Aspects of Normal Hearing

In normal hearing sound waves traveling through air reach the tympanic membrane via the ear canal, causing vibrations that move the three small bones of the middle ear. This action produces a piston-like movement of the stapes, the third bone in the chain. The “footplate” of the stapes is attached to a flexible membrane in the bony shell of the cochlea called the oval window. Inward and outward movements of this membrane induce pressure oscillations in the cochlear fluids, which in turn initiate a traveling wave of displacement along the basilar membrane (BM), a highly specialized structure that divides the cochlea along its length. This membrane has graded mechanical properties. At the base of the cochlea, near the stapes and the oval window, it is narrow and stiff. At the other end, near the apex, the membrane is wide and flexible. These properties give rise to the traveling wave and to points of maximal response according to the frequency or frequencies of the pressure oscillations in the cochlear fluids. The traveling wave propagates from the base to the apex. For an oscillation with a single frequency, the magnitude of displacements increases up to a particular point along the membrane and then drops precipitously thereafter. High frequencies produce maxima near the base of the cochlea, whereas low frequencies produce maxima near the apex.

Motion of the BM is sensed by the inner hair cells (IHCs) in the cochlea, which are attached to the top of the BM in a matrix of cells called the organ of Corti. Each hair cell has fine rods of protein, called stereocilia, emerging from one end. When the BM moves at the location of a hair cell, the rods are deflected as if hinged at their bases. Such deflections in one direction increase the release of a chemical transmitter substance at the base (other end) of the cells, and deflections in the other direction inhibit the release. The variations in the concentration of the chemical transmitter substance act at the terminal ends of auditory neurons, which are immediately adjacent to the bases of the IHCs. Increases in chemical transmitter substance increase discharge activity in the nearby neurons, whereas decrements in the substance inhibit activity. Changes in neural activity thus reflect events at the BM. These changes are transmitted to the brain via the auditory nerve, the collection of all neurons that innervate the cochlea.

The steps described above are illustrated in the top panel of Fig. 100.1 , which shows a cartoon of the main anatomical structures, including the tympanic membrane, the three bones of the middle ear, the oval window, the BM, the IHCs, and the adjacent neurons of the auditory nerve.

Cartoons of anatomical structures in normal and deafened ears. For simplicity not all structures are shown, and the structures that are shown are not necessarily to scale.

Reproduced from Dorman, M.F., Wilson, B.S., 2004. The design and function of cochlear implants. Am. Sci. 92, 436–445, with permission from the American Scientist and Sigma Xi.

Loss of Hearing

The principal cause of hearing loss is damage to or complete destruction of the sensory hair cells. Unfortunately, the hair cells are fragile structures and subject to a wide variety of insults, including but not limited to genetic defects, infectious diseases (e.g., rubella and meningitis), overexposure to loud sounds, certain drugs (e.g., kanamycin, streptomycin, and cisplatin), and aging. In the deaf or deafened cochlea, the hair cells are largely or completely absent, severing the connection between the peripheral and central auditory systems. The function of a cochlear prosthesis is to bypass the (missing) hair cells by stimulating directly the surviving neurons in the auditory nerve.

The anatomical situation faced by designers of CIs is illustrated in the bottom panel of Fig. 100.1 . The panel shows a complete absence of hair cells. In general, a small number of cells may remain for some patients, usually in the apical (low-frequency) part of the cochlea.

Without the normal stimulation provided by the hair cells, the peripheral parts of the neurons (between the cell bodies in the spiral ganglion and the terminals within the organ of Corti) undergo “retrograde degeneration” and eventually die ( ). Fortunately, the cell bodies are far more robust. At least some usually survive, even for prolonged deafness or virulent etiologies such as meningitis ( ).

Electrical Stimulation of the Auditory Nerve

Direct stimulation of the nerve is produced by currents delivered through electrodes placed in the scala tympani (ST), one of three fluid-filled chambers along the length of the cochlea. A cutaway drawing of the implanted cochlea is presented in Fig. 100.2 . The figure shows a partial insertion of an array of electrodes into the ST. The array can be inserted through an incision in the round window membrane, a drilled enlargement of the area ordinarily occupied by the membrane, or a drilled opening (“cochleostomy”) near the basal end of the cochlea and as illustrated in the figure.

Cutaway drawing of the implanted cochlea. Illustrated is the electrode array developed at the University of California at San Francisco (UCSF) ( ). That array includes eight pairs of bipolar electrodes spaced at 2 mm intervals and with the electrodes in each pair oriented in an “offset radial” arrangement with respect to the neural processes peripheral to the ganglion cells in the intact cochlea. Only four of the bipolar pairs are visible in the drawing, as the others are “hidden” by cochlear structures. This array was used in the UCSF/Storz and Clarion 1.0 devices and is no longer used today.

Reproduced from Leake, P.A., Rebscher, S.J., 2004. Anatomical considerations and long-term effects of electrical stimulation. In: Zeng, F.-G., Popper, A.N., Fay, R.R. (Eds.), Auditory Prostheses: Cochlear Implants and beyond. Springer-Verlag, New York, pp. 101–148, with permission of Springer-Verlag.

Different electrodes in the array may stimulate different subpopulations of neurons. As described previously, neurons at different positions along the length of the cochlea respond to different frequencies of acoustic stimulation in normal hearing. Implant systems attempt to mimic or reproduce this “tonotopic” encoding by stimulating basally situated electrodes (first turn of the cochlea and lower part of the drawing) to indicate the presence of high-frequency sounds, and by stimulating electrodes at more apical positions (deeper into the ST and ascending along the first and second turns in the drawing) to indicate the presence of sounds with lower frequencies. Closely spaced pairs of bipolar electrodes are illustrated here, but arrays of single electrodes that are each referenced to a remote electrode outside the cochlea may also be used. This latter arrangement is called a “monopolar coupling configuration” and is used in all present-day implant systems that are widely applied worldwide; one such array is illustrated in Fig. 100.3 .

A modern electrode array for cochlear implants (CIs). This particular array is highly flexible and has a narrow and tapered cross-sectional area; these properties, along with a flexible silicone “carrier,” allow safe insertions deep into the scala tympani (ST) of the cochlea in many cases. Other arrays now in widespread use have more electrodes and shallower insertions, and some are designed to “hug” the inner wall of the ST for the closest possible apposition to the spiral ganglion cells, which are the putative neural target for CIs.

Diagram courtesy of MED-EL GmbH.

The spatial specificity of stimulation with an ST electrode most likely depends on a variety of factors, including the orientation and geometric arrangement of the electrodes, the proximity of the electrodes to the target neural structures, and the condition of the implanted cochlea in terms of nerve survival and ossification. An important goal of electrode design is to maximize the number of largely nonoverlapping populations of neurons that can be addressed with the electrode array. Present evidence suggests, however, that no more than four to eight sites are effective using current designs and placements of electrode arrays, even for arrays with as many as 22 electrodes (e.g., ). Most likely the number of effective sites is limited by substantial overlaps in the electric fields from adjacent (and more distant) electrodes. The overlaps are unavoidable for electrode placements in the ST, as the electrodes are “sitting” in the highly conductive fluid of the perilymph and additionally are relatively far away from the target neural tissue in the spiral ganglion. A closer apposition of the electrodes next to the inner wall of the ST would move them a bit closer to the target cells (see Fig. 100.2 ), and such placements have been shown in some cases to produce an improvement in the spatial specificity of stimulation ( ). However, a large gain in the number of independent sites may well require a fundamentally new type of electrode, a fundamentally different placement of electrodes, or optical rather than electrical stimulation (e.g., ). In addition, drug-induced growth of neural processes (“neurites”) from the ganglion cells toward the electrodes in the ST may well increase both the dynamic range and the spatial specificity of electrical stimulation by those electrodes (e.g., ).

Fig. 100.2 shows a complete presence of hair cells (in the labeled organ of Corti) and a pristine survival of cochlear neurons. However, the number of hair cells is zero or close to it in cases of complete hearing loss. In addition, survival of neural processes peripheral to the ganglion cells (the “dendrites”) is at least unusual in the totally deafened cochlea, as noted previously. Survival of the ganglion cells and central processes (the central axons) ranges from sparse to substantial. The pattern of survival is in general not uniform, with reduced or sharply reduced counts of cells in certain regions of the cochlea. In all, the neural substrate or target for a CI can be quite different from one patient to the next. A detailed review of these observations and issues is presented by .

Electrode arrays in current widespread use are thinner and more flexible than their predecessors. The array illustrated in Fig. 100.3 , for example, is quite thin and flexible and has “wavy” interconnecting wires that contribute to the flexibility ( ). These aspects of this particular design allow deep insertions into the ST and the possibility to address neurons along most of the length of the cochlea ( ).

Components of Cochlear Implant Systems

The components shared by all CI systems in current widespread use are illustrated in Fig. 100.4 and include a microphone for sensing sound in the environment; a processor to transform the microphone input into a set of stimuli for the implanted array of electrodes; a transcutaneous link for the transmission of power and stimulus information across the skin; an implanted receiver/stimulator to decode the information received from the radio-frequency signal produced by an external transmitting coil and then generate stimuli using the instructions obtained from the decoded information; a cable to connect the outputs of the receiver/stimulator to the electrodes; and the array of electrodes. These components must work together as a system to support excellent performance, and a weakness in a component can degrade performance significantly. For example, a limitation in the data bandwidth of the transcutaneous link can restrict the types and rates of stimuli that can be specified by the external processor, and this restriction can in turn limit performance.

Components of cochlear implant systems.

Diagram courtesy of MED-EL GmbH.

One “component” that is not illustrated in Fig. 100.4 is the biological part central to the auditory nerve (the nerve is at the right and is colored yellow in the figure), including the auditory pathways in the brainstem and the auditory cortices of the implant recipient. As described in detail in , and , this part varies in its functional integrity and capabilities across patients, and is at least as important as the other parts in determining outcomes with implants.

Transformation of Input Sounds Into Stimuli for the Implant

An important aspect of the design for any type of sensory neural prosthesis is how to transform an input from a sensor or array of sensors into a set of stimuli that can be interpreted by the nervous system. The stimuli can be electrical or tactile, for example, and usually involve multiple sites of stimulation corresponding to the spatial mapping of inputs and representations of those inputs in the nervous system. One approach to the transformation (and probably the most effective approach) is to mimic or replicate at least to some extent the damaged or missing physiological functions that are bypassed or replaced by the prosthesis.

For CIs, this part of the design is called the processing strategy. As noted previously, advances in processing strategies have produced quite large improvements in the speech reception performance of implant patients, from recognition of a tiny percentage of monosyllabic words with the first strategies and multisite stimulation, for example, to recognition of a high percentage of the words with current strategies and multisite stimulation.

One of the simplest and most effective approaches for representing speech and other sounds with present-day CIs is illustrated in Fig. 100.5 . This is the continuous interleaved sampling (CIS) strategy ( ), which is a processing option in all implant systems now in widespread clinical use and the basis for other processing options in current use ( ).

Block diagram of the continuous interleaved sampling (CIS) processing strategy for cochlear implants. The circles with “x” marks within them are multiplier blocks, and the green traces beneath those blocks are stimulus waveforms. Band envelopes can be derived in multiple ways and only one way is shown. BPF , bandpass filter; EL , electrode; LPF , low-pass filter; Pre-emp , pre-emphasis filter; Rect ., rectifier.

The diagram is adapted from Wilson, B.S., Finley, C.C., Lawson, D.T., Wolford, R.D., Eddington, D.K., Rabinowitz, W.M., 1991. Better speech recognition with cochlear implants. Nature 352, 236–238, and is used here in its modified form with the permission of the Nature Publishing Group. The inset is from Hüttenbrink, K.B., Zahnert, T., Jolly, C., Hofmann, G., 2002. Movements of cochlear implant electrodes inside the cochlea during insertion: an X-ray microscopy study. Otol. Neurotol. 23, 187–191, and is reproduced here with the permission of Lippincott Williams & Wilkins.

The CIS strategy filters speech and other input sounds into bands of frequencies with a bank of bandpass filters. Envelope variations in the different bands are represented at corresponding electrodes in the cochlea with modulated trains of biphasic electrical pulses. The envelope signals extracted from the bandpass filters are compressed with a nonlinear mapping function prior to the modulation to map the wide dynamic range of sound in the environment (around 90 dB) into the narrow dynamic range of electrically evoked hearing (about 10 dB or somewhat higher). The output of each bandpass channel is directed to a single electrode, with low-to-high channels assigned to apical-to-basal electrodes, to mimic at least the order, if not the precise locations, of frequency mapping in the normal cochlea. The pulse trains for the different channels and corresponding electrodes are interleaved in time, so that the pulses across channels and electrodes are nonsimultaneous. This eliminates a principal component of electrode interaction, which otherwise would be produced by direct vector summation of the electric fields from different (simultaneously stimulated) electrodes. The corner or “cut-off” frequency of the low-pass filter in each envelope detector typically is set at 200 Hz or higher, so the fundamental frequencies of speech sounds are represented in the modulation waveforms. CIS gets its name from the continuous sampling of the (compressed) envelope signals by rapidly presented pulses that are interleaved across electrodes. Between 4 and 24 channels (and corresponding stimulus sites) have been used in CIS implementations to date.

Other strategies have also produced outstanding results, including the n -of- m ( ), spectral peak ( ), advanced combination encoder ( ), fine structure processing ( ), “HiResolution” ( ), HiResolution 120 ( ), CIS+ ( ), and “high-definition” CIS ( ) strategies. Detailed descriptions of these and prior strategies are presented in and . In addition, considerably more information about the CIS strategy is presented in , and .