The cochlear amplifier: augmentation of the traveling wave within the inner ear

Abstract

Purpose of review: There have been many recent advancements in our understanding of cochlear function within the past ten years. In particular, several mechanisms that underlie the sensitivity and sharpness of mammalian tuning have been discovered. This review focuses on these issues.

Recent findings: The cochlear amplifier is essentially a positive feedback loop within the cochlea that amplifies the traveling wave. Thus, vibrations within the organ of Corti are sensed and then force is generated in synchrony to increase the vibrations. Mechanisms that generate force within the cochlea include outer hair cell electromotility and stereociliary active bundle movements. These processes can be modulated by the intracellular ionic composition, the lipid constituents of the outer hair cell plasma membrane, and the structure of the outer hair cell cytoskeleton.

Summary: A thorough understanding of the cochlear amplifier has tremendous implications to improve human hearing. Sensorineural hearing loss is a common clinical problem and a common site of initial pathology is the outer hair cell. Loss of outer hair cells causes loss of the cochlear amplifier, resulting in progressive sensorineural hearing loss.

Figure 1. Organ of Corti

There is a single row of inner hair cells and three parallel rows of outer hair cells. Outer hair cells are supported by Deiter cells. The hair cells and all supporting cells sit on the basilar membrane. A section of the basilar membrane is enlarged to demonstrate the radial arrays of collagen filaments within it. The basilar membrane and the tectorial membrane are fixed at different locations to the modiolus. When sound vibrations cause the organ of Corti to move up and down, a shearing force is created, which deflects the hair cell stereocilia.

Figure 2. Pressure waves begin propagating up the length of the cochlear duct towards the apex

(A) Acoustic energy propagation down the cochlea. Sound pressure waves enter the scala vestibuli through movement of the stapes footplate. The acoustic energy propagates down the perilymph, traversing the basilar membrane predominantly at the region of its characteristic frequency. This creates the classical “traveling wave” motion of the basilar membrane. The region of the characteristic frequency is the area of maximal vibrations of the basilar membrane. The energy then propagates back to the round window through scala tympani. (B) Peak amplitudes of basilar membrane motion with and without the cochlear amplifier. These plots are based on simulations of the cochlear traveling wave as it propagates down the cochlea from the stapes to the helicotrema when a single frequency tone is played into the ear. The peak amplitude of the traveling wave is plotted. Without the cochlear amplifier, the traveling wave gradually reaches a peak, and then rapidly declines. With the cochlear amplifier, there is a large increase in basilar membrane motion. Also, note that there is sharpening of the peak with the cochlear amplifier. This permits improved frequency discrimination.

Figure 3. Stereotypical hair cell

The boundary between the endolymph and the perilymph is the apical tight junctions between hair cells and supporting cells (the reticular lamina). There are three major functions within all hair cells. (1) Mechanoelectrical transduction occurs at the tips of the stereocilia, allowing ions from the endolymph to enter the cell. (2) Efferent nerve terminals and other ion channels modulate the intracellular voltage inside the hair cell and permit potassium exit from the cell for recycling. (3) Depolarization of the hair cell causes synaptic transmission of the afferent auditory nerve terminals. The neurotransmitter is glutamate. Figure derived from Eatock (1997) [84].

Figure 4. Outer hair cell electromotility

Outer hair cell electromotility. Outer hair cells contract and elongate with each cycle of sound as their intracellular voltage changes. This amplifies the vibration of the organ of Corti, permitting exquisite hearing sensitivity and frequency selectivity. OHCs have an intracellular turgor pressure to help maintain their shape. Loss of OHC turgor pressure causes the cell to constrict so that it can no longer produce electromotile force. Figure derived from Brownell (1999) [85].

Figure 5. Diagram of OHC with detail of lateral wall components

The lateral wall is composed of the plasma membrane, the cytoskeleton, and the subsurface cisterna. The cytoskeleton contains actin, spectrin, and pillar molecules. Some (perhaps most) of the particles in the plasma membrane are prestin proteins. Figure derived from Oghalai et al. (1998) [26].