141

ANATOMY AND PHISIOLOGY OF HEARING

This chapter provides a brief summary of the most basic features of the anatomy and physiology of the ear. It is divided into sections on the external and middle ear, cochlea, and central nervous system (CNS). The focus is on the anatomic and physiologic bases of audition with an effort directed at functional features. Surgical anatomy, vasculature, and eustachian tube function are not discussed.

EXTERNAL EAR

The external ear consists of the pinna (auricle) and the external auditory canal (EAC) from the meatus to the tympanic membrane (Fig. 141.1). The pinna of humans is composed mostly of cartilage and has no useful muscles. The center of the pinna, the concha, leads to the external auditory meatus, which is about 2.5 cm long. The lateral third of the canal is the cartilaginous portion. It contains cerumen-producing glands and hair follicles. The remaining medial two-thirds is the bony portion, including an epithelial lining over the tympanic membrane (1).

The external ear and the head have a passive but important role in hearing because of their acoustic properties. The concha, or bowl of the auricle, has a resonance of about 5 kHz, and the irregular surface of the pinna introduces other resonances and antiresonances. These acoustic features are useful to help differentiate whether sound sources are in front of the listener or behind.

The EAC is essentially a tube that is open at one end and dosed at the other; thus, the EAC behaves like a quarter-wave resonator. The resonant frequency (f0) is determined by the length of the tube; the curvature of the tube is irrelevant. For a tube of 2.5 cm, the resonant frequency is approximately 3.5 kHz:

f0 = Velocity of sound @ 350 m/s/(4 x2.5 cm)

A flat, wide-band sound measured in a sound field is changed considerably by the acoustic properties of the head and external ear. As Figure 141.2 demonstrates, a gain of about 15 dB occurs in the 3-kl-Iz range of the human, cat, and chinchilla, and 10 dB between 2 and 5 kHz. The acoustic properties of the external ear are one of the reasons noise-induced hearing losses occur first and most prominently at the 4-kHz frequency region (boilermaker notch).

In addition to the prominence of noise-induced hearing loss in the 4-kHz region, the acoustic properties of the head and external ear have an important role in several hearing functions. In localization of sound sources, the head acts as an attenuator at frequencies at which the width of the head is greater than the wavelength of the sound. Thus at frequencies greater than 2 kHz, a head shadow effect occurs, in which interaural intensity differences of 5 to 15 dB are used to localize sound sources. At lower frequencies, at which the wavelength of the sound is larger than the width of the head, little attenuation is provided by the head. Interaural time differences (0.6 ms for sound to travel across the head) are the salient cues for localization. The head-shadow effect is the reason right-handed hunters using rifles and shotguns have larger hearing losses in their left ears than in their right ears and vice versa. The muzzle of the gun, where the acoustic energy is greatest, is doser to the left ear, and the right ear is protected by the head- shadow effect.

The 10- to l5-dB gain provided by the external ear in the 3- to 5-kHz region is useful for improving the detection and recognition of low-energy, high-frequency sounds such as voiceless fricatives. The importance of the acoustic properties of the external ear and head is reflected in hearing-aid design and evaluations. Finally, the resonance of the external canal is approximately 8 kHz in infants and decreases to adult values after approximately 2.5 years of age. This developmental feature has several clinical implications, especially for sound-field testing and for hearing- aid design and evaluation of infants.

MIDDLE EAR

The middle ear transmits acoustic energy from the air-filled EAC to the fluid-filled cochlea. It functions as an impedance-matching device inasmuch as it couples the low impedance of air to the high impedance of the fluid-filled cochlea. The impedance match is achieved in three ways. The first and most important factor is that the effective vibratory area of the tympanic membrane is approximately 17 to 20 times greater than the effective vibratory area of the stapes footplate (Fig. 141.3). A second factor involves the lever action of the ossicular chain. The arm of the long process of the incus is shorter, by a factor of 1.3, than the length of the manubrium and neck of the malleus. A third and minor factor is the shape of the tympanic membrane. The combined result of these three factors is a pressure gain of approximately 25 to 30 dB. The variance in published measurements of the transformer ratio is noteworthy. With the exception of studies of acoustic impedance of the ear, most data are from studies of human cadavers, with all of their shortcomings, or of animals, usually cats. In addition to its role in the transfer of power to the inner ear, the tympanic membrane protects the middle ear space from foreign material of the ear canal and maintains the air cushion that prevents insufflations of foreign material from the nasopharynx though the eustachian tube.

The vibratory behavior of the ossicular chain is described in Figure 141.3. The transformer action of the tympanic membrane and ossicular chain provides for relatively efficient transfer of power to the inner ear, and the fidelity of sound transmission across the middle ear is outstanding. Distortion of sound signals does not occur in the middle ear, even for input signals with sound levels greater than 130 dB sound pressure level (SPL).

The middle ear, including the tympanic membrane, ossicular chain with supporting ligaments, and middle ear space, can be viewed as a passive mechanical system with both mass and compliant elements and therefore resonant properties. This linear system is coupled to the cochlea, which contributes a large resistance. The result is a middle ear system that is highly damped and linear and has a wide frequency response. The inputoutput function or transfer function of the middle ear is shown in Figure 141.4A. The ratio of the volume velocity of the stapes to sound pressure at the tympanic membrane increases in humans to approximately 800 to 900 Hz, which is the resonant frequency of the middle ear, and decreases at higher frequencies. Phase shift or time lag between movement of the tympanic membrane and the stapes generally increases with frequency (Fig. 141.4B). Although the middle ear is an impressive system in terms of frequency response, linearity, and transformer properties, considerably less than half of the power entering the middle ear actually reaches the cochlea because of the absorption of energy by the ligaments and middle ear. As shown in Figure 141.5, the human middle ear is particularly inefficient at frequencies greater than 2 kHz, especially in comparison with the ears of cats and chinchillas. It also is important to recall that a 50% loss of power is a loss of only 3 dB.

Auditory function is profoundly affected by cochlear impedance as well as the combined acoustic effects of the head, external ear, and middle ear. The combined effects of the acoustic properties of the head, external ear, and middle ear, as well the input impedance of the cochlea, have a profound effect on auditory function. For example, these factors determine the shape of the audibility curve and therefore the frequency range of human hearing (Fig. 141.6). For example, humans do not detect and recognize sounds greater than approximately 20 kHz because such high-frequency sounds are not transmitted efficiently through the middle ear to the cochlea. A second example of this sound transformation is shown in Figure 141.7, in which the spectrum of a cannon measured in a sound field is compared with the spectrum by the time it is transformed and shaped by the acoustic properties of the eternal cal; head, middle ear, and input impedance of the cochlea. Low-frequency energy is not transmitted to the cochlea, and the frequency region of greatest energy concentration is 3 to 4 kHz. Thus, these acoustic properties are primarily responsible for the ability of intense low- frequency sounds (measured in a sound field) to produce high-frequency hearing losses and injuries in the basal region of the cochlea.

Two striated muscles, the tensor tympani and the stapedius, are located in the middle ear. The former attaches to the malleus and is innervated by the trigeminal nerve. The stapedius muscle attaches to the stapes and is innervated by the stapedial branch of the facial nerve. Noticeably the stapedius and tensor tympani muscles are the smallest striated muscles in the body and also have a high innervation ratio, that is, nerve fibers per muscle fiber. Although no question remains that contraction of these muscles affects sound transmission through the middle ear, the details of the effect and the extent of the influence of the middle ear muscles are still not fully understood. A number of disparate functions have been attributed to the middle ear muscles.

One function of the middle ear muscles is to protect the cochlea from loud sounds (2). When sounds louder than approximately 80 dB SPL are presented monaurally or binaurally, consensual (bilateral) reflex contraction of the stapedius muscle occurs. This contraction increases the stiffness of the acicular chain and tympanic membrane, attenuating sounds less than approximately 2 kHz. Although the tensor tympani contracts as part of a startle response, acoustic reflex data from human subjects with neurologic involvement of cranial nerves V and VII suggest that the tensor tympani does not normally respond to intense acoustic stimulation. Laboratory and field studies of noise-induced hearing loss have shown convincingly that the stapedial reflex protects the cochlea, particularly from low-frequency ( 100 dB SPL), the auditory system must have neurons the thresholds of which cover a wide range and have firing rates that also cover a wide range of intensities. The ability of the human ear to respond appropriately to sounds over a 120-dB range (10,13) is remarkable. One way is with low-spontaneous fibers; another is recruitment of fibers of characteristic frequency.

One of the most common features of sensorineural hearing loss is recruitment of loudness. Figure 141.20 gives an explanation. It is assumed that loudness depends on the total activity of the auditory nerve. As Figure 141.20A shows, the number of fibers activated increases slowly as intensity is increased, and only the tips of the tuning curves are activated. As the intensity increases further, the tails of the tuning curves are encountered, and the number of fibers activated increases rapidly. In the case of sensorineural hearing loss, the tips of the tuning curves are missing. and the fibers are not activated until the level of the signal is sufficient to reach the tails of the tuning curves. Abruptly, many fibers then are abruptly activated simultaneously.

NONLINEAR PROPERTIES OF THE EAR

Some of the outstanding features of the middle ear transformer are its linear properties, but the outstanding features of the cochlea and auditory nerve are the nonlinear characteristics. Perhaps the most studied nonlinearilies are combination tones, described herein in relation to cochlear emissions, and two-tone rate suppression, as recorded in auditory nerve fibers.

Two-tone rate suppression is the reduction in firing rate produced by one tone when a second tone is introduced. Figure 141.21 shows a tuning curve with a suppression area outlined above the characteristic frequency of the nerve fiber and an area below the characteristic frequency of the fiber. Tones presented in the dotted or suppression areas in the figure reduce the firing rate caused by the probe tone. Both the excitor and suppressor tones are presented simultaneously, and because little or no time lag is associated with this phenomenon nor is any evidence available that it is neurally produced, the effect is called suppression rather than inhibition. Two-tone suppression in single units is reflected in the compound action potential. Figure 141 21 (right) shows tuning curves of the compound action potential with suppression areas shown in the dotted areas. In this case, the amplitude of the compound action potential is altered by the suppressing signal, whereas in the single- unit case (left), the firing rate of a neuron is reduced by an arbitrary amount (20%). The single-unit and compound action potential suppression areas are similar. Inasmuch as two-tone suppression can be observed in the DC intracellular response of inner hair cells, it is probable that two-tone suppression originates in the active nature of cochlear mechanics and before the inner hair cells.

In the presence of sensorineural hearing loss caused by exposure to noise or to ototoxic drugs, two-tone rate suppression is severely affected, if at all measurable. Two-tone rate suppression appears normal or nearly so in cases of cochlear hearing loss in which the sensory cells, including stereocilia, are normal or nearly so, but in the stria vascularis is affected. The latter scenario leads to presbycusis (17).

Otoacoustic emissions (OAEs) are sounds that are detected in the ear canal when the tympanum receives vibrations transmitted through the middle ear from the cochlea. OAEs provide support for the notion that the cochlea is riot just a passive receiver of acoustic energy but can also generate or amplify sounds. Several different types of OAEs are found (18). Spontaneous OAEs occur in the absence of acoustic stimulation and are typically highly stable pure tones of 10 to 30 dB SPL, which are found in 30% to 40% of healthy young ears (19,20). The precise frequency of a spontaneous OAE does not imply an origin at a precise place in the cochlea, but only a particular coincidence of travel time and reflection from an ill-defined region of high outer cell activity. Spontaneous OAEs can be recorded over long periods with only minor but seemingly systematic variations in frequency and amplitude.

A second class of OAEs are produced after exposure to an acoustic signal. Transient-evoked OAEs (TEOAE) are made via a probe placed in the ear canal. The oscillatory sound pressure waveform seen in TEOAE responses actually corresponds to the motion of the eardrum resulting from pressure fluctuations generated within the cochlea (Fig. 141 .22). Although stimulatory clicks excite the entire cochlea, TEOAE responses can be used to give frequency-specific information about the cochlea through splitting of the responses into different frequency bands. TEOAEs are highly sensitive to cochlear pathology in frequency-specific manner. Frequencies at which hearing thresholds exceed 20 to 30 dB hearing loss (HL) are typically absent in the TEOAE response (21,22). Because of their sensitivity to cochlear dysfunction, TEOAEs have found widespread application in newborn hearing screening programs (23).

Distortion-product OAEs also are used widely in clinical situations. The TEOAE and DPOAE techniques complement each other. DPOAEs offer a wider frequency range of observation with less sensitivity to minor and subclinical conditions in adults. When two primary tones, F1 and F2, are presented to the cochlea, several distortion products are produced. The most prominent of all these intermodulation distortion products is the cubic distortion tone, 2F1-.F2. Measurement of DPOAEs at multiple stimulus levels can establish the OAE growth rate. Healthy ears tend to exhibit a DPOAE growth rate of 1 dB of OAE per 1 dB of stimulus or less. Ears with some impairment show steeper growth. Single DPOAE results can be misleading, and results must be averaged across a range of frequencies. The DPOAE is easily recordable in patients with a normal middle ear system (24,25).

AUDITORY CENTRAL NERVOUS SYSTEM

The ascending and descending auditory pathways are described briefly herein in relation to auditory evoked potentials. Schematics of the afferent and efferent pathways are shown in Figures 141.13 and 141.23, respectively. These diagrams oversimplify the system but provide a rough introduction to the auditory CNS and its complexity. All eighth-nerve afferent fibers stop at the level of the cochlear nucleus. Five major cell types are found within the cochlear nucleus, each with distinct morphologic and physiologic features, such as response to stimulus onset, stimulus offset, and frequency modulation. From the cochlear nucleus, most fibers cross the brainstem to the contralateral superior olivary complex; a much smaller number of fibers run to the ipsilateral superior olivary complex.

The superior olivary complex is considered the first center in the ascending auditory system, where inputs from both ears converge. Auditory nuclei above the superior oh- vary complex can be excitatory or inhibitory with inputs from each ear. Stimulation of the contralateral ear typically is excitatory to cell bodies of the auditory CNS, whereas stimulation of the ipsilateral ear is inhibitory. As shown in Figure 141.13, the medial superior olivary complex is the origin of the crossed efferent fibers that terminate on outer hair cells, whereas the lateral superior olivary complex is the origin for the uncrossed efferent fibers that terminate on inner hair cells. Although many functions have been attributed to the efferent auditory system, especially protecting the cochlea from loud sounds, the functions of the system are unknown; those that have been proposed are easily debated (26,27).

The inferior colliculus is a complex nucleus with at least 18 major cell types and at least five areas of specialization. It is involved in probably all forms of auditory behavior, including differential sensitivity for frequency and intensity, loudness, and binaural hearing. The inferior colliculus is dearly more than a relay center. The medial geniculate body of the thalamus sends projections to the auditory cortex, but its specific functions are unknown.

The auditory cortex is located in the sylvian fissure of the temporal lobe; many secondary auditory areas are clustered around the primary area. In each area, the cells are tonotopically organized in a columnar manner, each column having a special attribute. The cells in one column can have different tuning at a similar characteristic frequency, whereas another column can be associated with intensity encoding, another with providing inhibitory responses to stimulation of one ear and excitatory responses of the other ear, and so on. As is common for thalamic connections with the cortex, nuclei within the medial gerticulate body that send fibers to the auditory cortex also receive fibers from the same area of the cortex. Bilateral lesions of the temporal lobe have been shown to produce wide-ranging effects (cortical deafness, in which several auditory behaviors are severely affected, including speech discrimination, localization of sound, temporal processing of information, and the detection of faint, short duration signals) (28). Another important feature of the auditory system is its tonotopic nature. From the basilar membrane to the auditory cortex, the system is organized spatially with respect to frequency. Each place on the basilar membrane responds best to a specific frequency high-frequency sounds are localized to the base, and low- frequency sounds, to the apex. The tonotopic organization of the cochlea is preserved at the cochlear nucleus. Figure 141.24 shows that as an electrode penetrates the cochlear nucleus, fibers with different characteristic frequencies are contacted, and the characteristic frequencies form an orderly progression. Similar data exist at all nuclei of the auditory CNS, including the auditory cortex.

The most obvious clinical application of basic information on the auditory CNS involves interpretation of evoked potentials. The auditory brainstem response (ABR) is one component of auditory evoked potentials. The existence of the ABR was first reported by Sohmer and Feinmesser in 1967 (29). The ABR is recorded from electrodes attached to various positions on the head. The ABR consists of a series of seven waves occurring within about 10 milliseconds after stimulus onset. The convention in the United States is to label wave peaks with Roman numerals, It is generally accepted that the ABR is generated by the auditory nerve and subsequent fiber tracts and nuclei within the auditory brainstem pathways. It is widely believed that each wave is generated as follows: wave I and II are the eighth nerve, Ill is cochhear nucleus, IV is superior olive/lateral leminiscus, and V is lateral leminiscus/inferior colliculus.

The ABR is generated by a dick stimulus because it yields the clearest response. The ABR is used clinically both in the estimation of auditory sensitivity and in otoneurologic assessment. In this way, it can be used to detect lesions along the auditory nerve and brainstem pathways. The study can be performed regardless of state of wakefulness, and the result is unaffected by most medications. As a result, children are often tested while under sedation or during sleep.

The field of clinical objective audiometry has recently gained an additional technique in the auditory evoked response battery. The auditory steady-slate response (ASSR) promises to be a valuable study in the workup of auditory dysfunction. Unlike ABRS, which are obtained through the use of transient stimuli, ASSRs are evoked by using sustained continuous tones. The tones are frequency specific because the continuous tones do not have spectral distortion problems as do brief tone bursts or click (30,31). Of note, ASSR also can be performed regardless of the state of wakefulness.

There are several advantages of ASSR over ABR. First, ASSR is a better technique for evaluating hearing aid performance because hearing aids and cochlear implants process continuous stimuli with less signal distortion than transient stimuli. Furthermore, ASSR can provide threshold information in a frequency specific manner at intensity levels of 120 dB or greater (32,33). This allows differentiation of severe and profound hearing loss, which cannot be accomplished with ABR. This characteristic of ASSR may allow it to be used in assessing pediatric patients for cochlear implant candidacy (34). Last, ASSR has been shown to be more time efficient by determining more thresholds in a shorter time compared with ABR (3537). Future research and clinical use are likely to solidify the status of ASSR in the audiologic armamentarium.

The neuroanatomic features of the system are complicated. Processing of neural information probably involves both parallel and serial processing. The former is anatomically described by a single fiber with ramifications to many target areas. Serial processing involves a fiber going to one target, which in turn goes to another target, and so forth. In the auditory CNS, both serial and parallel processing are involved. Because the auditory CNS is a highly redundant, complicated, and extremely powerful system, interpretation of evoked-potential data, and of other CNS neural data, is not straightforward.

HIGHLIGHTS

The acoustic properties of the head and external ear are important, particularly because they provide cues for localizing sources of sound.

The middle ear acts as a transformer between air and the fluid-filled cochlea and provides a sound pressure gain of 25 to 30 dB. The combined effect of the acoustic properties of the head, external ear, and middle ear, and the input impedance of the cochlea determine the frequency range of human hearing.

The cochlea is a coiled bony tube approximately 35 mm long and divided into three compartmentsthe scala tympani, scala vestibuli, and scala media. The scalae tympani and vestibuli contain perilymph and are connected through the helicotrema at the apex of the cochlea. The scala media contains endolymph and has a positive DC resting potential of approximately 80 mV, which arises from Na -K-ATPase pumps in the stria vascularis.

The auditory transducer is the organ of Corti, which contains sensory cells (three rows of outer hair cells and one row of inner hair cells). Deflection of stereoduia (hairs) of the sensory cells by a mechanical traveling wave starts transduction.

A traveling wave, from the base toward the apex of the cochlea, arises in response to piston-like movement of the stapes. The traveling wave has a sharply tuned peak at the base for high-frequency sound that progresses toward the apex as frequency decreases.

Deflection of stereocilia by the traveling wave opens and doses ion channels; the result is current flow (potassium ion) into the sensory cell. The potassium flux arises from the +80 mV endocochlear potential added to the negative intracellular potential of inner and outer hair cells. The resulting depolarization causes an enzyme cascade that releases chemical transmitters and activates afferent nerve fibers.

Approximately 90% to 95% of the radial nerve fibers (type I) innervate inner hair cells. Approximately 5% to 10% (type II, outer spiral fibers) are connected to outer hair cells. Each inner hair cell is innervated by 15 to 20 type I neurons. Each type II neuron branches to innervate approximately 10 outer hair cells. Approximately 1,800 efferent fibers project to the sensory cells from the ipsilateral and contralateral superior olivasy complexes.

The most basic measure of auditory nerve function is the tuning curve of a single auditory nerve fiber. Tuning curves of single fibers of the nerve are strikingly similar to tuning curves of the mechanical traveling wave, Injury to sensory cells and stereocilia alters the features of tuning curves, including sensitivity and sharp tuning.

The middle ear system is passive and linear in response to signals as great as 130 dB SPL, but the inner ear is an active system with its own amplifier and is nonlinear. These properties allow the inner ear to respond to a wide range of intensities and provide the basis for suppression phenomena.

Although the efferent auditory system is well developed, the functional significance is not well understood. It may have a role in the cochlear transduction and in protecting the cochlea from overexposure to intense sound.