Chapter 44. Anatomy & Physiology of the Ear

Mechanical events resulting from sound, gravitational forces, and rotational acceleration are detected by the cochlea and vestibular organs within the inner ear. Sound is a mechanical vibration (eg, as produced by a vibrating piano string). This vibration sets up small oscillations of air molecules that, in turn, cause adjacent molecules to oscillate as the sound propagates away from its source. Sound is called a pressure wave because when the molecules of air come closer, the pressure increases (compression); as they move further apart, the pressure decreases (rarefaction).

A sound is characterized by its frequency and intensity. The frequency of a sound is its pitch. Middle C on a piano has a frequency of 256 cycles per second, whereas high C (seven white keys to the right) has a frequency of 512 cycles per second (Figure 44–1). People with normal hearing can tell the difference between two sounds that differ in frequency by less than 0.5%. To appreciate how small a difference this is, one needs only to realize that middle C differs from C sharp by more than 5%. Human hearing is limited to sound waves between 20 and 20,000 Hz. Many other mammals can hear ultrasound (>20,000 Hz), and some, such as whales, approach up to 100,000 Hz.

The intensity of a sound determines its loudness and reflects how tightly packed the molecules of air become during the compression phase of a sound wave. The ear can detect sounds in which the vibration of the air at the tympanic membrane is less than the diameter of a hydrogen molecule (< 0.24 nm). The mammalian ear has the ability to discriminate a wide range of intensities—over a 100,000-fold difference in energy (120 dB).

To maximize the transfer of sound energy from the air-filled environment to the fluid-filled inner ear, land animals evolved external ears as sound collectors and middle ears as mechanical force amplifiers (Figure 44–2).

The task of the cochlea is to analyze environmental sounds and transmit the results of that analysis to the brain. The inner ear first determines how much energy is present at different frequencies that make up a specific sound. The cochlea can do this because of its tonotopic organization, whereby different frequency tones stimulate different areas of the cochlea. This mapping of frequency information is just one of the several strategies that the ear uses to code incoming information. The frequency analysis of environmental sounds begins in the external ear.

Pinna

The external ear consists of the pinna and the external auditory canal. The pinna (Figure 44–3) is a three-layered structure. The central framework consists of elastic cartilage surrounded by a layer of skin. There is minimal subcutaneous tissue between the skin and the perichondrium. Physiologically, the pinna acts to funnel sound waves into the ear canal. The intricate shape of the pinna affects the frequency response of incoming sounds differently, depending on the vertical position from which the sound originated. This information is used by the brain to localize the sound source in three-dimensional space. Overall, the shape of the external ear provides approximately 20 dB of gain to sounds in the middle frequency range (2–4 kHz).

External Auditory Canal

The external auditory canal consists of a lateral cartilaginous portion and a medial bony portion. Each portion of the canal takes up approximately half of its length. The tragus forms the anterior cartilaginous canal. Directly in front of it lies the parotid gland. The facial nerve exits the stylomastoid foramen 1 cm deep to the tip of the tragus (the tragal pointer). Within the anterior and inferior portions of the cartilaginous ear canal, there are small fenestrations through the cartilage called the fissures of Santorini. Infection of the ear canal (otitis externa) can spread to the parotid gland through these fissures and may lead to skull base osteomyelitis. The tympanic portion of the temporal bone forms most of the bony ear canal. Anterior to the bony canal is the temporomandibular joint. The skin of the ear canal is thicker in the cartilaginous canal and contains glands that secrete cerumen (ear wax). The skin of the bony ear canal is very thin and fixed to the periosteum. No cerumen is secreted in the bony ear canal.

The great auricular nerve (from nerve roots C2 and C3) provides sensory innervation to the skin overlying the mastoid process as well as to most of the pinna. Cranial nerves V (the trigeminal nerve), VII (the facial nerve), and X (the vagus nerve) innervate the external auditory canal.

Tympanic Membrane

The tympanic membrane consists of three layers: outer, middle, and inner. The outer layer arises from the ectoderm, which consists of squamous epithelium. The inner layer originates from the endoderm and consists of cuboidal mucosal epithelium. The middle layer originates from the mesenchyme and is called the middle fibrous layer. The middle fibrous layer of the tympanic membrane consists of both radial and circumferential fibers. These fibers are important in maintaining the strength of the tympanic membrane as well as in aiding the proper vibration of the tympanic membrane with different frequency sounds.

The tympanic membrane has an oval shape and is approximately 8 mm wide and 10 mm high (Figure 44–4). The tympanic membrane is sloped so that the superior aspect is lateral to the inferior aspect. In addition, the tympanic membrane is tented medially by the long process of the malleus (manubrium). Around the circumference of the tympanic membrane is the fibrous annulus, which sits in the tympanic sulcus, a groove in the bone at the medial end of the external auditory canal. The annulus is incomplete superior to the anterior and the posterior malleal folds. The pars flaccida is above the anterior and posterior malleal folds while the pars tensa is inferior to the folds. The pars flaccida is also known as the Shrapnell membrane. The middle fibrous layer of the pars flaccida is weaker than that of the pars tensa. This area of the tympanic membrane can easily retract inwardly when the middle ear pressure is less than the environmental air pressure and is often the starting point of an attic cholesteatoma. Blood vessels enter the tympanic membrane through the superior external auditory canal skin (the vascular strip) as well as circumferentially from around the fibrous annulus.

Middle Ear Cavity

The middle ear cavity (Figure 44–5) originates embryologically from the first branchial pouch. It is connected to the nasopharynx via the eustachian tube. Posterior to the middle ear cavity are the mastoid air cells, which connect with the attic through the aditus ad antrum. The middle ear cavity and mastoid air cells are lined with ciliated mucosal epithelium. Anatomically, the middle ear space can be divided into five portions based on their relationship to the tympanic annulus: the mesotympanum, hypotympanum, attic, protympanum, and retrotympanum (see Figure 44–5). The retrotympanum includes the sinus tympani and facial recess.

The blood supply in the middle ear and mastoid originates from the internal and external carotid arteries. Vessels off the external carotid artery include the anterior tympanic artery and the deep auricular artery (branches of the internal maxillary artery), the superior petrosal and superior tympanic arteries (branches of the middle meningeal artery), and the stylomastoid artery (a branch of the occipital artery that runs up the stylomastoid foramen). In addition, the caroticotympanic artery, a branch of the internal carotid artery, forms a plexus over the promontory of the middle ear.

Ossicular Chain

There are three ossicles (Figure 44–6): the malleus, the incus, and the stapes. The malleus has a long process, a short process, and a head. The malleus is bonded to the tympanic membrane from the tip of the long process (the umbo) to the short process. The head of the malleus articulates with the body of the incus in the attic.

The short process of the incus is tethered to the posterior wall of the middle ear cavity for structural support and the long process is connected to the stapes capitulum. The distal portion of the long process is known as the lenticular process. The blood supply to the ossicular chain is most tentative at the lenticular process and is the first portion of the ossicular chain to be resorbed in patients with chronic otitis media, producing ossicular discontinuity.

The stapes consists of a footplate and a superstructure. The superstructure includes the anterior and posterior crus, which are attached at the capitulum. The footplate sits within the oval window.

The stapedius muscle (Figures 44–7 and 44–8) originates from the pyramidal eminence. The tensor tympani muscle is anchored by the cochleariform process where it turns 90° and becomes a tendon that connects to the malleus. The ponticulus is a ridge of bone between the round window and the oval window. The subiculum is a ridge of bone just anterior to the round window. The promontory is the medial wall of the middle ear cavity. Medial to the promontory is the cochlea.

The embryologic development of the ossicles is complex. The ossicular portions found in the attic are formed from the first branchial arch. This includes the head of the malleus and the body and short process of the incus. The ossicular portions that are found within the mesotympanum originate from the second branchial arch. This includes the long process of the malleus, the long process of the incus, and the stapes superstructure. The stapes footplate originates from the otic capsule (the primordial otocyst), rather than from a branchial arch. The ossicles are full-sized cartilage models by 15 weeks of gestation, and endochondral ossification is complete by 25 weeks. The middle ear is adult sized at birth.

Nervous Structures

The facial nerve is the major nerve traversing the middle ear cavity (Figure 44–7). After entering the temporal bone via the internal auditory canal, the labyrinthine segment courses to the geniculate ganglion, immediately superior to the cochlea. The facial nerve then turns (first genu) and runs horizontally through the middle ear space (the tympanic portion of the facial nerve). The nerve lies superior to the oval window and the bone is often missing (dehiscent facial nerve) at this point. The nerve then turns again (second genu) and runs vertically (the vertical portion of the facial nerve). The nerve exits the temporal bone through the stylomastoid foramen, which is medial to the digastric muscle but lateral to the styloid process.

There are three branches of the facial nerve within the temporal bone. The greater superficial petrosal nerve (Figure 44–5) branches off at the geniculate ganglion and delivers parasympathetic nerves to the lacrimal gland and to the minor salivary glands of the nose. Another branch of the facial nerve goes to the stapedius muscle. Finally, the chorda tympani nerve branches off from the vertical portion of the facial nerve and runs underneath the tympanic membrane, medial to the malleus, before exiting the middle ear space through the petrotympanic fissure. It joins up with cranial nerve V3 and supplies both taste to the anterior two thirds of the tongue as well as parasympathetic innervation to the sublingual and submandibular glands. The cell bodies of these nerves are found in the geniculate ganglion.

Cranial nerve IX (the glossopharyngeal nerve) has a branch that runs across the tympanic promontory called the tympanic nerve or Jacobson's nerve. It innervates the mucosa of the middle ear space and Eustachian tube as well as provides parasympathetic innervation to the parotid gland. There is also a branch of the vagus nerve within the middle ear cavity called Arnold's nerve, which supplies innervation to the external auditory canal. Patients often cough when their ear canal is cleaned because of the referred sensation to the throat.

The Facial Recess and the Sinus Tympani

Understanding the area around the second genu of the facial nerve is critical for conducting safe middle ear surgery (Figure 44–8). The bony ear canal ends at the level of the annulus. The space medial to the end of the ear canal, but lateral to the facial nerve, is the facial recess. Medial to the facial nerve is another pocket of space called the sinus tympani. It is impossible to visualize the sinus tympani by looking either through the ear canal or through an opening made through the mastoid. Residual cholesteatoma is often found here because of remnants left behind (and not seen) during primary surgery.

Physiology of the Middle Ear

The middle ear provides an acoustic impedance match between the environmental air and the fluid-filled inner ear. The middle ear amplifies the airborne sound vibration in two ways. First, the large surface area of the tympanic membrane, compared with the small surface area of the stapes (14:1), imparts an increase in vibrational amplitude. Second, the lever arm effect of the malleus and incus imparts a further increase in vibrational amplitude (1.3:1.0). Thus, the total middle ear gain is between 20 and 35 dB. In addition, the mass and stiffness of the ossicular chain affect its frequency response. Overall, the middle ear acts as a band-pass filter, with a maximum energy transfer over the range of 1–10 kHz.

Changing the mass and stiffness of the middle ear modulates its frequency response, which can be observed clinically. For example, the stapedius and tensor tympani muscles contract through a neural reflex arc mediated by loud sounds (>80 dB). They act to stiffen the ossicular chain and protect the inner ear from noise damage, particularly at low frequencies. In contrast, cholesteatoma formation in the middle ear can contact the ossicular chain, increasing the total mass, causing a predominantly high-frequency conductive hearing loss.

The middle ear is aerated through the eustachian tube to keep it at the same pressure as that of the ear canal. If the eustachian tube is blocked (eg, by edema of the nasopharynx secondary to allergy, adenoid hypertrophy, nasopharyngeal tumor, etc.), the middle ear pressure becomes lower than atmospheric pressure, pulling the tympanic membrane inward. As the tympanic membrane is richly innervated, this can be painful. The occasional opening of the eustachian tube, with a resultant change in middle ear pressure, can cause a patient to experience a popping sensation, pain, and a mild fluctuation in the sensation of hearing. If the tube becomes chronically blocked, a serous middle ear effusion with conductive hearing loss can develop.

Development

The inner ear begins at 3 weeks gestation as a thickening of the ectoderm on the side of the embryo. This otic placode invaginates to form the otic pit. It then pinches off and begins to enlarge, forming the otocyst. Beginning in weeks 5–6, the otocyst elongates and partitions itself into what will become six different sensory structures (three semicircular canals, two otolithic organs, and one cochlea) and the endolymphatic duct and sac (Figure 44–9). By 12 weeks, the formation of the membranous labyrinth is complete and the sensory cells have differentiated. By 16 weeks, cartilage has formed around the membranous labyrinth. By 23 weeks, this has undergone complete endochondral ossification to form the adult-size otic capsule. By 26 weeks, the human inner ear is sending auditory information to the brain.

Fluid Compartments

The inner ear is divided into two fluid-filled chambers, one inside the other (Figure 44–10). The fluid in the two chambers differs on the basis of the kind of salt that each contains. The fluid in the outer or bony chamber is filled with a sodium salt solution called perilymph, which resembles cerebrospinal fluid. The inner or membranous chamber is filled with a high potassium salt solution called endolymph, which resembles intracellular fluid. Marginal cells in the stria vascularis (see Figure 44–21) actively pump potassium into the membranous chamber to maintain the difference in the sodium and potassium concentrations. The difference in the chemical composition between perilymph and endolymph provides the electrochemical energy that powers the activities of the sensory cells. The inner ear is unique because the sensory cells rely on energy provided by other cells. In virtually all other systems, whether it is heart muscles, the brain, or the retina of the eye, the principal cells must combine nutrients and oxygen to produce the energy they use to perform their functions.

Hair Cell Function

Hair cells (Figure 44–11) are the sensory receptor cells of hearing and balance and are the most important cells in the inner ear. Their name derives from the fact that they have about 100 stereocilia at their apical end. Individual stereocilia are packed with a filamentous actin cytoskeleton. Hair cells are specialized mechanoreceptors that convert the mechanical stimuli associated with hearing and balance into neural information for transmission to the brain. The conversion of one type of energy to another is called transduction.

The stereocilia of each hair cell are arranged in a precise geometry. This arrangement is asymmetrical and polarized because the stereocilia are arranged in rows of short, intermediate, and tall stereocilia. A single kinocilium is located adjacent to the tallest row. It has a 9/2 microtubule organization similar to motile cilia found elsewhere in the body. The kinocilium is thought to establish the morphologic polarization of the stereocilia bundle and is not required for mechanoelectrical transduction. It is present in embryonic cochlear hair cells but is resorbed by the time cochlear hair cells mature.

There is a stepwise progression from the shortest row to the tallest row. The organization of the bundle from short to tall rows is related to the functional consequences of bending the bundle on the cell's membrane potential. The mechanoelectrical transduction channels that are in the stereocilia are tethered to adjacent stereocilia by “tip links” (see Figure 44–11). The deflection of the stereocilia toward the tallest row causes shearing between the stereocilia, which causes the tip links to pull on the transduction channels, opening them. Deflection in the other direction releases the tension of the tip link, causing the transduction channels to close. Bending the bundle in the direction of the tallest row leads to the entry of K+ and Ca2+ ions into the hair cell through channels that open at the tips of the stereocilia. This causes the hair cell to depolarize. Bending the bundle in the opposite direction promotes channel closure and results in hair cell hyperpolarization.

Within the stereociliary bundle, there is movement of the bundle back and forth parallel with the axis of symmetry through the kinocilium. Movement in this direction produces a maximal receptor potential (change in the intracellular voltage). As the bundle is moved at larger angles away from this axis, the receptor potential is reduced. In Figure 44–12, note that the receptor potential is asymmetric, with larger depolarizing swings compared with hyperpolarizing swings. This is because the current–voltage characteristics of the hair cell are nonlinear and are shaped by the various voltage- and calcium-dependent ion channels in its basolateral plasma membrane. The lowest tracing (see Figure 44–12) demonstrates that deflection of the stereociliary bundle perpendicular to the bundle's axis of symmetry produces no receptor potential.

Hair cells have synapses located at their basal pole. When a hair cell is mechanically stimulated, it releases a chemical that modulates the electric activity of the afferent neurons (Figure 44–13). This neurotransmitter release is regulated by changes in the membrane potential of the hair cell in response to bending its stereocilia bundle. Efferent synapses at the termination of the fibers originating in the brainstem are also present. The neural signals from the brain conveyed by these efferent fibers modulate the gain (amplification) of the hair cells they innervate.

The Organs of Hearing and Balance

The inner ear sensory epithelia are among the smallest organs in the body, containing less than 20,000 sensory cells. (By comparison, about 1 million photoreceptors are in the eye.) The inner ear organs must be small because any increase in their size would increase their mass. An increase in mass would increase the mechanical force required to stimulate them. Any increase in the driving force would represent a decrease in the sensitivity of the system (a hearing loss). The small number of cells in the hearing organ means that the loss of even a small number affects hearing.

Inner ear sensory organs differ in a way the stereocilia bundles of the hair cells are mechanically bent. The hair cells in each organ are grouped in one of three types of sensory epithelia. The maculae (Figures 44–14 and 44–15) and the cristae (Figure 44–16) are the sensory epithelium of the vestibular system (balance) and the organ of Corti (Figure 44–17) is the sensory epithelium of the cochlea. There are two maculae (the saccule and the utricle), three cristae, and one organ of Corti on each side of the head.

Anatomy & Physiology of the Vestibular Organs

The maculae (see Figure 44–15) of the otolithic organs are responsible for sensing gravity (linear acceleration). The maculae are flat, ovoid structures that are covered with hair cells across their surface. The stereocilia of the hair cells protrude upward and are embedded in the gelatinous otolithic membrane, which contains calcium carbonate crystals called otoconia. Otoconia have a density greater than water, so when the head is tilted from side to side, gravity causes a shearing force between the otolithic membrane and the surface of the maculae. This results in a bending of the stereocilia. Deflection toward the longer stereocilia causes the transduction channels to open and hair cell depolarization to occur. Deflection toward the shorter stereocilia causes the transduction channels to close and the cell to hyperpolarize.

The utricle and saccule take advantage of this bidirectional coding because there are hair cells oriented in both directions across their surface. In this way, a single macule can produce both excitatory and inhibitory signals with a change in the head position. The striola is defined as a thinning in the center of the otolithic membrane in the utricle and a thickening in that of the saccule (see Figure 44–15). This roughly defines the area on the sensory epithelium that divides hair cells oriented in one direction from those oriented in the opposite direction. Both the utricle and the saccule have a gently-curved shape. Two-dimensional information is able to be detected by a single otolithic organ because of the distributed orientation of the hair cell stereociliary bundles in all directions.

Hair cells have a mechanism for adjusting their set points, which is particularly important to the otolithic organs. When a steady-state head tilt occurs, hair cell stereocilia are deflected and a receptor potential occurs within the cell. However, over the next few seconds, the intracellular potential partially returns to normal levels, which is termed adaptation. It permits the hair cell to respond to further changes in the head position rather than resting unresponsively in a fully deflected position. Molecular motors within the stereocilia are thought to be activated in a manner that maintains an optimal tension in the tip links between adjacent stereocilia.

The ampullae (see Figure 44–16) of the semicircular canals are responsible for sensing head turning (angular acceleration). The semicircular canal ampulla contains the crista, which has a shape similar to a horse saddle. Hair cells lie on the surface of the crista. The stereocilia protrude upward off the surface of the crista and into a gelatinous material called the cupula. With a turn of the head, the inertia of the endolymph within the semicircular canal causes the cupula to move, deflecting the hair cell stereocilia and stimulating transduction. The three semicircular canals (lateral, superior, and posterior) are perpendicular to one another and thereby provide sensory signals from any type of head rotation.

Each semicircular canal is paired with one in a parallel plane on the opposite side of the head (see Figure 44–9). For instance, both lateral canals are in the same plane, the left posterior canal is in the same plane as the right superior canal, and the right posterior canal is in the same plane as the left superior canal. One vestibular organ gives an excitatory response, and the other vestibular organ gives an inhibitory response for rotation in a given plane. This paired input is then integrated by the brainstem to control balance. The kinocilia of the hair cells in the lateral semicircular canals are oriented toward the utricular side; therefore, the displacement of the cupula toward the vestibule provides an excitatory response (ampullopetal endolymph flow). In contrast, the kinocilia of the superior and posterior semicircular canals are oriented toward the canal side. Therefore, the displacement of the cupula toward the canal provides an excitatory response (ampullofugal endolymph flow).

Within the otolithic organs and the semicircular canals are two different types of hair cells, Type I and Type II (Figure 44–18). Physiologically, these cells act differently, although both are mechanoreceptor cells that transduce the head position and send this information to the brain.

Neurophysiology

Vestibular eighth nerve fibers project to the ipsilateral vestibular nuclei. The neural signals coming from the semicircular canals start the vestibuloocular reflex (Figure 44–19). The vestibuloocular reflex is critical to the ability to visually fixate on an object while one's head is turning. In contrast, keeping one's head still while trying to follow a moving target with the eyes is predominantly under cortical and cerebellar control. This is a much slower, multisynaptic, response compared with the three-neuron reflex arc of the vestibuloocular reflex.

An excitatory response from one semicircular canal results in an excitatory signal that crosses the midline of the brainstem via a second neuron to the contralateral abducens nucleus. The abducens nucleus then sends inputs via the sixth cranial nerve (the abducens nerve) to the lateral rectus muscle in the contralateral eye, causing the eye to deviate away from the side of the vestibular excitation. In addition, the abducens nucleus sends an excitatory input via the medial longitudinal fasciculus to the ipsilateral ocular motor nucleus. This controls the ipsilateral medial rectus muscle, causing the ipsilateral eye to deviate away from the side of the vestibular excitation. Because this input is paired, inhibitory signals from the other ear cause precisely the opposite response.

Balance is a complex interplay among input from the inner ear, the eyes, and musculature in the body and cervical spine. These signals are integrated in the brainstem, the cerebellum, and the cortex (Figure 44–20). The utricle and saccule send information regarding the head position to the brain and to the spinal cord, relaying changes in orientation to the antigravity musculature. These vestibulospinal reflexes are important for postural maintenance, equilibrium, and resting muscular tone. The cerebellum modulates these effects as well. The muscles responsible for postural control include the abdominal and paraspinal muscles around the hip, the hamstrings and quadriceps in the thigh, and the gastrocnemius and tibialis anterior in the calf. The vestibulospinal reflexes are carried by many distinct vestibulospinal tracts. The most important is the lateral vestibular spinal tract. Fibers within this tract cause a monosynaptic excitation of the ipsilateral extensors and disynaptic inhibition of contralateral extensors. Hence, a unilateral labyrinthine lesion causes increased contralateral extensor activation. For example, patients who have an acoustic neuroma and decreased vestibular input from one side tend to fall toward the side of the lesion because of the contralateral extensor activation.

The Cochlea

The cochlea achieves a greater mechanical sensitivity than the vestibular organs. The energy required for this process is provided by the stria vascularis (Figure 44–21). This structure forms the outer wall of the scala media and sits within the spiral ligament. It is highly vascular and metabolically active in order to maintain the high potassium concentration within the scala media. There are tight junctions between the apex of the hair cells and the surrounding supporting cells that form the barrier (the reticular lamina) between the endolymph and the perilymph. The stria vascularis acts as a battery whose electrical current powers hearing. In addition to elevated potassium concentrations, it creates a positive potential within the endolymph relative to the perilymph. This increases the electrochemical gradient that drives a constant flow of K+ ions from the endolymph into the hair cells. This “silent current” is modulated as hair cell stereocilia are deflected. Potassium ions are recycled back to the stria vascularis by diffusion through the perilymph and through supporting cells via gap junctions. The gap junction proteins are called connexins, and mutations of their genes result in sensorineural hearing loss. Connexin mutations are the most common mechanism of genetic hearing loss.

Passive Mechanics Within the Cochlea

The hair cells in the organ of Corti vibrate in response to sound. Differential movements between the basilar membrane and the tectorial membrane bend the stereocilia bundle (see Figure 44–17). In this figure, the flexible basilar membrane is anchored to the bony shelf on the left and a ligament (not shown) on the right. A single flask-shaped inner hair cell is shown on the left, and three rows of cylindrically shaped outer hair cells are seen on the right. The tips of the outer hair cell stereocilia are embedded in a gelatinous mass called the tectorial membrane, which lies on top of the organ of Corti. When sound is transmitted to the inner ear, the organ of Corti vibrates up and down. Since the basilar membrane is attached to bone and ligament at its two ends, the area of maximal vibration is near the third (furthest right) row of outer hair cells. The basilar membrane is fixed at the osseous spiral lamina, whereas the tectorial membrane is fixed at a different position. Movement of the basilar membrane up and down, induced by sound waves within the cochlear fluids, causes a shearing force to deflect the hair cell stereocilia.

The cochlea acts as both a passive and an active filter. Passive filtering produces a traveling wave in response to sound vibrations (Figure 44–22). The location of the peak of the traveling wave changes with the frequency of the sound played into the ear. The change in location results from the tonotopic organization of the organ of Corti. There are systematic differences in its mass and stiffness along its length that determine the frequency response at any specific location. At the base of the cochlea (the high-frequency region), it has a lower mass and a higher stiffness. In contrast, at the apex of the cochlea (the low-frequency region), the organ of Corti has a higher mass and a lower stiffness. Sound vibrations that enter the cochlea at the stapes footplate propagate along the length of the cochlear duct and are maximal when they match the characteristic frequency at a specific location.

Active Processes Within the Cochlea

Analyses of the cochlea based only on passive mechanical properties such as mass and stiffness cannot explain the exquisite frequency selectivity of human hearing or the frequency selectivity that is measured from individual auditory nerve fibers. The frequency selectivity of the cochlea is enhanced by an amplification mechanism within the cochlea. The amplification process generates sounds called otoacoustic emissions that can be measured with a sensitive microphone in the ear canal. They are routinely measured in the clinic to assess hearing. The outer hair cell is the amplifier. It elongates and shortens in response to the receptor potential generated by the stereocilia. This is called electromotility. The function of the outer hair cell in hearing is to refine the sensitivity and frequency selectivity of the mechanical vibrations of the cochlea.

Outer Hair Cells

Pressurization of the Outer Hair Cells

Most cells have a cytoskeleton to maintain cell shape. Because such an internal skeleton would impede electromotility, a central cytoskeleton is missing in the cylindrical portion of the outer hair cell, thereby improving the cell's flexibility. The outer hair cell must be more than flexible; it must also be strong enough to transmit force to the rest of the organ of Corti. As a result, outer hair cells are pressurized.

Most cells do not tolerate internal pressure because their membrane is weak. The outer hair cell plasma membrane is reinforced with a highly organized actin–spectrin cytoskeleton just underneath the plasma membrane (Figure 44–23). The shape of the outer hair cell is maintained by a pressurized fluid core that pushes against an elastic wall. The lateral wall of the outer hair cell is about 100 nm thick and contains the plasma membrane, the cytoskeleton, and an intracellular organelle called the subsurface cisternae. Particles sit within the plasma membrane and may be related to electromotility. The cytoskeleton consists of actin filaments that are oriented circumferentially around the cell and that are crosslinked by spectrin molecules. Pillar molecules tether the actin–spectrin network to the plasma membrane. The plasma membrane may be rippled between adjacent pillar molecules.

Electromotility of Outer Hair Cells

Outer hair cells have a cylindrical shape (Figure 44–24). They vary in length from approximately 12 μm at the basal or high-frequency end of the cochlea to >90 μm at the low-frequency end. Their diameter at all locations is approximately 9 μm. Their apical end is capped with a rigid cuticular plate into which the stereocilia are embedded, and their synaptic end is a hemisphere (compare with the typical hair cell shown in Figure 44–11).

Each of these three regions (flat apex, middle cylinder, and hemispheric base) has a specific function. The stereocilia at the apex of the cell are responsible for converting the mechanical energy of sound into electrical energy. Synaptic structures are found at the base of the hair cell and are responsible for converting electrical energy into chemical energy by modulating the release of neurotransmitters. The apex and the base of the outer hair cell perform functions that are common to all hair cells. The elongated cylindrical portion of the outer hair cell is where electrical energy is converted into mechanical energy. This function is unique to the outer hair cell. No other hair cell is able to change its length at acoustic frequencies in response to electrical stimulation. These length changes can be greater than 1% of the cell's original length if the electrical stimulation is large.

The electromotility of the outer hair cells is based on a novel membrane-based motor mechanism in the plasma membrane of the cells' lateral walls. The membrane protein prestin and intracellular chloride ions are required for the motor to work. The mechanical force generated by the membrane is communicated to the ends of the cell by means of an elegant cytoskeletal structure immediately adjacent to the plasma membrane (see Figure 44–23). This motor mechanism is a biological form of piezoelectricity similar to that used in sonar or ultrasound imaging. Both cochlear and vestibular hair cells from humans have similar properties to those of rodents, the animal models in which most research has been done.

Humans are able to discriminate between sounds that are very close in frequency because the outer hair cell acts as the cochlear amplifier. The role of the outer hair cell in hearing is both sensory and mechanical. When the organ of Corti begins to vibrate in response to the incoming sound, each hair cell senses the vibration through the bending of its stereocilia. The bending results in a change in the voltage within the outer hair cell, causing electromotility. If the resulting mechanical force is at the natural frequency of that portion of the cochlea, then the magnitude of the vibration increases. If the electromotile force is at a different frequency, the vibrations decrease. The intact system has greater sensitivity and frequency selectivity than when the outer hair cells are missing or damaged.

One consequence of having an active system is that oscillations can occur even when no energy is coming into the system from the outside. This happens in the cochlea, and the resulting sound vibrations can be measured in the ear canal. These are called spontaneous otoacoustic emissions and are observed only in living ears. Other types of otoacoustic emissions can be measured as well, including distortion product, otoacoustic emissions, and transient evoked otoacoustic emissions. These can be triggered as needed by playing certain types of sound stimuli into the ear and are therefore more useful clinically than the measurement of spontaneous otoacoustic emissions. Measuring otoacoustic emissions has become an important diagnostic tool for determining if outer hair cells are working, particularly in newborn hearing screening (see Chapter 45, Audiologic Testing).

Sensorineural hearing loss is a common clinical problem and has many possible causes, including noise exposure, ototoxicity, and age-related hearing loss (presbycusis). The common site of pathology for all of these conditions within the inner ear is the outer hair cell (see Figure 44–24). The attachments of outer hair cell stereocilia to the tectorial membrane can be broken, even with mild noise exposure. This reduces the ability of outer hair cell electromotility to provide a positive feedback, leading to a temporary hearing loss. With further damage, the actin core of the outer hair cell stereocilia can fracture. With enough trauma, hair cell death occurs and a permanent hearing loss results because mammalian cochlear hair cells do not regenerate. After outer hair cells begin to degenerate, further structures within the cochlea die as well, including inner hair cells, supporting cells, and auditory nerve cells.

A low level of trauma that produces disarray of both inner and outer hair cell stereocilia proportionally elevates eighth nerve tuning curve thresholds (Figure 44–25A). When outer hair cells are lost, only the sharp peak of the tuning curve is lost (Figure 44–25B and D). Loss of inner hair cells produces a dramatic elevation in tuning curve thresholds (Figure 44–25C). Outer hair cell damage blocks the cochlear amplifier, but the passive tuning properties of the cochlea are retained. In contrast, inner hair cell damage reduces cochlear function overall. In summary, outer hair cells are responsible for the cochlear amplifier, whereas inner hair cells provide afferent input.

Input from both cochleae are integrated, and the acoustic environment is reconstructed in the brainstem and auditory cortex. This begins with the conversion of mechanical vibrations of the organ of Corti into changes of inner hair cell membrane potentials. Synaptic transmission to the afferent eighth nerve fibers (the auditory nerve) modulates the ongoing action potential discharge of the fiber. As a result of the faithful link between basilar membrane mechanics and the afferent fiber, each auditory nerve fiber is tuned to a particular characteristic frequency (see Figure 44–25). In this way, the central nervous system knows that there is energy at that specific frequency entering the ear.

Auditory brainstem-evoked response (ABR) is a clinical test to verify that the pathway from the cochlea to the midbrain is intact. Electrodes placed on the scalp (similar to those used with an electroencephalogram) can measure the electrical signals being relayed from the cochlea to the auditory cortex. By playing a “click” into the ear, a large number of auditory nerve fibers are excited simultaneously. This is called the compound action potential, and is Wave 1 of the ABR (see Chapter 45, Audiologic Testing). ABR Waves 2, 3, 4, and 5 represent the sequential activation of neurons as the signal is passed up the brainstem (distal auditory nerve, cochlear nucleus, superior olivary complex, and lateral lemniscus). Each wave should occur within a certain timeframe after the previous wave. If delayed, a conduction block can be diagnosed, which may represent brainstem pathology. The most common conduction delays are measured between Waves 1 and 3 and Waves 1 and 5, which may suggest the presence of an acoustic neuroma that is slowing conduction along the eighth cranial nerve. Many other types of pathology, including other cerebellopontine angle tumors, multiple sclerosis, chronic meningitis, and brainstem malformation, need to be included in the differential diagnosis. In most instances, an abnormal ABR indicates the need to order an MRI with and without gadolinium contrast to evaluate for retrocochlear pathology.

In all sensory systems, an important part of the neural code is determined by what location of the sensory organ is stimulated. In the case of the eye, a spot of light falls on a few photoreceptors and they excite nerves that map a representation of the visual world in the brain. In the ear, the acoustic world is coded by a one-dimensional representation of frequency. This frequency map then projects to the brain, which reconstructs the three-dimensional acoustic “world”. Parts of the auditory cortex contain a true three-dimensional representation of the outer world so that the sound of a twig snapping behind an individual excites nerve cells in one location while a twig snapping on the right of an individual excites nerve cells in another spatially precise location. The analysis of speech appears to take place in parts of the brain that are highly developed only in humans. The amazing machinery that accomplishes the reconstruction of the acoustic world relies on the delicate structures of the inner ear that deconstruct the original sounds.