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Hearing Basics


Hearing loss comprises reduced sensitivity for pure tones (the audiogram) and problems in the understanding of speech. The loss of sensitivity results from deficits in the transmission of sound via the middle ear and/or loss of transduction of mechanical vibrations into electrical nerve activity in the inner ear. Problems of speech understanding mainly result from deficits in the synchronization of auditory nerve fibers’ (ANFs) and central nervous system activity. This can be the result of problems in the auditory periphery but may also occur in the presence of nearly normal audiometric hearing. In order to appreciate the interaction of the audibility and “understanding” aspects of hearing loss, I will, besides presenting a condensed review of the auditory system, pay detailed attention to new findings pertaining to the important role of the ribbon synapses in the inner hair cells (IHCs), parallel processing in the ascending auditory system, and finally the importance of the efferent system.

1.1

Hearing Sensitivity in the Animal Kingdom

Every animal that grunts, croaks, whistles, sings, barks, meows, or speaks can hear. Most of the hearing animal species that we are familiar with are vertebrates, however insects also have keen hearing. For cicades and crickets that come as no surprise as these form choruses to enliven our nights. It may also turn out that the humble fruit fly, Drosophila , whose song is barely audible ( ), and the favorite of geneticists, may become important to elucidate the genetics of hearing loss ( ).

A common way to quantify the hearing sensitivity (or loss) in humans is by way of the audiogram—a plot of the threshold level of hearing at a fixed series of (typically octave-spaced) frequencies between 125 Hz and 8 kHz when used in a clinical setting. In research settings, a wider and more finely spaced range of frequencies is employed ( Fig. 1.1 ). In research settings, the just audible sound pressure level (dB SPL) is plotted, whereas in clinical settings the loss of sensitivity relative to a normalized value is represented (dB HL). To avoid confusion we call the research representation the “hearing field.”

Figure 1.1, Representative hearing fields from the five vertebrate classes: hardhead catfish, bullfrog, sparrow, cat, bobtail skink, and human.

As Fig. 1.1 shows, hearing sensitivity differs considerably between vertebrates, even between mammals. Small mammals often have better high-frequency hearing than humans, with the 60 dB SPL upper limits of the hearing field ranging from 34.5 kHz for the Japanese macaque, and about 60 kHz for the cat to more than 120 kHz for the horseshoe bat ( ). One reason for this variation may be that small mammals need to hear higher frequencies than larger mammals do in order to make use of sound localization cues provided by the frequency-dependent attenuating effect of the head and pinnae on sound. As a result, mammals with small heads generally have better high-frequency hearing than mammals with large heads, such as the elephant. Almost all mammals have poorer low-frequency hearing than humans, with the 60 dB lower limits ranging from 28 Hz for the Japanese macaque to 2.3 kHz for the domestic mouse ( ; not shown). Only the Indian elephant, with a 60-dB low-frequency limit of 17 Hz, is known to have significantly better low-frequency hearing than humans, reaching into the infrasound range ( ).

Birds are among the most vocal vertebrates and have excellent hearing sensitivity. However, a striking feature of bird hearing is that the high-frequency limit, which falls between 6 and 12 kHz—even for small birds—is well below those of most mammals, including humans. Fig. 1.1 shows a typical bird audiogram represented by the sparrow. Among reptiles, lizards such as the bobtail skink ( Fig. 1.1 ) are the best hearing species and are up to 30 dB more sensitive than alligators and crocodiles.

Anurans (frogs and toads) are very vocal amphibians: In specific parts of the year, depending on the species, their behavior is dominated by sound. As I wrote earlier ( ): “Sound guides toads and frogs to breeding sites, sound is used to advertise the presence of males to other males by territorial calls, and sound makes the male position known to females through mating or advertisement calls. To have the desired effect these calls must be identified as well as localized. Frogs and toads are remarkably good in localizing conspecific males, especially when we take into account their small head size and the fact that hardly any of the territorial or mating calls has sufficient energy in the frequency region above 5 kHz to be audible at some distance.” Especially, the bullfrog’s threshold is relatively low at 10 dB SPL around 600 Hz ( Fig. 1.1 ).

Teleost fishes, the largest group of living vertebrates, include both vocal and nonvocal species. This is especially evident for some by their intense sound production during the breeding season ( ). Except for the hardhead catfish ( Fig. 1.1 ) that hears sounds at approximately 20 dB SPL for 200 Hz, most fishes have thresholds around 40 dB SPL, and with few exceptions do not hear sounds above 2 kHz ( ).

Nearly all insects have high-frequency hearing ( ). For instance, the hearing ranges for crickets are 0.1–60 kHz, for grasshoppers 0.2–50 kHz, for flies 1–40 kHz, and for cicades 0.1–25 kHz. Tiger moths are typically most sensitive to ultrasound frequencies between 30 and 50 kHz. The frequency sensitivity of the ears of moth species is often matched to the sonar emitted by the bats preying upon them ( ).

1.2

The Mammalian Middle Ear

“The auditory periphery of mammals is one of the most remarkable examples of a biomechanical system. It is highly evolved, with tremendous mechanical complexity” ( ).

Transmission of sound energy from air to fluid typically results in considerable loss as a result of reflection from the fluid surface and estimated at about 99.7% of the incoming energy. This is compensated by the pressure gain provided by the ratio of the areas of the tympanic membrane (TM) (typical 0.55 cm 2 ) and the stapes footplate (typical 0.032 cm 2 ) for human, which is approximately 17, and the lever action of the middle ear bones which contributes a factor approximately 1.3 ( ). This would theoretically result in a combined gain of a factor 22 (about 27 dB). In practice, the gain is considerably less and maximal between 20 and 25 dB in the 800–1500 Hz range ( ).

extensively described the middle ear action as the result of two mechanisms: ossicular and acoustic coupling. Ossicular coupling incorporates the gain in sound pressure that occurs through the TM and ossicular chain. In the normal middle ear, sound pressure in the ear canal results in TM motion transmitted through the malleus and incus to produce a force at the stapes head ( Fig. 1.2 ). This force applied over the area of the footplate produces a pressure P S . P S represents the ossicular coupling of sound to the cochlea. Acoustic coupling refers to the difference in sound pressures acting directly on the oval window (OW), P OW , and round window (RW), P RW . In normal ears, acoustic coupling, Δ P =( P OW −P RW ), is negligibly small, but it can play a significant role in some diseased middle ears ( ).

Figure 1.2, Illustration of ossicular and acoustic coupling from ambient sound to the cochlea. In the normal middle ear, sound pressure in the ear canal results in TM motion transmitted through the malleus and incus to produce a force at the stapes head ( red path). This force applied over the area of the footplate produces a pressure P S . P S represents the ossicular coupling of sound to the cochlea. TM motion also compresses and dilates the air in the middle ear cavity, creating sound pressure in the middle ear ( blue paths), which just outside the OW equals ( P OW ) and at the RW ( P RW ). The difference between these two acoustic pressures, Δ P = P OW − P RW represents the acoustic coupling of sound to the cochlea. In the normal ear, this acoustic coupling is negligibly small.

1.3

The Mammalian Inner Ear

Until 1971, the basilar membrane (BM) was considered to be a linear device with broad mechanical tuning, as originally found already in the 1940s by . The bridge to the narrow ANF tuning was even long thereafter considered the result of a “second filter” ( ). Thus, it took a while before the results from indicating that the BM was a sharply tuned nonlinear filtering device were accepted. Appreciating these dramatic changes in viewing the working of the cochlea, wrote: “We are in the midst of a major breakthrough in auditory physiology. Recent experiments force us, I believe, to accept a revolutionary new hypothesis concerning the action of the cochlea namely, that an active process increases the vibration of the basilar membrane by energy provided somehow in the organ of Corti.” Then, another crucial discovery was that the outer hair cells (OHCs), in response to depolarization, were capable of producing a mechanical force on the BM ( ) later called the “cochlear amplifier,” but this is in essence the “second filter.”

1.3.1

Basilar Membrane Mechanics

The BM presents the first level of frequency analysis in the cochlea because of its changing stiffness and mass from base to apex. High-frequency sound produces maximal BM movement at the “base” of the cochlea (near the stapes) whereas low-frequency sound also activates the apical parts of the BM. Thus each site on the BM has a characteristic frequency (CF), to which it responds maximally in a strict tonotopic order ( ). BM movements produce motion of hair cell stereocilia, which open and close transduction channels therein. This results in the generation of hair cell receptor potentials and the excitation of ANFs.

In a normal ear the movement of the BM is nonlinear, i.e., the amplitude of its movement is not proportional to the SPL of the sound, but increases proportionally less for increments in higher SPLs. In a deaf ear, the BM movement is called passive (Békésy-labeled wave and envelope in Fig. 1.3 ) as it just reacts to the SPL, without cochlear amplification. proposed a model for the activation of IHCs that combined a passive BM movement and an active one resulting from the action of a cochlear amplifier. The passive BM movement only activates the IHCs at levels of approximately 40 dB above normal hearing threshold ( ). At lower sound levels and up to about 60 dB above threshold, the cochlear amplifier provides a mechanical amplification of BM movement in a narrow segment of the BM near the apical end of the passive traveling wave envelope ( Fig. 1.3 ). The OHC motor action provides this amplification. noted that both the classical high-intensity system and the active low-level cochlear amplifier system compress the large dynamic range of hearing into a much narrower range of mechanical movement of BM and consequently the cilia of the IHCs. found that the high sensitivity and sharp-frequency tuning, as well as compression and other nonlinearities (two-tone suppression and intermodulation distortion), are highly labile, suggesting the action of a vulnerable cochlear amplifier. underestimated the effect of the cochlear amplifier considerably ( Fig. 1.3 ) as the next section shows.

Figure 1.3, A traveling wave, as described by von Békésy (1960) , is shown by the dashed line and its envelope by the heavy full line. The wave travels from right (base) to left (apex). The form of the envelope and the phase relations of the traveling wave are approximately those given by von Békésy (1960) . To the envelope is added, near its left end, the effect of the cochlear amplifier. A tone of 2000 Hz thereby adds a peak at about 14 mm from the (human) stapes. The peak corresponds to the “tip” of the tuning curve for CF=2000 Hz.

1.3.2

The Cochlear Amplifier

Because of the high-frequency selectivity of the auditory system, predicted that active feedback mechanisms must amplify passive BM movements induced by sound in a frequency-selective way. This active cochlear amplification process depends critically on OHCs, which are thought to act locally in the cochlea. When a pure tone stimulates a passive BM a resonance occurs at a unique location and activates the OHCs. These activated OHCs feed energy back into the system thereby enhancing the BM vibration. Because of saturation, the cochlear amplifier shows a compressive nonlinearity so that the lowest SPL sounds are amplified substantially more than high SPL ones ( ). detailed this active process as characterized by amplification, frequency selectivity, compressive nonlinearity, and the generation of spontaneous otoacoustic emissions (SOAEs) ( Fig. 1.4 ).

Figure 1.4, Characteristics of the ear’s active process. (A) An input–output relation for the mammalian cochlea relates the magnitude of vibration at a specific position along the BM to the frequency of stimulation at a particular intensity. Amplification by the active process renders the actual cochlear response ( red ) over 100-fold as great as the passive response ( blue ). Note the logarithmic scales in this and the subsequent panels. (B) As a result of the active process, the observed BM response ( red ) is far more sharply tuned to a specific frequency of stimulation, the natural frequency, than is a passive response driven to the same peak magnitude by much stronger stimulation ( blue ). (C) Each time the amplitude of stimulation is increased 10-fold, the passive response distant from the natural frequency grows by an identical amount ( green arrows). For the natural frequency at which the active process dominates, however, the maximal response of the BM increases by only 10 1/3 , a factor of about 2.15 ( orange arrowheads). This compressive nonlinearity implies that the BM is far more sensitive than a passive system at low stimulus levels, but approaches the passive level of responsiveness as the active process saturates for loud sounds. (D) The fourth characteristic of the active process is SOAE, the unprovoked production of one or more pure tones by the ear in a very quiet environment. For humans and many other species, the emitted sounds differ between individuals and from ear to ear but are stable over months or even years.

The OHC electromotile response is also nonlinear and works in a cycle-by-cycle mode up to a frequency of at least 70 kHz ( ). Recently, a gene that is specifically expressed in OHCs was isolated and termed Prestin ( ). The action of prestin is orders of magnitude faster than that of any other cellular motor protein. Note that gene names are commonly indicated in italics whereas the expressed protein, which may have the same name, is indicated in normal font. Prestin is required for normal auditory function ( Fig. 1.5 ) because prestin knockout (KO), or knockin (KI), mice do not exhibit OHC electromotility ( ) and thus do not show cochlear amplification. A gene KO is a genetic technique in which one of an organisms genes is made inoperative (“knocked out” of the organism). A gene KI refers to a genetic engineering method that involves the insertion of a protein coding a cDNA sequence at a particular locus in an organism’s chromosome.

Figure 1.5, Average (±SD) compound action potential masking tuning curves from an RW electrode for KI and wild-type mice. Probe tone frequency: 12 kHz.

Functional consequences of loss of this nonlinear amplification process result in hearing loss, loudness recruitment, reduced frequency selectivity, and changes temporal processing. This manifests itself in hearing-impaired listeners as difficulties in speech understanding, especially in complex acoustic backgrounds ( ).

recently challenged the involvement of the cochlear amplifier in BM movement, as sketched above. They recorded the vibrations at adjacent positions on the BM in sensitive gerbil cochleas with a single-point laser vibrometer to measure the velocity of the BM. This measurement was converted in a putative power amplification by the action of the OHCs, and the local wave propagation on the BM. No local power amplification of soft sounds was evident, and this was combined with strong local attenuation of intense sounds. also reported that: “The waves slowed down abruptly when approaching their peak, causing an energy densification that quantitatively matched the amplitude peaking, similar to the growth of sea waves approaching the beach.”

1.3.3

Mechanoelectrical Transduction

“The [BM] displacement is transferred to the hair bundles by means of the tectorial membrane, which contacts the OHC stereocilia and produces fluid movements that displace the IHC stereocilia. Movement of the hairs in the excitatory direction (i.e., toward the tallest row) depolarizes the hair cells whilst opposite deflections hyperpolarize them” ( ).

There are two hair cell types in the cochlea: IHCs and OHCs. The IHCs receive up to 95% of the auditory nerve ’ s afferent innervation ( ), but are fewer in number than the OHCs by a factor of 3–4 ( ). As we have seen, the OHCs provide a frequency-dependent boost to the BM motion, which enhances the mechanical input to the IHCs, thereby promoting enhanced tuning and amplification. This occurs as follows as labeled in Fig. 1.6 : (1) Pressure difference across the cochlear partition causes the BM to move up (purple arrow). (2) The upward BM movement causes rotation of the organ of Corti toward the modiolus and shear of the reticular lamina relative to the tectorial membrane that deflects OHC stereocilia in the excitatory direction (green arrow). (3) This stereocilia deflection opens mechanoelectrical transduction channels, which increases the receptor current driven into the OHC (blue arrow) by the potential difference between the endocochlear potential (+100 mV) and the OHC resting potential (−40 mV). This depolarizes the OHC. (4) OHC depolarization causes conformational changes in prestin molecules that induce a reduction in OHC length (red arrows). The OHC contraction pulls the BM upward toward the reticular lamina, which amplifies BM motion when the pull on the BM is in the correct phase. In contrast to OHCs that are displacement detectors, IHCs are sensitive to velocity of the fluid surrounding the stereocilia ( ).

Figure 1.6, Steps in the cochlear amplification of BM motion for BM movement toward scala vestibuli. TM, tectorial membrane; RL, reticular lamina; IP, inner pillar.

1.3.4

Cochlear Microphonics and Summating Potentials

Both IHC and OHC generate receptor potentials in response to sound ( ). It has long been known that population responses from the cochlea can be recorded at remote sites such as the round window, tympanic membrane, or even from the scalp and can be used clinically ( ; Fig. 1.7 ). These responses are called the cochlear microphonic (CM) and the summating potential (SP). The CM is produced almost exclusively from OHC receptor currents and when recorded from the RW membrane is dominated by the responses of OHCs in the basal turn. The SP is a direct-current component resulting from the nonsymmetric depolarization–hyperpolarization response of the cochlea, which can be of positive or negative polarity, and is likely also generated dominantly by the OHCs ( ). The compound action potential (CAP) is mixed in with the CM and SP and will be described in Section 1.4.3 .

Figure 1.7, Sound-evoked gross potentials in the cochlea. In response to short tone bursts three stimulus-related potentials can be recorded from the cochlea. These potentials, CM, SP, and CAP, appear intermingled in the recorded response from the promontory. By presenting the stimulus alternately in phase and counter phase and averaging of the recorded response, a separation can be obtained between CM on the one hand and CAP and SP on the other. High pass filtering provides a separation between SP and CAP. This can also be obtained by increasing the repetition rate of the stimuli, which results in an adaptation of the CAP but leaves the SP unaltered.

1.3.5

Otoacoustic Emissions

“Unlike other sensory receptor systems, the inner ear appears to generate signals of the same type as it is designed to receive. These sounds, called otoacoustic emissions (OAEs), have long been considered byproducts of the cochlear amplifier, the process that makes cochlear mechanics active by adding mechanical energy at the same frequency as a stimulus tone in a positive feedback process. This feature of the inner ear is one of the most important distinctions from other sensory receptors” ( ).

discovered that sound could evoke “echoes” from the ear. These echoes, called OAEs, result from the action of the cochlear amplifier. described their generation as follows: “As a traveling wave moves apically [along the BM] it generates distortion due to cochlear nonlinearities (mostly from nonlinear characteristics of the OHC [mechanoelectrical transduction] channels, the same source that produces the nonlinear growth of BM motion), and encounters irregularities due to variations in cellular properties. As a result, some of this energy travels backwards in the cochlea and the middle ear to produce OAEs.” Normal human ears generally exhibit SOAEs. SOAEs arise from multiple reflections of forward and backward traveling waves that are powered by cochlear amplification likely via OHC-stereocilia resonance ( ). OAEs can be measured with a sensitive microphone in the ear canal and provide a noninvasive measure of cochlear amplification. There are two main types of OAEs in clinical use. Transient-evoked OAEs (TEOAEs) are evoked using a click stimulus. The evoked response from a click covers the frequency range up to around 4 kHz. Distortion product OAEs (DPOAEs) are evoked using a pair of primary tones f1 and f2 (f1<f2) and with a frequency ratio f2/f1<1.4. In addition to the stimulus tones the spectrum of the ear canal sound contains harmonic and intermodulation distortion products at frequencies that are simple arithmetical combinations of the two tones. The most commonly measured DPOAE is at the frequency 2f1−f2 ( ). Recording of OAEs has become the main method for newborn and infant hearing screening (see chapter: Early Diagnosis and Prevention of Hearing Loss ).

1.4

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