VI. THE INNER EAR: THE COCHLEA

Figure VI-1 illustrates increasingly expanding cross sections of the cochlea. In Figures VI-1B and C are seen the scala vestibuli and scala tympani separated by the cochlear partition, except in the apical turn where the two scalae are in continuity via the helicotrema. Within the modiolus is seen the spiral ganglion. The central processes of spiral ganglion neurons form the cochlear nerve and exit the temporal bone in the internal acoustic meatus. The cochlear partition, which includes the endolymph-filled scala media, is bounded by Reissner's membrane and the basilar membrane, on which sits the auditory receptor organ, the organ of Corti.

Expanded views of a cross section of one turn of the cochlea are shown in Figure VI-1D. At this magnifications it is possible to identify clearly the tectorial membrane, inner and outer hair cells, supporting cells and distal terminals of auditory nerve fibers.

The sensory cells of the organ of Corti are held in place by specialized supporting cells. Some of these are relatively rigid structures containing stiff protein filaments. The hair cells are tightly gripped at their apical ends by processes of one of the filamentous supporting cells, the phalangeal cells. These phalangeal processes together form the reticular lamina. 

The lateral wall of the cochlear duct is formed by the stria vascularis. Histologically, the stria is a very highly specialized stratified epithelium, with capillaries that invade the territory of the epithelium. The lower cells of the epithelium are richly supplied with mitochondria and basal infoldings which are characteristics of cells involved in the control of water and electrolytes. The stria plays an important role in cochlear function by producing endolymph, whose ionic composition more closely resembles intracellular fluid than it does CSF. In the process of producing endolymph (the fluid of the scala media), the stria is also responsible for maintenance of the +90 mv endocochlear potential within the cochlear duct. Endolymph is resorbed through the wall of the endolymphatic sac into the vessels of the dura matter. 

Reissner's membrane is the third side of the cochlear duct and separates perilymphatic space (scala vestibuli) from endolymphatic space (cochlear duct). It is two layers thick  being composed of simple squamous epithelium (toward endolymph) and a connective membrane.  

As can be seen in the cross section of the cochlear spiral (Figure VI-1B), the bony cochlea becomes smaller and smaller in cross-sectional area as the apex is approached. At the same time the basilar membrane becomes progressively wider toward the apex. This is because the osseous spiral lamina is broadest at the cochlear base where the basilar membrane is only about 0.16 mm wide (in humans); at the apex the basilar membrane has  broadened to about 0.52 mm. This variation in width of the basilar membrane correlates with its variation in stiffness  which, in turn, underlies the kind of mechanical motion it undergoes in response to sound waves.

There are two kinds of hair cells in the organ of Corti: inner hair cells (IHC) and outer hair cells (OHC) (Figure VI-2).  Usually there is but a single row of IHCs and three to four rows of OHCs. In humans there are approximately 3,500 IHCs and 12,000 OHCs. The hairs of both species are related to the auxiliary structure of the organ of Corti, the tectorial  membrane. Unlike vestibular hair cells, these have no kinocilium in adult life (although a remnant, the basal body,  remains in the cell body). They differ from one another in their shape and in the pattern of the stereocilia. They are also innervated differently. Nearly 95% of the afferent fibers of the cochlea division of the eighth nerve originate at the base of inner ear cells. Most of the efferent input to the cochlea from the central nervous system reaches the bases of the OHCs. Motion of the basilar membrane, under the influence of sound, results in a shearing motion between the stereocilia and tectorial membrane resulting in activation of the hair cell and the afferent auditory nerve fibers connected to it.

Our understanding of the operations of the inner ear began in the late 19th century.  Hermann von Helmholtz, a brilliant German physicist at the time viewed the basilar membrane in the inner ear as a series of mechanical resonators arranged like the strings of a harp, varying in tuning from high frequency at the base of the cochlea to low frequency at the apex. According to this view, the basilar membrane vibrates maximally at the spot whose resonance frequency matches the frequency of the stimulus, giving rise to excitation of only those nerve fibers which innervate that spot. This is a form of labeled-line, or "place," theory of pitch perception in which the locus of maximal vibration along the cochlear spiral determines the perceived pitch by activating a specific small group of nerve fibers.  Many years passed before Helmholtz's theory was tested by direct observation of the mechanical vibration patterns of the inner ear by the Hungarian physicist, Georg von Bekesy, a feat which earned him the Nobel Prize.

Over the past 50 years considerable progress has been made using modern physical recording methods in further elucidating the mechanical properties of the organ of Corti. We can now state the mechanical events that take place in the cochlea when a sound wave enters the inner ear:

1. Sound waves normally enter the inner ear via the oval window and are transmitted rapidly through the cochlear fluid. Movement of the oval window by the stapes footplate is met with equal and opposite action of the round window (Figure VI-3).

2. The basilar membrane is a resonant structure. The basilar membrane is deflected in response to sound waves in the inner ear. Each location along the basilar membrane responds best to a small range of sound frequencies. The basilar membrane is NOT under tension, however. Therefore, it does NOT operate as a series of independent tuned resonators, like the strings of a harp. Figure VI-4 illustrates resonance curves derived from different regions along the basilar membrane.

3.  The deformation of the basilar membrane is a traveling wave. When motion of the stapes establishes a sound wave in the fluid of the inner ear, each small region of the basilar membrane deflects in response to this pressure with a time delay that depends upon its own mechanical properties. The wave then diminishes rapidly in both amplitude and velocity as it continues to move toward the apex. Figure VI-5A illustrates a traveling wave at four successive instants in time, together with the envelope of the peaks of the displacement.

The part near the base, with its high resonance frequency and correspondingly short mechanical "time constant," moves first, followed by successively more apical segments. The displacement thus constitutes a traveling wave of deformation which progresses from base toward apex. Figure VI-5B is a three-dimensional rendition of the traveling wave envelope.

4. Different regions of the basilar membrane respond maximally to different sound frequencies based on the local physical properties. There is a systematic shift in the locus of maximal vibration from the apex toward the base as the frequency of a pure tone stimulus is raised. The curves in Figure VI-6 show in cartoon form the travelling wave for low, mid, and high frequency sounds. Thus, the basilar membrane is said to be tonotopically organized.

5. The primary factor which changes the tuning along the cochlear partition is the variation in width of the basilar membrane (Figure VI-7). This results in a systematic change in effective stiffness from base to apex.

6. Hair cells are 'active' participants in the mechanoelectric transduction process. By mechanisms not yet fully understood, outer hair cells change shape under the influence of sound. Shape change is driven by a 'molecular motor,' which has not yet been characterized structurally or chemically. This mechanism, nonetheless, renders the operation of the organ of Corti highly non-linear, which is essential to account for the ears phenomenal sensitivity and dynamic range of frequency and intensity.

When sound energy is introduced into the inner ear, the resultant up-and-down motion of the basilar membrane produces shearing motion between the stereocilia projecting from the apical surfaces of hair cells and the tectorial membrane. Shearing occurs because of the relative positions of the hinge points for the basilar membrane and the tectorial membrane (Figure VI-8). This shearing action displaces the stereocilia which, in turn, results in cellular depolarization or hyperpolarization through the transduction mechanisms described earlier.

The transduction process results in a non-propagated receptor potential, which is associated with the release of neurotransmitter at the base of the hair cell and the excitation of primary afferent neurons. The propagated, all-or-none impulses that arise in the auditory nerve fibers then carry to the CNS the coded information concerning the auditory stimulus. All information about our acoustic environment is, thus, carried in trains of nerve impulses in bundles of auditory nerve fibers of the left and right ears.

What is the innervation pattern in the organ of Corti and what are the codes used in carrying acoustic information from the ear to the brain?

There are two types of fibers that innervate hair cells in the organ of Corti: afferent and efferent. Afferent innervation comes via peripheral processes of bipolar neurons in the spiral ganglion; the central processes of the spiral ganglion neurons project to cells in the brainstem. This accounts for about 95% of the axons in the auditory nerve. The remaining efferent innervation arises from neurons in the brainstem and carries information from the brain to the cochlea.

Afferent innervation: The greatest number of afferent fibers make contact with inner hair cells (Figure VI-9). There is little divergence of afferent fibers in the cochlea: each auditory nerve fiber contacts but one inner hair cell. Each inner hair cell contacts as many as 20 auditory nerve fibers. A relatively small number (about 5%) of afferents innervate outer hair cells.

Efferent innervation: Axons arising from neurons in the superior olivary complex of the brainstem reach the cochlea (in the olivocochlear bundle) where they synapse mainly at the base of outer hair cells. The bundle arises from olivary neurons on both sides of the midline, forming two olivocochlear systems.

Like in all other sensory systems, information about the outside world is carried to the brain in trains of all-or-none action potentials in ensembles of peripheral afferent nerve fibers. As applied to the auditory system, the term "code" is simply a way of describing the manner in which information about sound is represented in such neural activity.

The Place Principle of Hearing - a labeled-line code

Johannes Müller suggested more than a century and a half ago that different nerve fibers elicit different sensations by virtue of their "specific nerve energies." In modern terms this theory states that: different sets of auditory nerve fibers, when active, elicit different auditory sensations by virtue of their central connections. It is most often applied to the perception of pitch and the quality of tones. This is because auditory nerve fibers exhibit a selectivity for the frequency of a sound. Figure VI-10A illustrates this with a curve that relates the threshold of response of a single auditory nerve fiber to sound frequency. Such a curve is called the threshold tuning curve, and it mirrors the mechanical tuning of the spot on the basilar membrane innervated by the fiber. The frequency to which a fiber is most sensitive is referred to as the characteristic frequency (CF). Different fibers will have a CF dependent on the location of the hair cell to which they are attached (Figure VI-10B). Because these auditory nerve fibers each innervate a single inner hair cell, and because the basilar membrane is itself tonotopically organized in a mechanical sense, the characteristic frequency of a nerve fiber is directly related to a location (or a 'place') along the basilar membrane.

Figure VI-11 shows the relationship between cochlear place and the regions of greatest frequency sensitivity. Hair cells that are traumatized, either mechanically, by disease or by ototoxic drugs, exhibit very poor frequency selectivity. Destruction of hair cells results in loss of hearing sensitivity in the frequency region represented by those cells. This is a major cause of a sensorineural hearing loss.

Rate code

Acoustic information may be carried by the rate or frequency of the discharge of a neuron. The peripheral encoding of sound intensity is associated with this type of code. Figure VI-12 illustrates the change in discharge rate as a function of sound pressure level for a single fiber of the auditory nerve. Over a range of some 40-70 dB a very small change in intensity results in a relatively large change in discharge rate. Because a single fiber can not respond over the full listening range of 120 dB, intensity must be coded in a population of fibers with different thresholds, as illustrated in Figure VI-12B.

Temporal code - the Volley Theory of Hearing

It has long been known that the auditory system preserves temporal information. Listeners use temporal cues, along with others, in encoding the low frequency information in our language -- the vowel sounds -- and in preserving interaural time differences used by listeners in localizing the source of a sound in space. Temporal coding comes about because the hair cells in the cochlea are functionally polarized, which means that deflection of the stereocilia in one direction is excitatory for the hair cells and movement in the opposite direction is inhibitory. Thus, when the basilar membrane vibrates in response to low-frequency signals, below about 4 kHz, the hair cells in the region of vibration exhibit an alternating excitation-inhibition at the frequency of vibration. This, in turn, generates action potentials in auditory nerve fibers attached to those hair cells. The action potentials in the nerve reflect the time-pattern of excitation and inhibition in the hair cell. The result is a train of nerve impulses time locked to the individual cycles of the acoustic stimulus. For a simple sine wave, the impulses are generated around a particular point on the sine-wave cycle, a process that is referred to as phase locking. Because of its refractory period, an auditory nerve fiber can not respond to every successive cycle of a stimulus. When it responds, however, it does so around a constant phase angle of the stimulus. Consequently, the impulses occur around integral multiples of the period of the sine-wave stimulus (Figure VI-13).

A population of auditory nerve fibers, all phase-locking to the same stimulus, represent in their combined discharge pattern the complete temporal representation of the stimulus. The combined time sequence of events in called 'volleying,' and the theory that describes it as a way of carrying information is called the 'Volley Theory of hearing.' Figure VI-14 illustrates this phase-locking of an ensemble of auditory nerve fibers to a low frequency pure tone. Each fiber is incapable of responding to every cycle of the stimulus, but collectively they can do so.

Ensemble code

It is unlikely that any natural stimulus engages but a single inner hair cell (IHC) and thereby excites but one or even that small number of auditory nerve fibers associated with a single receptor cell. Indeed, a single auditory nerve fiber is probably not capable of encoding unambiguously the frequency or intensity of a sound, as described above. Rather, when some finite number of receptor cells is brought to threshold level of activation in a temporal sequence that is governed by the velocity and slope of the traveling wave envelope on the cochlear partition, the information about that displacement pattern is coded in terms of the profile of the rate and timing of activity across all or part of the eighth-nerve array.

Knowledge of coding mechanisms is used in diagnosis and treatment of hearing disorders

Increasing clinical use is being made of our growing knowledge of the neural coding of auditory information. Recording of the compound action potential of the auditory nerve by electrodes placed near the round window is used in certain situations for testing the integrity of the cochlea and auditory nerve. Hearing aids are becoming highly sophisticated, with their circuitry tuned to take advantage of the function of surviving receptors. Surgeons are now implanting electrode arrays inside the cochleas of patients who have suffered loss of hair cells but who have at least partially intact auditory nerves. Such a prosthetic device permits direct electrical stimulation and partial restoration of hearing. Success in these efforts requires that the spatial and temporal patterns of neural excitation which occur in the normal ear be duplicated as closely as possible.

Efferent effects

Efferent axons, arising in the brainstem in the vicinity of the superior olivary complex, contact mainly outer hair cells. Stimulation of efferents has a profound effect on the afferent input to the brain. Such effects are mediated via active processes in outer hair cells. Outer hairs cells change shape in response to efferent activation, which in turn alters the micromechanical action of inner hair cells, and hence the flow of information from the ear to the brain.

The cochlea, once thought to be a 'passive' transducer of sound energy into electrical nerve impulses, is now knows to contain 'active' elements. This means that the cochlea not only responds to energy imposed on it, but it also generates energy. One way in which this is now believed to occur is by movement of the outer hair cells. A change in configuration of an outer hair cell may have a substantial influence on the mechanical response of inner hair cells, the main transducers and signallers of acoustic information entering the inner ear.