective microbeads on the undersurface of the basilar membrane. Illustrations based on originals provided by M. C. Liberman. Abbreviations: AN – auditory nerve; ANF – auditory nerve fibre; BM – basilar membrane; CN – cochlear nucleus; IHC – inner hair cell; OHC – outer hair cell; MOCE – medial olivocochlear efferent; SOC – superior olivary complex.

Figure 2. Frequency dependence of MOCE fast effects on BM motion in the guinea-pig cochlea

A, amplitude growth functions for BM responses to tones below, near, and above the BM's characteristic frequency (CF) immediately before (blue) and during (green) electrical stimulation of MOCE fibres. B, iso-displacement tuning curves for BM motion immediately before (blue) and during (green) MOCE stimulation. The two iso-displacement criteria (0.1 and 3.16 nm) were selected to contrast the relative strengths of the MOCE effects at sound levels near and well-above the thresholds of most auditory nerve fibres, respectively. Adapted with permission from Cooper & Guinan (2006).

Figure 3. Fast and slow effects of MOCE stimulation on BM motion in the guinea-pig cochlea

A, BM responses to 160 ms tone-bursts at four instants before, during and after a 100 s period of repetitive MOCE stimulation (the yellow ‘test’ period). The tone bursts were presented at 35dB SPL at the BM's CF (19 kHz), and the stimulus repetition period was 330 ms. Pulse trains (red) above responses 2 and 3 illustrate the fine timing patterns of the MOCE stimulation. Slow effects of the MOCE stimulation are manifest as changes in the BM responses near the onset of each tone (shaded blue) across individual tone-bursts (i.e. as differences from the control or baseline responses, illustrated by horizontal dashed lines). Fast effects are manifest as changes in the BM responses within individual tone-bursts (i.e. as differences between the blue and green sections of each response). B, amplitude and phase changes attributed to the fast (▵) and slow (•) effects. Each effect inhibits the BM's motion by more than 10 dB, but the fast and slow forms of inhibition are accompanied by phase leads and phase lags, respectively. Reproduced from Cooper & Guinan (2003).