Chapter 9: Hearing and Balance



I. Overview

Modern day aquatic vertebrates possess lateral-line sensory systems that detect vibrations and movements in their watery surrounds. Lateral lines comprise lines of pits running down both sides of the body. Movements are transduced by clusters of sensory hair cells embedded in a gelatinous dome that protrudes from each lateral-line pit. When the dome is displaced by local water currents or vibrations, the embedded hairs are displaced also, generating a receptor potential in the hair cell body.

Although humans did not retain lateral-line organs during evolution, the hair cell transduction system works so well that it was adapted for use in the inner ear. The inner ear contains two contiguous, hair cell–based sensory systems. The auditory system uses hair cells to transduce vibrations generated by sound waves. The vestibular system uses hair cells to transduce head movements.

II. Sound

Sounds are atmospheric pressure waves created by moving objects. For example, striking a metal gong causes its metal surface to vibrate back and forth (Figure 9.1). The gong alternately compresses and then decompresses the surrounding air to create a pressure wave that propagates outward at a speed of 343 m/s. We perceive these pressure waves as sounds, the wave’s frequency reflecting its pitch. The ability to transduce sound waves (audition) allows us to detect objects at a distance and, therefore, has clear survival advantages.

If an approaching object represents a threat (e.g., a predator or speeding truck), advance warning of its approach allows time for evasive maneuvers. The ability to hear vocalizations allowed for the development of oral communication and speech. The ability to perceive sound requires that the energy of sound waves be converted into an electrical signal, a process that occurs within the inner ear and relies on sensory hair cells.

Figure 9.1 Sounds are pressure waves that travel through air.

III. Auditory System

Designing a system that transduces sound is relatively easy because sound waves vibrate membranes. For example, a dog’s bark creates vibrations in the wall of an empty soda can or milk jug that can easily be sensed by mechanoreceptors in the fingertips. Sounds are usually very complex, however, comprising a series of changing frequencies. The ear decodes such sounds using an array of sensory hair cells embedded within a membrane that is designed to resonate at different frequencies along its length. It combines this with an amplifier to create a remarkably sensitive acoustic analyzer.

A. Structure

The auditory system, or ear, can be divided into three main anatomical components: the outer, middle, and inner ear (Figure 9.2).

Figure 9.2 Ear anatomy.

Modified from Krebs, C., Weinberg, J., and Akesson, E. Lippincott’s Illustrated Review of Neuroscience. Lippincott Williams ; Wilkins, 2012

1. Outer ear

The pinna collects and focuses sounds. Sounds are channeled into the ear canal (external auditory meatus), which allows them to pass through the skull’s temporal bone. The canal ends blindly at the tympanic membrane (eardrum), which vibrates in response to sound.

2. Middle ear

The middle ear is an air-filled chamber lying between the eardrum and the inner ear. It connects with the nasopharynx via the eustachian tube, which drains fluids and allows the pressure across the eardrum’s two surfaces to equalize. Eardrum vibrations are transmitted to the inner ear by an articulating lever system comprising three, small, fragile bones called ossicles (Figure 9.3). The bones are known as the malleus (hammer), incus (anvil), and stapes (stirrup), their names roughly reflecting their shapes. The malleus is attached to the eardrum’s inner surface and transmits vibrations to the incus. The incus transmits them to the stapes. The stapes’ footplate inserts into and is firmly attached to the oval window of the inner ear.

Figure 9.3 Ossicles and their role in impedance matching.

Modified from Bear, M.F., Connors, B.W., and Paradiso, M.A. Neuroscience—Exploring the Brain. Third Edition. Lippincott Williams & Wilkins, 2007

3. Inner ear

The inner ear contains a convoluted series of fluid-filled chambers and tubes (membranous labyrinth). The structures are encased within bone (the bony labyrinth) with a thin layer of perilymph trapped between bone and membranes. The labyrinth has two sensory functions. The auditory portion is called the cochlea. The vestibular portion contributes to our sense of balance (see section V below). It comprises the otolith organs (utricle and saccule) and three semicircular canals.

B. Impedance matching

The inner ear is filled with fluid that has a high inertia and is difficult to move compared with air. The middle ear’s function is, thus, to harness the sound wave’s inherent energy and transmit it to the inner ear with sufficient force to overcome the inertia of the fluid contents. This process is called impedance matching.

1. Mechanism

The ossicles form a lever system that amplifies eardrum movements by ~30% (see Figure 9.3). It also focuses the movements on the stapes’ footplate, whose surface area is ~17 times smaller than the eardrum. Amplification and focusing combined increase force per unit area ~22-fold, which allows sounds to be transferred to the inner ear with sufficient force to overcome cochlear fluid inertia.

2. Damping

Lever system flexibility is modulated to reduce sound amplitude under certain circumstances. The malleus and stapes are attached to two tiny muscles under autonomic control (Figure 9.4). The tensor tympani anchors the malleus to the wall of the middle ear and is innervated by the trigeminal nerve (cranial nerve [CN] V). The stapes is anchored by the stapedius, which is innervated by the facial nerve (CN VII). When the two muscles contract, the ossicular chain becomes more rigid, and sound transmission is attenuated. The attenuation reflex can be triggered by loud sounds but is probably designed to dampen the sound of our own voices when talking.

Figure 9.4 Attenuation reflex.

Modified from Bear, M.F., Connors, B.W., and Paradiso, M.A. Neuroscience—Exploring the Brain. Third Edition. Lippincott Williams & Wilkins, 2007

C. Cochlea

The cochlea is a long (~3 cm), tapered tube containing three fluid-filled chambers that run the length of the tube. The tube is coiled like a snail shell in vivo, but the functional architecture is easier to understand when considered uncoiled (Figure 9.5). The three chambers are called the scala vestibuli, the scala media, and the scala tympani.

Figure 9.5 Cochlear chambers.

1. Scala vestibuli and scala tympani

The upper and lower chambers are both filled with perilymph (a fluid approximating plasma) and are physically connected by a small opening (the helicotrema) at the cochlear apex.

2. Scala media

The center chamber is separated from the scala vestibuli by the Reissner membrane (or vestibular membrane) and from the scala tympani by the basilar membrane. The scala media terminates short of the cochlea apex and is sealed off from the other two chambers. It is filled with endolymph, a K+-rich fluid produced by the stria vascularis, a specialized epithelium lining one wall of the chamber (see Figure 9.5). The scala media contains the organ of Corti, which is the auditory sensory organ.

IV. Auditory Transduction

Sound waves enter the cochlea via the oval window, which forms the basal end of the scala vestibuli (Figure 9.6). Stapes motion sets up a pressure wave in the perilymph that runs down the chamber’s length to the apex, passes through the helicotrema, and then pulses back down the scala tympani to the cochlear base. Here, it encounters the round window, a thin membrane located between the inner and middle ear. The membrane vibrates back and forth in reverse phase with the wave generated by stapes movement. The stapes would not be able to displace the oval window and set the perilymph in motion if the round window did not exist because the cochlear chamber walls are otherwise rigidly encased in bone. The scala media, which approximates a fluid-filled sac suspended between the two chambers, is buffeted by the pressure wave as it pulses back and forth. Thus, although the sound wave never enters the scala media directly, the entire structure wobbles, much as a waterbed responds when pushed down on hard at one corner. It is this buffeting that is sensed by the organ of Corti.

Figure 9.6 Sound wave passage through the cochlear chambers.

Modified from Bear, M.F., Connors, B.W., and Paradiso, M.A. Neuroscience—Exploring the Brain. Third Edition. Lippincott Williams ; Wilkins, 2007

A. Organ of Corti

The organ of Corti comprises a sheet of auditory receptor cells (hair cells) and their associated structures, all of which rest on the basilar membrane (Figure 9.7).

Figure 9.7 Organ of Corti.

Modified from Bear, M.F., Connors, B.W., and Paradiso, M.A. Neuroscience—Exploring the Brain. Third Edition. Lippincott Williams ; Wilkins, 2007

1. Hair cell types

The hair cells are arranged in rows down the length of the cochlea. Two types of hair cell (inner and outer) can be distinguished based on their location, innervation, and function.

a. Inner

Inner hair cells ([IHCs] ~3,500 total) form a single row toward the center of the cochlea. They are densely innervated by sensory neurons (up to 20 per cell), whose axons make up the bulk of the cochlear nerve (part of the vestibulocochlear nerve, or CN VIII). IHCs are the ear’s primary sound transducers.

b. Outer

There are an additional three rows of outer hair cells (OHCs). Although they number around 20,000 in total, their contribution to auditory nerve output is only ~5%. OHCs amplify and fine-tune auditory signals.

2. Reticular lamina

Hair cells are covered with a stiff, membranous reticular lamina (see 4?II?A) that is anchored to the basilar membrane by struts (rods of Corti). The reticular lamina both provides structural support for the hair cells and also forms a barrier to ion movement between endolymph and perilymph.

3. Tectorial membrane

Hair cells bear ~100 sensory stereocilia at their apical surface. They protrude through the reticular lamina into endolymph, a K+-rich fluid whose unusual ion composition is critical for generating an auditory receptor potential (see below). The tips of OHC stereocilia embed in a gelatinous tectorial membrane, which lies over the cells like a blanket. When the basilar membrane is buffeted by sound, the hair cells are dragged back and forth beneath the blanket, and the stereocilia are forced to bend (see Figure 9.7).

B. Hair cell function

In order for sound waves to be perceived as such by the central nervous system (CNS), their energy must be converted to an electrical signal. Movement is sensed at the molecular level by mechanoreceptive ion channels located on sensory hair cells.

1. Hair cell structure

Hair cells are polarized, nonneuronal sensory cells. The apical side bears several rows of stereocilia, which are stepped in height to form ranks (Figure 9.8). The basal side synapses with one or more sensory afferent neurons, which the hair cell communicates with using an excitatory neurotransmitter (glutamate) when stimulated appropriately.

Figure 9.8 Role of stereocilia in mechanosensory transduction.

2. Stereocilia

At birth, hair cells contain a true cilium (kinocilium) that may help establish stereociliary orientation. The kinocilium is not involved in auditory transduction, degenerating shortly after birth. Stereocilia are actin filled and rigid. They taper at their base where they meet the hair cell body, creating a hinge that allows for deflection (see Figure 9.8). Cilia are linked at their tips down the ranks by fine elastic protein strands called tip links, the lower ends of which are connected to a mechanosensitive or mechanoelectrical transduction (MET) channel. When the stereocilia bend toward the tallest rank, the tip links tense and pull the MET channel open. This is the mechanosensory transduction step.

C. Mechanotransduction

The hair cells straddle two compartments with strikingly different ion compositions, which favor an unusual depolarizing K+ current when the MET channel opens (Figure 9.9).

Figure 9.9 Mechanosensory transduction and K+ recycling.

 K+ concentrations are given in mmol/L. Vm = membrane potential.

1. Endolymph

The stereocilia are bathed in endolymph, a unique fluid that is secreted by the stria vascularis, a highly vascularized epithelium (see Figure 9.9B). Endolymph is characterized by a K+ concentration of ~150 mmol/L, far higher than that of perilymph or extracellular fluid (~5 mmol/L). The inside of the hair cell relative to endolymph is ?120 mV, which creates a very strong electrochemical gradient for K+ influx across the stereociliary membrane.

2. Perilymph

The basolateral side of the hair cell is bathed in perilymph. This fluid is high in Na+ and low in K+, much like extracellular fluid. Perilymph is considered to be at 0 mV, so hair cell membrane potential (Vm) relative to perilymph is ?40 mV. The voltage difference between endolymph and perilymph, which approximates 80 mV, is known as the endocochlear potential.

3. Receptor currents

The mechanosensitive MET channel is relatively nonselective for cations and may be a member of the transient receptor potential channel family (see 2?VI?D). When it opens, K+ (and Ca2+) flow into the cell and cause a receptor depolarization (see Figure 9.9A). This stands in stark contrast to the usual effects of K+-channel opening on Vm. Most cells are bathed in low-K+ extracellular fluid, so K+-channel opening usually causes K+ efflux and hyperpolarization.

 Clinical Application 9.1: Congenital Hearing Loss

Congenital hearing loss (HL) results from mutations in any of the many genes required for auditory transduction, signaling, and processing. The most common form of HL results from a recessive mutation in the GJB2 gene (known previously as DFNB1), which encodes connexin-26. Connexins are proteins that form gap junction channels between adjacent cells in many tissues, including those of the stria vascularis (see 4?II?F).

The KCNJ10 gene encodes an adenosine triphosphate–gated K+ channel that is expressed in intermediate cells of the stria vascularis (see Figure 9.9B). These cells are responsible for maintaining high endolymph K+ concentrations. KCNJ10 mutation interrupts K+ recycling, collapses the endocochlear potential that is required for auditory transduction, and causes profound deafness.

4. Potassium recycling

K+ exits hair cells via K+ channels in the basolateral membrane (see Figure 9.9A) and is returned to the endolymph via the stria vascularis (see Figure 9.9B).