HANDBOOK OF THE SENSES

Audition Volume

Chapter 7: Mechano-Acoustical Transformations

Sunil Puria1,2 and Charles R. Steele1

Stanford University, Mechanical Engineering Department, Mechanics and Computation Division, 496 Lomita Mall, Durand Building, Room 206, Stanford, CA 94305 2 Department of Otolaryngology-Head and Neck Surgery, 801 Welch Road, Stanford, CA 94304

1. KEYWORDS 2. BIOMECHANICS, OTOBIOMECHANICS, COCHLEA, COLLAGEN FIBERS, EXTERNAL EAR, IMPEDANCE, INNER HAIR CELLS, LEVERS, MATHEMATICAL MODELS, MICROCT, MIDDLE EAR, ORGAN OF CORTI, OUTER HAIR CELLS, PRESSURE, TYMPANIC MEMBRANE, VIBRATION

I. Outline
In this chapter we examine the underlying biophysics of acoustical and mechanical transformations of sound by the sub components of the ear. The sub components include the pinna, the ear canal, the middle ear, the cochlear fluid hydrodynamics and the organ of Corti. Physiological measurements and the deduced general biophysics that can be applied to the input and output transformations by the different sub components of the ear are presented.

II. Abstract
The mammalian auditory periphery is a complex system, many components of which are biomechanical. This complexity increases sensitivity, dynamic range, frequency range, frequency resolution, and sound localization ability. These must be achieved within the constraints of available biomaterials, biophysics and anatomical space in the organism. In this chapter, the focus is on the basic mechanical principles discovered for the various steps in the process of transforming the input acoustic sound pressure into the correct stimulation of mechano-receptor cells. The interplay between theory and measurements is emphasized.

III. Main Body

A. Introduction
The auditory periphery of mammals is one of the most remarkable examples of a biomechanical system. It is highly evolved with tremendous mechanical complexity. What is the reason for such complexity? Why cant hair cells tuned to various frequencies just sit on the outside and detect motion due to sound? Clearly, the complexity serves the animal by providing greater functionality. This can be appreciated by looking at simpler auditory systems. One of the simplest hearing organs is that of the fly (Drosophila melanogaster), which has a tiny feather-like arista that produces a twisting force directly exerted by sound. This sound receiver mechanically oscillates to activate the Johnstons organ auditory receptors with a moderately damped resonance at about 430 Hz (Gopfert and Robert 2001). The level required to elicit a response, due to wing-generated auditory cues involved in courtship, are in the 70 to 100 dB SPL range (Eberl et al. 1997). An example of a simpler anatomy with more complex function than that of the fly is the Mllers organ of the locust. This invertebrate is capable of discriminating sounds at broadly tuned frequencies of approximately 3.5-5, 8, 12 and 19 kHz corresponding to the four mechanotransduction receptors attached to the tympanic membrane (Michelsen 1966). The best threshold for the receptor cells is about 40 dB SPL. The resonances of the tympanic membrane and attached organs provide the greater number of frequency channels than the fly (Windmill

et al. 2005). Amphibians evolved to have a basilar papilla with a few hundred receptor cells in a fluid medium. Other amphibians, birds and mammals have many thousands of hair cells. Other such examples, where structure that is more complex leads to greater hearing capability, are found in some of the other chapters in this volume. The peripheral part of the auditory system comprising of the external ear, middle ear and the inner ear systematically transform and transduce environmental sounds to neural impulses in the auditory nerve. The precise biophysical mechanisms relating the input variables to the output variables of some of the subsystems are still being debated. However, there is general agreement that these transformations lead to improved functionality. Five of the most important functional considerations are described below. 1. Sensitivity. The human ear is most sensitive to a range of sounds from the loudest at about 120 dB SPL to the softest at about 3 dB SPL. At its most sensitive frequency near 4 kHz, the displacement at the tympanic membrane is less than 1/10th the diameter of a hydrogen atom. At this threshold, the amount of work that is done at the eardrumi is 3 x 10-18 J. In comparison, the amount of work done for the perception of light at the retinaii is 4x10-18 J, which is close to the calculated value at the threshold of hearing. This suggests that at its limits, the two sensory modalities have comparable thresholds. 2. Dynamic range. The dynamic range of psychophysical hearing in humans is about 120 dB SPL corresponding to environmental sounds and vocalized sounds. However, the neurons of the auditory nerve have a dynamic range that is typically less than 60 dB SPL. The organ of Corti mechanics must facilitate this dynamic range mismatch problem. 3. Frequency range. Hearing has about 8.5-octave frequency range in human and in some other mammals this range can be as wide as 11.5-octaves (ferrets). To handle this processing mechanically, the sensory receptors should have physical variations on a similar scale. However, the large range is achieved over an extraordinarily small space in comparison to the wavelengths of sound. 4. Frequency resolution. One of the most important functions of the cochlea is the tonotopic organization, which maps different input frequencies to its characteristic place in the cochlea. Like a Fourier frequency analyzer, each characteristic place has narrow frequency resolution, which provides greater sensitivity to narrow-band signals by reducing bandwidth and thus input noise at the individual mechano-receptor hair cells and thus the auditory nerve. 5. Sound localization. The physical characteristics of the pinna and head diffract sound in a spatially dependent manner. The diffraction pattern provides important cues that allow the more central mechanisms to localize, segregate and stream different sources of sound. In this chapter, we follow the chain of acousto-mechanical transformations of sound from the pinna to modulation of tension in inner hair cell tip links which is the final mechanical output variable of the cochlea from our vantage point. The tension in the tip links opens ion channels in the stereocilia, which then starts a chain of biochemical events that leads to the firing of the auditory neurons. We designate the output of a given

sub system a proximate variable. The chain of proximate variables leads to the ultimate output variable, the tip-link tension in hair cells. Input variables are sound pressure level, morphometry of anatomical structures, and mechanical properties of those structures. Biomechanical processes combined with the input variables lead to the proximate variables, which are physiologically measurable.

B. Theories of sound transmission in the ear

Starting with Helmholtz, mathematical models have played a key role in improving our understanding of the underlying biomechanical processes of the auditory periphery. In comparison to using natural languages to describe the observed phenomena, mathematical formulations have advantages and disadvantages. The advantages include a methodology for the possibility to describe compactly a correspondence to reality. The disadvantages are that the description may be incomplete or its validity difficult to test. A mathematical model is also often a statement of a scientific theory that captures the essence of the current state of the empirical observations. The power of a specific model is its ability to evolve as more facts become available and to be able to predict facts not yet observed. Thus the interplay between theory and experiments allows one to test different hypotheses and generate new hypotheses. In this chapter we provide a foundation for physiological measurements in the form of mathematical models. Below we present some common principles, found all through the auditory periphery, to transform the input variables to the ultimate output variable of hair cell tip link tension. Several general concepts are presented. These include how levers are formed, how Newtons laws apply not only to celestial mechanics as originally formulated but also in otobiomechanics, how sound transmission through different materials is described by transmission line formulations, and how modes of vibrations arise in structures. A combination of these principles is used to understand how the ear improves sensitivity, frequency range, frequency resolution, dynamic range, and sound localization within the constraints of biological materials and anatomic space.

1. Mechanical and acoustic levers

One of the simplest transformations of energy is achieved with a simple mechanical lever. There are numerous places in the auditory periphery where levers produce force and velocity transformations through anatomical changes in lengths and areas. These transformations take place in the context of improving sound transmission at the interfaces of different anatomical structures where there is a change in the impedance. An example of a change in impedance is the low impedance of air to the high impedance of the fluid filled cochlea. Examples of the lever action at work include an increase in sound pressure due to a decrease in area of the concha of the pinna to the ear canal, increase in pressure from the decrease in surface area from the tympanic membrane to the stapes footplate, increase in force due to the lever ratio in the ossicular chain, increase in volume velocity from the stapes footplate to the basilar membrane due to a decrease in surface area, and transformation of the basilar membrane displacement to hair cell stereocillia tip link tension due to relative shearing motion between the reticular lamina and the tectorial membrane.

2. Newtons second law of motion

A key principle in describing dynamic transformation of forces in mechanical systems to accelerations is the well-celebrated Newtons second law of motion elegantly written as
F = ma ,
(Eq. 1)

which states that a force F acted upon a mass, results in acceleration a. Newtons second law, transformed to the frequency domain, is:
" R K F (! ) = $ M + + $ j! j! #

( )

% ' a(! ) . 2 ' &

(Eq. 2)

Here the sinusoidal force F ( w) , with radian frequency ! , acts upon an object described by the variables in the square bracket. This object has now been generalized to include mass M, resistance R, and stiffness K. An alternative form of Eq. (2) in terms of particle velocity v (! ) is:
# K & F (! ) = % j! " M + R + " v (! ) , j! ( $ '
(Eq. 3)

where the term in the square bracket is the mechanical impedance Z m . Sound pressure P(! ) , measured with a microphone, is defined as the force per unit area A. Thus, Eq. (3) can be rewritten for acoustics as

# K & P(! ) = % j! " M a + Ra + a ( " V (! ) j! ' $

(Eq. 4)

The term in the square bracket is now the acoustic impedance Z a , which for uniform properties is the mechanical impedance Z m divided by A2, and V (! ) = v (! ) A is the volume velocity. One thing to keep in mind is that impedance concepts are limited to linear steady state analyses. Despite this limitation, Eqs. (3) and (4) play a prominent role in helping us understand transformations of forces and pressures to velocities and volume velocities throughout the ear. It is clear from these equations that the velocity of any structure is proportional to the applied force but inversely proportional to the impedance due to its mass (M), damping (R) and stiffness (K). At resonance the velocity reaches a maximum because the impeding effect of mass is cancelled by the impeding effect of stiffness. One of the challenges in efficient sound transmission to the hair cell detectors is in minimizing the impeding effect of fluid damping and stiffness and mass of structures.

3. Transmission lines
Many problems in sound and vibration are described by the wave equation that results from Newtons laws of motion. The one-dimensional (1-D) version of the wave equation 6

was formulated by dAlembert in 1747 for the vibrating string. It did not take Euler very long (1759) to formulate the first derivation of the wave equation for sound transmission in one dimension and later in three dimensions (3-D). The wave equation has stood the test of time as is evident by its use in disciplines that include electromagnetic theory, transverse waves in stretched membranes, blood vessels, and electromagnetic transmission lines. Because it was used so extensively in telephone communication and power line transmission problems, the 1-D wave equation is also known as the transmission line equation. In these equations the properties of the transmission system are assumed to be constant along the direction of propagation. A special form of the wave equation exists when a property along the propagation direction varies exponentially. As reviewed by Eisner (1967), these equations were originally formulated by Lord Rayleigh and are now known as Websters horn equation. Subsequent sections will show that the transmission line formulation can be used to describe ear canal acoustics, the coupling between the canal and tympanic membrane, wave propagation in the cochlea, and transverse motion on the basilar membrane. The series of transmission lines that are sequentially coupled may improve frequency bandwidth while maintaining sensitivity of the proximate variables.

4. Modes of vibration
Anatomical structures and membranes have various modes of vibration with peak responses at modal frequencies due to resonance. These modes of vibrations are not very different from modes of vibrations in the strings of violins, guitars and pianos where the ends of the strings are fixed are both ends. The resonant frequency is directly proportional to the string tension and density but inversely proportional to its length. More complicated modes of vibrations are found in membranes and plates. In the ear, examples where resonances are a characteristic feature include the pinna and ear canal, tympanic membrane, ossicles, the basilar membrane, organ of Corti, and hair cell stereocilia. Despite the presence of structural resonances in many of the proximate variables, the overall sensitivity of hearing varies smoothly with frequency and does not exhibit sudden changesiii. Understanding this dichotomy has been challenging.

5. The input and output variables

Which input variable, at the ear-canal entrance determines sensitivity? Which output variable characterizes changes in tension of the inner-hair-cell stereocilia? Possible candidates for the input variable are pressure measured with a microphone, volumevelocity (acceleration and displacement), power, or transmittance and reflectance. Since these variables are interrelated, it is difficult to truly separate the effects of one variable from another. However, the use of pressure has some advantages. Dallos (1973) showed that there is good agreement between hearing sensitivity measured behaviorally and the eardrum-to-cochlear pressure transfer function, also called the middle ear pressure gain resulting from ossicular coupling. It appears that the combined properties of the middle ear and its cochlear load are the dominant determinants of the animals measured behavioral sensitivity. This has been directly measured in cat (Nedzelnitsky 1980), guinea pig (Dancer and Franke 1979; 1980; Magnan et al. 1997), gerbil (Olson 1998) and human (Puria et al. 1997; Aibara et al. 2001; Puria 2003). In agreement with Dallos (1973), Puria et al (1997) show that there is 7

good correlation between the human middle ear pressure gain and behavioral threshold. This suggests that an important proximate variable, at least at the base of cochlea, is fluid pressure in the vestibuleiv. In the organ of Corti it is well accepted that tension in the tip links is the ultimate mechanical variable for the mechano-electric transduction (Corey and Hudspeth 1983; Howard and Hudspeth 1988). This tension opens ion channels and initiates the flow of ions through the stereocilia bundle resulting in depolarization of the hair cell body which results in firing of the auditory nerve. In the sections that follow we generally follow the path taken by sound from the external ear, through the middle ear, into the fluid filled cochlea. We then analyze the mechanisms that cause the basilar membrane and the organ of Corti to vibrate which then results in tension modulations of the hair cell stereocilia tip-links.

C. External ear
The external ear consists of the highly visible cartilaginous pinna flange, the cavum concha and the ear canal buried in the skull. It is generally accepted that sound source localization in a free field consists of two processes. The sound source azimuth is determined using interaural time or interaural intensity, whichever is the dominant, while sound source elevation is based on spectral cues from the pinna. There is significant variability in both size and shape of the external ear amongst mammals and the resulting pressure transformation from the free field to the tympanic membrane. Examples of anatomical variations include cone shaped pinna in cats to almost flat pinna in ferrets, numerous invaginations and protuberances of the pinna flange and concha, and changes in ear canal cross-sectional area often accompanied by bends in the canal. The ear canal and concha boost the sound field in the middle frequency range. A key role of the pinna is to diffract the sound in a spatially dependent manner and thus augment the sound field spectral cues. The torso also adds to elevation cues particularly at low elevations and low frequencies in the form of a shadowing effect (Algazi et al. 2002). A common measure of the effect of external ear function is the free field to tympanic membrane pressure ratio Ptm/Pff. When measured as a function of spatial angle, the magnitude of the ratio is often called the head related transfer function (HRTF). Not surprisingly, the effect of the anatomical structures on the HRTF is likely unique to each animal and varies significantly in individuals for a given species. The transformation of the free field sound pressure to that measured at the tympanic membrane is determined by diffraction, scattering, and resonances due to the asymmetric structures along the way. The frequency region where different structures become important occurs when the wavelength of sound becomes smaller than the physical dimensions of a feature of the external ear.

1. Concha and ear-canal resonance

Dimensionally, the largest feature of the human ear with some acoustic consequence is the ear canal, which is approximately 25 mm in length, and 7 mm in diameter with a 8

corresponding quarter-wavelength resonance near 2.5 kHz with an approximate pressure gain of about 10 dB (Bksy 1960; Shaw and Teranishi 1968; Shaw 1974). Significant developmental changes in the ear canal dimensions and wall properties take place even up to the age of 24 months (Keefe et al. 1993). The next larger feature is the concha with a height of 19 mm, a width of 16 mm and a depth of about 10 mm. There is significant individual variation in these dimensions with very little correlation between them or with other pinna dimensions (Algazi et al. 2001). The depth mode resonance in the 4-5 kHz range, results in a pressure gain of about 10 dB. Both the canal and concha-depth resonances are complementary effects and are approximately independent of angle of the free-field sound and produce a pressure gain that starts at about 1.5 kHz reaching a maximum gain of up to 20 dB near 3-4 kHz and then decreasing again. At frequencies above 5 kHz, the width and depth modes of the concha becomes important and excitation of these modes is dependent on the angle of incident sound (Shaw and Teranishi 1968; Teranishi and Shaw 1968).

2. Spatial diffraction by the Pinna

To a first order approximation, the pinna flange and the surface of the head mechanically behave as rigid bodies to acoustic waves. In humans and in some animals like ferrets the pinna is immobile while in other animals like mice and cats the pinna are mobile and able to move due to muscular control independent of the skull. Many of the mobile pinnae have a horn like structure, which improves their sound collecting ability. The larger cone may allow an effective interaural time delay that is greater than is possible for the head alone while the mobility allows for the possibility to modulate the interaural time difference (Shaw and Teranishi 1968). In humans the pinna is relatively large (64 mm x 29 mm) but it does not seem to be strongly correlated with a resonant mode (Algazi et al. 2001). One role for the larger pinna is to increase directivity and thus reduce background noise. There are several unique geometric features of the pinna that contribute to resonance modes at frequencies above 6-7 kHz. These modes are dependent on the angle of the incident sound and are clearly important for determining the HRTFs measured in individual subjects. The brain continually calibrates and interprets the HRTFs to infer the location of sound indicating that there is plasticity in the perception of the spectral cues (Hofman et al. 1998). This was demonstrated by modifying the pinna of adult human subjects with a prosthesis so as to disrupt the spectral cues resulting in poor spatial localization in the vertical plane. However, after a relearning period of about 30-45 days the subjects were able to localize accurately again. Furthermore, the subjects did just as well after removal of the prosthesis suggesting that the new cues did not interfere with the perception of previous cues.

3. Tympanic-membrane and ear-canal interface

The delicate tympanic membrane is located at the end of the long ear canal deep inside the skull likely for protection from mechanical damage. At frequencies above approximately 1 kHz the membrane response is very complex, while the cochlea provides a mainly resistive load (Onchi 1961; Mller 1963; Zwislocki 1963; Khanna and Tonndorf 1969; Lynch et al. 1994; Puria and Allen 1998). This resistive load is the primary

damping factor of the external ear resonances.

D. Middle ear
The ear canal is filled with air that is continuous with the free field. On the other hand the cochlea is filled with cerebro-spinal and other salty fluids. The mechanical properties of these media are shown in Table 1. What matters for effective wave propagation is the specific impedance, which is the product of density and wave-speed of the medium. Even though the fluid of the cochlea has mechanical properties close to saline, the flexibility of the cochlear partition greatly slows the wave speed, which causes a lower specific impedancev and an air-to-cochlea impedance ratio of about 1/200. Such a large impedance mismatch would cause most of the sound energy entering the ear canal to reflect and not enter the cochlea.
Table 1 Acoustical and mechanical properties of air, saline and the input widow to the cochlea.

medium

density ! (kg/m3) 1.29 1000 1000

speed of sound c (m/s) 350 1500 95 (approx)

Air Saline Cochlear input

specific impedance z = !c (Pa-s/m) 448 1.5x106 9.5x104

impedance ratio " =z/zcochlea 1/212= 0.0047 15.7 1

The above shows that the slower speed of sound in the cochlea fluid reduces the air to fluid impedance mismatch by a factor of 15.7 (24 dB). A simple model in Figure 1 illustrates this concept. The model consists of two semi-infinite tubes of cross-sectional areas A1 and A2, with the ratio # = A1/A2, filled with fluids with the densities !1 and !2 and speeds of sound c1 and c2. The acoustic impedances are z1 = !1c1 and z2 = !2 c2 , with the ratio " = z1/z2. The piston has one face in tube 1, and the other face in tube 2.

Figure 1: Greatly simplified model for the middle ear consisting of a piston connecting two acoustic tubes. Tube 1 represents the ear canal, with an incident wave and a wave reflected from the piston. Tube 2 represents the fluid filled inner ear with a transmitted wave.

The hypothetical piston is free from constraint and is massless, so the force on the two sides of the piston must be equal. An incoming acoustic wave in tube 1 (the ear canal)

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impinges upon the piston, causing the generation of a transmitted wave in tube 2 (the cochlea), as well as a reverse reflected wave in tube 1. The standard 1-D transmission line analysis for acoustic waves yields the ratios of the amplitudes of transmitted and incident pressure and energy:
p2 2! = p1in 1 + !"

E2 4!" = E1in 1 + !"

(Eq. 5)

The ratios for the areas of the tympanic membrane and the stapes footplate typical for human and cat give the results in Table 2. For conduction in air, the large ratio greatly improves the energy flowing into the cochlea. Since this is far from 100%, it is not impedance matching, but rather impedance mismatch alleviation. Perfect impedance matching #" = 1 would provide for humans only a 15 dB improvement in the transmitted pressure at the considerable cost of a 10 times larger tympanic membrane. It must be noted that larger areas enhance the signal-to-noise ratio at the hair cell level (Nummela 1995). So the large tympanic membrane is advantageous to human and cat for hearing in air. It is interesting to consider a change to hearing under water. For this, the air in tube 1 is replaced by water, which yields the results in the bottom section of Table 2. The acoustic pressure transmitted to the cochlea is greatly reduced to a value insensitive to the area ratio. The difference in pressure in air and water of 49 dB is close to the behavioral threshold difference measured in divers (Brandt and Hollien 1967; DPA 2005). This supports the simple relation in Eq. 5 as a fundamental consideration for the design of the middle ear.
Table 2 Effect of middle ear area ratio # and specific impedance ratio " in transmitting sound pressure and energy into the cochlea, according to the basic model in Figure 1. Replacing the air in the ear canal (tube 1) with saline simulates underwater hearing, which has a great reduction in the transmitted pressure. Tube 1 (EC) Air

" = z1/z2
0.0047

# = A 1/A 2
1 20 (human) 40 (cat) 212 1 20 (human) 40 (cat)

p2/p1 (lin)
2 36 67 212 0.12 0.13 0.13

p2/p1 (dB)
6 31 36 46 -18 -18 -18

E2/E1 (lin)
1.8% 25 53 100 22 1.7 0.6

Water

15.7

In Table 3 the amplitude of the incident sound wave at threshold is given for hearing in air and water (Fay 1988). The pinnipeds (marine mammals including sea lions, walruses, and true seals) spend time in both air and water and have hearing sensitivity worse than humans by a factor 10 (20 dB) in air and better by a factor of 5 (14 dB) in water. However, the cetaceans (whales and dolphins) have better hearing sensitivity in water than humans by factor of 54 (36 dB). It is interesting that the intensity of the sound at threshold is about the same for human in air and pinniped in water, and for human in water and pinniped in air. Obviously, the middle ear of the pinniped is designed for the

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water environment. Quite a different middle ear design provides the extraordinary sensitivity under water of cetaceans (Hemila et al. 1999).

Table 3 Some approximate thresholds of hearing in air and water. Pressure (Pa) 20 200 Air Intensity (Watts/m2) 8.9 x1013 8.9 x 1011 Pressure (Pa) 5400 1000 100 Water Intensity (Watts/m2) 2 x 1011 6.7 x 1013 6.7 x 1015

Human Pinnipeds Cetaceans

As the simple estimate indicates, without an effective middle ear, the sensitivity of the cochlea would be compromised and so would the overall bandwidth as is evident by pathological conditions of the ear repaired by otologists. As discussed in a subsequent section, another important role of the middle ear is in exerting some degree of dynamic range control at high input levels via the three sets of muscles. The simple model of Figure 1 is useful to certain degree but has significant limitations. In order to build an acoustic lever with an area change from the ear canal to the cochlea requires using biological materials consisting of bone and soft tissues. A rigid piston with a large area requires a large mass, which limits its ability to transduce sound particularly at the higher frequencies. A membrane is lighter but has a significant number of resonant modes particularly at frequencies above 2-3 kHz. In a very thorough study, Nummela (1995) show that malleus and incus masses scale with eardrum area, which further limits high frequency hearing. These factors must be considered when formulating mathematical models of the middle ear. More sophisticated models describing sound transmission in the middle ear have been around for some time. Early studies allocated various acoustic influences to the different middle ear structures interconnected in 5-6 functional blocks. The blocks were then assigned more detailed elements, which consist of masses, springs, and dashpots. Some of the earliest models by Onchi (1949; 1961), Zwislocki (1961), and Mller (1961) use dynamic analogies and represent the middle ear in the form of electrical circuit models. These phenomenological models have evolved and continue to be useful for understanding surgical interventions of the middle ear (Rosowski and Merchant 1995; Merchant et al. 1997; Rosowski et al. 2004). Nevertheless, they have limitations in that there is not a tight relationship between the underlying anatomical structure and function. To overcome these limitations requires models that explicitly incorporate morphometry of the middle ear into the formulation.

1. Tympanic membrane shape and internal structure

There remain many unanswered questions regarding the biomechanics of the tympanic membrane. For example, why does the tympanic membrane have a conical shape? Why do the tympanic membrane sublayers have a highly organized collagen fiber structure? What is the advantage of its angular placement in the ear canal? Why is there symmetrical malleus attachment to the eardrum in some animals while in others there is asymmetry? The functional significance of many of these gross anatomical features of the 12

tympanic membrane is just beginning to be understood and current status is discussed below. Helmholtz (1868) discussed the need for impedance matching of the air in the environment and the fluid of the inner ear and suggested that the tympanic membrane behaved as a piston. This assumption is widely used in lumped parameter (circuit) models of the middle ear, which build upon the free piston model (Eq. 5) by adding springs and the resonances of the malleus-incus complex and of the middle ear cavity. However, instead of piston behavior, surface displacement measurements revealed multiple modes of vibration for frequencies above a few kHz (Tonndorf and Khanna 1972). Since the toand-fro motion of a resonance mode would reduce the effective area for the sound pressure, the presence of these modes has been difficult to explain. Pioneering work by Rabbitt and Holmes (1986) formulated a continuum analytic model with asymptotic approximations for the cat tympanic membrane. They included the membrane geometry and anisotropic ultrastructure in combination with curvilinear membrane equations, but did not analyze the effects of the eardrum angle and the conical shape of the eardrum, nor have Eiber and Freitag (2002). Current finite-element models represent the eardrum as an isotropic membrane (Wada et al. 1992; Koike et al. 2002; Gan et al. 2004) and thus do not explain the need for the detailed fiber structure (Lim 1995). Two breakthroughs have increased our understanding of tympanic membrane mechanics. First, was the observation that there is significant acoustic delay in eardrum transduction (Olson 1998; Puria and Allen 1998). Second, the multiple modes of vibration seen on the surface of the eardrum are not transmitted to the cochlea. Rather, the pressure inside the cochlea as a function of frequency remains relatively smooth, even when measured at a high frequency resolution (Magnan et al. 1997; Puria et al. 1997; Olson 1998; Aibara et al. 2001; Puria 2003). Clearly these observations are tied to the complicated motions of the eardrum observed by Khanna and Tonndorf (1972) but need explanation.

2. Tympanic Membrane Biomechanics

To understand the functional consequences of the tympanic membrane structure on its sound transducing capabilities, a biocomputation model has been formulated which leads to some insights on the posed questions (Fay 2001; Fay et al. 2006). The model incorporates measurements of the geometry of the ear canal (Stinson and Khanna 1994), the 3-D cone shape of the eardrum (Decraemer et al. 1991), and details of the eardrum fiber structure (Lim 1995).

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Figure 2: Human eardrum photograph with its biomechanical model representation composed of adjacent wedges. The zoomed box shows the four layer composite of each wedge. The inner radial and circumferential collagen fiber layers, unique to mammals, provide the scaffolding for the tympanic membrane. Dimension and material property differences of the wedges lead to mistuned resonances at high frequencies. The thickness of the eardrum layers increases from the umbo to the tympanic annulus.

The discrete model for the human eardrum is shown in Figure 2, in which a series of adjacent wedges approximate the eardrum. Near the center, the eardrum is attached to the malleus, while the outer edge is attached to the bony annulus (not shown). The 1-D acoustic horn equation is used for a small cross-section of the ear canal. The change in area from the adjacent section, the curvature of the centerline, and the flexibility of the portion of the eardrum that intersects with that section of the ear canal are taken into account. Each strip of the eardrum has a curvature near the outer edge (locally a toroidal surface) and is straight in the central portion (locally conical). Because the main conical portion has few circumferential fibers, the approximation is that the radial strips are weakly coupled in the circumferential direction. The tympanic membrane is represented as a four-layer composite (Figure 2). The input 14

parameters for the formulation are the thickness of each layer as a function of position and the Youngs modulus of elasticity (a measure of resistance to deformation) for each layer. The outer most epithelial layer and the inner most submucosal layers are relatively flexible. Because the sub-epidermal layer and the sub-mucosal layers consist of connective tissue and are also relatively flexible, they are part of the epidermal and mucosal layers respectively (Figure 2). The inner two layers have collagen fibers that are radially oriented in one layer and circumferentially oriented in the layer directly below. These two layers, unique to mammals, provide the majority of the scaffolding for the eardrum and thus those layers mostly determine the compliance of the membrane. The mass on the other hand comes from overall thickness of the membrane. Quantitative measurements for cat were used for the overall thickness (Kuypers et al. 2005). From these measurements and from sparse measurements of collagen sublayers, the thickness of each sub layer was estimated for human (Figure 2) and cat (Fay et al. 2006; Fay et al. 2005). Direct measurements of the static elasticity of portions of the eardrum (Bksy 1960; Decraemer et al. 1980) indicate an effective modulus of elasticity of around 0.03 GPa. This was re-examined using three very different methods to determine the eardrum modulus of elasticity (Fay et al. 2005). First, constitutive modeling incorporating the Youngs modulus of collagen and experimentally observed fiber densities in cat and human were used. Second, the experimental tension and bending measurements (Bksy 1960; Decraemer et al. 1980) were reinterpreted using composite laminate theory. And third, dynamic measurements of the cat surface displacement patterns were combined with a composite shell model. All three methods lead to similar modulus of elasticity value of 0.1-0.4 GPa for near the center of the eardrum. The corresponding values near the outer edge are approximately ! these values due to the liner taper in the elastic modulus. In previous models the eardrum is treated as a single layer having a uniform elastic modulus resulting in a low value of elastic modulus (Funnell et al. 1987; Prendergast et al. 1999; Koike et al. 2002; Gan et al. 2004). In the four-layer model, the collagen fiber sub layer is much thinner than the overall thickness and hence the estimated elastic modulus is higher. The modulus of elasticity was combined with the sub layer thickness to formulate a complete model of the cat tympanic membrane. The calculation for the dynamic response of each strip was performed with an algorithm for elastic shells (Steele and Shad 1995), which has no restriction on wavelength along the strip.

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Figure 3: Effect of modification of the eardrum depth. (a) In the center is the anatomically normal eardrum. The zcoordinate of all the points is divided by a factor of 10 to obtain the shallow eardrum on the left, and multiplied by a factor of 2 to obtain the steep eardrum on the right. (b) Effect of eardrum depth on the middle ear pressure transfer function, which is the ratio in dB of the pressure delivered to the vestibule inside the cochlea (pv) divided by the input pressure in the ear canal (pec). The deep eardrum calculation is nearly the same as the normal, but the shallow eardrum has more than a 20 dB loss at higher frequencies. For the normal and deep eardrums, the phase delay is steeper than it is for the shallow drum, indicating more acoustic delay. (Reproduced from Fay et al., 2006 with permission).

The full 1-D interaction of the air in the ear canal and the eardrum is included. Behind the eardrum are the middle ear cavities and the middle-ear bones connected to the cochlea, for which lumped-element approximations were used. Verification involved mesh refinement studies, comparison with exact solutions for limiting cases, anatomical values of geometry, best estimate for elasticity, and comparison with physiological measurements to 20 kHz, all for the cat middle ear. Different depths of the eardrum play an important role as shown in Figure 3. With a shallow eardrum (no cone shape) there is a loss of more than 25 dB for frequencies above about 4 kHz (Figure 3b, top panel). A deep eardrum shows a response similar to that seen in anatomic specimens, with little loss for low frequencies. Above 4 kHz, the phase for the normal and deep eardrum continues to decrease while for the shallow drum the phase tends to go in the opposite direction and increases. This suggests that there is more phase delay for the deep and normal shape than for shallow eardrums. In comparison to the

16

normal eardrum the deep drum requires more real estate in the skull, which competes for space with other organs. The effect of the two collagen-fiber sub-layers was also analyzed. This was done by examining the effects of isotropic eardrums that had the same stiffness in the radial and circumferential directions and orthotropic eardrums where there were radial fibers but no circumferential fibers (Fay 2001; Fay et al. 2006). Results indicate that there is an advantage of the orthotropic microstructure with a dominance of radial fibers in the central region. In the normal drum when both are present, the radial fibers on the inner portion of the tympanic membrane result in an effectively orthotropic membrane while the outer circumferential fibers provide a low-impedance beam-like support. The orthotropic central portion allows maximal sound transmission at both low and high frequencies. The model calculations indicate that sound transmission from the ear canal to the cochlea varies smoothly despite the fact that there are a significant number of resonances at different points on the eardrum. This suggests a design where drum sections are deliberately mistuned. Because these resonant points are added together at the malleus, no single mode ever dominates. Thus the ensemble of eardrum modes produces a relatively large and yet fairly smooth response at the malleus at the higher frequencies. Understanding of eardrum biomechanics is of critical importance to the development and improvement of myringoplasty which is a surgical procedure for repairing damaged eardrums. The underlying disease process is often chronic inflammatory disease of the middle ear and mastoid, referred to as chronic otitis media (COM), which leads to a partial or total loss of the tympanic membrane or ossicles. Clinically, isotropic materials like temporalis fascia are used for myringoplasties. To improve hearing results at the higher frequencies, orthotropic material with collagen scaffolding preferentially oriented in the radial direction would be a better choice for improved high frequency hearing outcomes. Improving post-operative high frequency results may be important for the perception of sound localization cues present at high frequencies. Currently the standard practice is to measure clinically to 6 kHz. The above results suggest that clinical measurements at frequencies above 6 kHz might better show the effects of different materials. Since the modulus of elasticity and the biocomputation approach using asymptotic methods is already developed for the cat, the challenge will be to estimate eardrum morphometry for other species such as human (Figure 2 shows an approximate guess). Of particular interest is determining how the shape and thickness of the tympanic membrane varies from subject to subject. Such quantification will allow for the possibility of using the eardrum biocomputation on individual subjects. Non-destructive high-resolution imaging methods are needed to obtain morphometry on individual subjects. A promising new imaging technology is described in the next section.

3. Middle ear imaging

To obtain morphometry of the ear, histological methods have been the primary technique. However, this age old technique is destructive and certainly not appropriate for in-vivo imaging of individual subjects. One of the most recent advances for obtaining anatomical information is micro computed tomography (microCT). This has been used to

17

obtain volume reconstructions of the temporal bone of living subjects at a resolution of less than 125 "m (Dalchow et al. 2006). In-vitro resolution can be increased by an order of magnitude (Decraemer et al. 2003).

Figure 4: MicroCT image of an intact cadaver temporal bone. This is image #769, of 1897 images spanning a length of 28.455 mm. The image illustrates that most of the middle ear structures can be visualized from an intact temporal bone ear scan. The resolution for both in-plane and out-of-plane (slice thickness) is 15 m. The tympanic membrane although visible is faint, suggesting that the basic geometry and an approximate thickness can be obtained. The 30.72 mm scan diameter outline is clearly seen.

Figure 4 shows an image slice from an intact human cadaver temporal bone ear. The image resolution in the x, y, and z planes is 15 m (iso-volume). Most of the middle ear structures, including the tympanic membrane cone shape and thickness, ossicles, and suspensory soft tissue, can be visualized because there is good density contrast between these structures and air in the ear canal and middle ear cavity. Because they provide the best resolution, histological methods remain the standard. However, CT imaging offers some distinct advantages (Decraemer et al. 2003). These include: (1) elimination of stretching distortions commonly found in histological preparations, (2) use of a nondestructive method, (3) shorter preparation time (hours rather than 12-16 months), and (4) results already in digital format. This imaging technology is rapidly evolving and it is likely that similar resolutions will be possible for in-vivo imaging in the near future.

4. Malleus-incus complex
The middle ear of most non-mammalian terrestrial animals consists of the tympanic membrane and a columella, while mammals have a tympanic membrane and a malleusincus complex. Amongst vertebrates a great majority of mammals are sensitive to ultrasonic sounds (above 20 kHz), while non-mammals are notvi. This suggests that the mammalian hearing organ evolved to be a superior organ for high-frequency response compared to that of non-mammals and that the incorporation of the malleus-incus complex may have something to do with this capability (Fleischer 1978; 1982). However, the biomechanics of this sub system of the middle ear are not well understood. Since the time of Helmholtz (1868) the handle of the malleus and the long process of the incus were described as the two arms of a lever with a fixed axis. Ossicle suspension also further supported the notion that the malleus and the incus rotate about a fixed axis

18

while driving the stapes in a piston like manner. However, detailed measurements of the ossicles have changed this view (Decraemer et al. 1991; Decraemer and Khanna 1995). The malleus motion changes with frequency and all 3-D components of translation and rotation are present at biologically relevant stimulation levels. These measurements suggest that a full 3-D model of ossicle motion is required. Between the malleus and incus is a saddle-shaped joint formed from an indentation in the head of the malleus into which the surface of the body of the incus fits (Figure 5). The incus also has a depression into which a part of the malleus head fits, forming a cog-like mechanism as described by Helmholtz (1868). The significance of such a mechanism is thought to be a locking of the joint causing one part to move with the other during rotation in one direction but leaving the parts free to rotate in the orthogonal direction (Wever and Lawrence 1954). However, measurements (e.g., Helmholtz 1868; Bksy 1960) suggested that the incus and malleus are fused together indicating that there is no slippage at the incudo-malleolar joint (IMJ). Making measurements in the cat ear, Guinan and Peake (1967) showed clear evidence of slippage at the IMJ above about 8 kHz. Using time-averaged holography measurements Gundersen and Hgmoen (1976) concluded that the malleus and incus rotate like one stiff body for frequencies below about 2 kHz. Due to these measurements, mathematical models of the human middle ear generally treat the two ossicles as fused and do not include slippage (Goode et al. 1994; Koike et al. 2002). More recent measurements suggest slippage between the incudo-malleolar joint and lack of slippage in previous measurements was possibly due to methodological reasons including a possible lack of a cochlear load and insensitive measurement techniques (Willi et al. 2002). In some animals, like guinea pig and chinchilla, the IMJ is fused and thus there is no slippage (Puria et al. 2006). On the other hand, there is no controversy regarding slippage at the joint between the incus and the stapes, and most mathematical models currently include it (e.g., Goode et al. 1994). Natural mode shape calculations indicate that the ossicles can be treated as rigid bodies only for frequencies below about 3.5 kHz (e.g., Beer et al. 1999). Consequently, the ossicles have been modeled as finite elements, which require much more computation time. An alternative approach is to model the ossicles as elastic bodies incorporating just the first two or three modes in each body (Sim et al. 2003). Not unlike the biological ligaments found in other parts of the body, the suspensory ligaments and tendons of the middle ear are a composite, consisting of collagen and elastin embedded in an amorphous intercellular material often called ground substance or matrix which is composed of proteoglycans, plasma constituents, metabolites, water and ions. Almost two-thirds of the weight of ligaments is water, while about three-quarter of the remaining weight can be attributed to the fibrillar protein collagen (reviewed by Weiss and Gardiner 2001). Like the eardrum, the primary component resisting tensile stress in ligaments and tendon is collagen. The primary role of the ground substance is in maintenance of the collagen scaffolding. As such, the biomechanical behavior of a ligament is determined by its geometry, shape of the articulating joint surfaces, orientation and type of insertions to bone, in-situ pretension, and material properties. What role do the suspensory ligaments play in the complicated 3-D vibrations of the middle ear bones? This question has yet to addressed with any degree of satisfaction. In the cat study discussed above, a simple ball and stick model for the malleus-incus complex was used (Fay et al. 2006). This was a gross simplification but allowed 19

concentration on the tympanic membrane biomechanics. A goal of several laboratories is to combine anatomical data with human cadaver temporal bone malleus-incus complex 3D motions into a computational model for individual ears, which should increase understanding of the functional consequences of the anatomy of the ossicles and suspensory ligaments and tendons. a) b)

Figure 5 : Volume reconstruction of the malleus and incus from uCT slices. (a) The incus is made transparent to allow better visualization of the incudo-malleolar joint. (b) The incudo-malleolar joint saddle shape and thickness map (0 is dark green while about 300 !m is red).

The biomechanical characterization of the malleus-incus complex requires morphological and dynamical measurements from individual ears. The center of mass, moments of inertia, anatomical location and orientation of the ligaments and tensortympani tendon, are obtained from 3-D volume reconstructions (Figure 6) based on CT images of the isolated preparation.

Figure 6: Three-dimensional volume reconstruction of the malleus, incus, suspensory ligaments and the tensor tympani tendon. The soft tissue is represented as tapered cylinders or as a polyhedron. The origin is at the umbo. All dimensions are in mm.

The morphometry is used to construct a computational biomechanical model for the malleus-incus complex that includes ligament and tendon attachments to the bony walls and muscle, and slippage at the incudo-malleolar joint. Bending of the malleus and incus 20

handles is also allowed. The viscoelastic parameters of each ligament, tensor tympani tendon, and the incudo-malleolar joint cannot be determined from the morphometry and thus 3-D motion measurements are required. As discussed in previous sections, the biomechanics of the tympanic membrane can be fairly complicated. This implies that the input to the malleus-incus complex is also relatively complicated and thus it is difficult to deduce the dynamics of ossicles and soft tissue attachments with the sound driven eardrum. To better understand ossicle dynamics an isolated malleus-incus complex preparation was developed where the tympanic membrane and the stapes were dissected. Without an eardrum or a cochlea, the middle ear bones have to be directly driven. A tiny magnet and a coil around the tympanic annulus were used to drive the malleus-incus complex (Sim et al. 2003). The magnet on the tip of the malleus is oriented to drive it in the forward direction. The preparation is placed on a set of goniometers and malleus-incus motion measurements made at several points at several different angles. The resulting three-dimensional x, y and z vector components of velocity at each point is used within the biomechanical model to obtain the soft tissue viscoelastic parameters. The 3D volume reconstruction of the magnet and coil combined with electro-magnetic theory allows accurate calculation of the 3D forces and moments exerted by the magnet to the malleus. The combined, imaging, physiology and biomechanics approach should help us better understand the structure and functional relationships at audio frequencies in normal and pathological ears. The above discussion concerns the dynamics of the malleus-incus complex. At high positive and negative static pressures such as during sneezing and coughing the suspensory ligaments may also play a critical role (Huttenbrink 1989). Incorporation of this mode of operation requires extension of the linear models to non-linear models.

5. Lenticular process
The inferior end of the long process of the incus terminates in a short perpendicular bend called the lenticular process consisting of the pedicle and the lenticular plate surrounded by soft tissue. Between the lenticular plate and the stapes head is the incudostapedial joint. Motion from the incus is transmitted to the stapes via this process and thus its mechanical description is of significance. Most previous modeling work has treated the lenticular process to be a rigid bone that transmits the incus motion directly to the stapes head or with a slippage representing the incudo-stapedial joint (Beer et al. 1999; Koike et al. 2002). Recent anatomical measurements suggest that the plate-like bony pedicle is perpendicular to the lenticular plate and is extremely thin and fragile. In cat the dimensions of the pedicle are 240 m x 160 m x 55 m (Funnell et al. 2005). Model calculations of static displacements suggest that there is significant relative motion between the incus long process and stapes head (Funnell et al. 2005). Funnell and colleagues have hypothesized that one role for the thin pedicle and lenticular plate arrangement may be to convert the rotational modes of vibration of the incus into translational motion of the stapes. More work is needed to further test this hypothesis. It has been observed that at high static pressures, there is a large lateral displacement of the lenticular process and this serves to protect the cochlea from large motions (Huttenbrink 1988). Clearly, bending of the pedicle may be involved.

21

6. Stapes
The interface between the malleus-incus complex and the vestibule of the fluid filled cochlea is the stapes, which is held in place in the oval window (Fenestra vestibule) by the annular ligament. The mechanics of the stapes is quite independent of the malleusincus complex and of the cochlear fluid load. For this reason the stapes can be considered a semi-independent sub system of the mammalian ear (Fleischer 1978). This treatment of the stapes is widely accepted (Wada and Kobayashi 1990; Wada et al. 1992; Goode et al. 1994; Puria and Allen 1998; Beer et al. 1999; Koike et al. 2002).

7. Ossicular reconstruction
While we are discussing the ossicles this is good place to discuss ossiculoplasty, which is the reconstruction of the middle ear bones to improve hearing sensitivity. Two of the most common pathologies are missing (or eroded) incus and ossified stapes. Both result in significant conductive hearing loss. Since the introduction of these surgical procedures more than fifty years ago, ossiculoplasty continues to pose significant challenges to otologists. The interposition of passive prostheses between the malleus or tympanic membrane and the stapes head or footplate is used to reconstruct the transfer function of the middle ear in the missing or eroded incus condition. These are the incus replacement prostheses. Two types, depending on the circumstance, are the partial ossicular reconstruction prosthesis (PORP) to the stapes head while another is the total ossicular reconstruction prosthesis (TORP) to the stapes footplate. The PORP is typically used if there is an intact stapes superstructure. However, ear canal pressure to cochlear pressure transfer function and clinical measurements suggest that even if the stapes superstructure is present there are acoustico-mechanical advantages to placing the foot of the prostheses on the footplate (Murugasu et al. 2005; Puria et al. 2005). In a very different disease process called otosclerosis, the stapes becomes fixed to the surrounding oval window through ossification. The immobile stapes prevents sounds from entering the cochlea and results in significant hearing loss. The precise cause of otosclerosis is not well understood. However, it is becoming well established that otosclerosis is hereditary. Otolaryngologists repair the condition by a procedure called stapedotomy. A hole is made in the footplate often with a surgical laser (Perkins 1980) and then covered with soft tissue to prevent the inner ear fluid perilymph from leaking out. Sound transmission is restored with a piston like prosthesis. One end of the prosthesis is crimped to the long process of the mobile incus while the other end is inserted in the covered artificial hole in the footplate.

8. Middle-ear muscles
The malleus and stapes each have a tendon attached to a tiny muscle, the tensor tympani muscle and the stapedius muscle respectively. The muscles contract when exposed to high level sounds and are part of the middle ear reflex arc involving the spiral ganglion neurons, the auditory nerve, cochlear nucleus, the superior olive, the facial nerve nucleus, the facial nerve and the two middle ear muscles (Margolis 1993). This reflex arc can reduce sound transmission through the middle ear at high levels and may serve to control the dynamic range of the auditory system and to protect the cochlea at

22

high sound levels. The reflex is slow and thus does not provide protection to the cochlea against sudden impulsive sounds. The time for the stapedius reflex may be on order of about 20 ms while the tensor tympani arc is more than ten times slower. Two additional functions are attributed to the middle ear muscle reflex. Low frequency sounds, particularly when they are high in level, normally tend to mask mid and high frequency sounds due to their upward excitation patterns on the basilar membrane. One role of the middle ear muscles is to reduce the level of low frequency inputs so they do not mask the higher frequency sounds on the basilar membrane (Pang and Guinan 1997). A second role of the middle ear reflex is in the reduction of the audibility of generated sounds during speech, mastication, yawning and sneezing (Simmons and Beatty 1962; Margolis and Popelka 1975). Because the reflex arc involves so many mechanisms, its measurement is clinically used to diagnose central and peripheral pathologies. Recently it has been discovered that there are smooth muscle arrays on the peripheral edge, annulus fibrous, of the tympanic membrane in all four (bats, rodents, insectivores, and humans) of mammalian species studied (Henson and Henson 2000; Henson et al. 2005). The role of this rim of contractile muscle cells in the par tensa region is not clear, but two suggested possibilities are to maintain tension of the tympanic membrane and to control blood flow to the membrane (Henson et al. 2005). Measurements indicate that these smooth muscles can exert control over the input to the cochlea as measured by cochlear microphonics (Yang and Henson 2002).

9. Middle-ear cavity
One role of the middle-ear cavity is to act as a baffle for the tympanic membrane so that sound does not impinge on both sides of the eardrum. Without this, the sensitivity of the membrane, and thus hearing sensitivity, would be significantly reducedvii. However, the presence of the cavity results in an increase in overall impedance, due to volume compliance, at low frequencies and resonant modes at high frequencies. An increase in middle ear impedance results in a decrease in hearing sensitivity (Wiener et al. 1966). In humans the middle ear cavity is relatively large but is irregular in shape. The mastoid cavity portion has many air cells, or air pockets, that results in an increase in surface area. Each cell is lined by a mucous membrane of thin epithelial cells. It is thought that the irregular shape minimizes resonant modes and the air cells effectively dampen remaining resonance (Fleisher, 1978).

10.

Middle-ear acoustic load

The primary load to the middle ear is the acoustic input impedance of the cochlea Zc. As defined by Zwislocki (1975), Zc is the ratio of sound pressure in the scala vestibuli at the stapes footplate to the volume velocity of the footplate. Based on simplifications to the equations of motion at the base of the cochlea, Zwislocki (1948; 1965; 1975) predicted that the cochlear input impedance is primarily resistive. Direct measurements in the cat (Lynch et al. 1982), guinea pig (Dancer and Franke 1980), and human cadaver ears (Aibara et al. 2001) suggest that the prediction by Zwislocki was essentially correct for a broad range of frequencies. Zwislockis calculation had not included effects from the apical region of the cochlea. Calculations of the cochlear input impedance in the constant scalae area standard box

23

models of the cochlea, that include the apical region, shows that below approximately 1-2 kHz, the cochlear input impedance magnitude decreases and becomes more mass like. This calculated result diverges from the measured data and from Zwislockis prediction (Puria and Allen 1991; Shera and Zweig 1991). The decrease in the acoustic impedance and mass like response is shown to be due to the use of constant cross sectional area for the scala vestibule and scala tympani in all standard box models. Using a more realistic scalae area that decreases from base to apex of the cochlea avoids the diverging catastrophe in the model calculations of cochlear input impedance at low frequencies. The resistive nature of the cochlear input impedance, which is the primary damping component of sound transmission in the middle ear, has two consequences. Foremost is that a large fraction of the acoustic energy that enters the cochlea is absorbed by it rather than being reflected by it. Second, is that it smoothes out the peaks and valleys resulting from any resonances in the middle ear structures.

E. Cochlear hydrodynamics
In the preceding section, methods of imaging, physiology, and computational biomechanics were presented in the context of understanding the relationship between acousto-mechanical transformations of sound by the middle ear. The end result is that the proximate output variable of the middle ear, which is the vestibule pressure at the base of cochlea, smoothly varies with frequency and typically with pressure gain for a wide bandwidth relevant to the specific species. In the following sections we analyze how sound energy at the base of the cochlea propagates in the cochlea. Much effort has been devoted to this topic, on which many survey papers have been written, as represented by Allen and Neely (1992), Nobili et al. (1998), and deBoer (1991). DeBoer (2006) provides a summary of current thought. In addition, other articles in this Handbook address different aspects of cochlear function. Our focus is on what appear to be key acoustomechanical mechanisms that have a basis in the physiology.

1. Vestibule pressure
A simple description of what happens to the pressure transmitted into the cochlea by the middle ear is shown in Figure 7 for a given frequency. This represents a standard tapered box model for the cochlea with two symmetric fluid ducts divided by a partition. The stapes provides the input pressure. The wall of the cochlea is bone, which is normally assumed to be rigid, so for air-conducted sound the stapes and round window have equal and opposite volume displacement, preserving the volume of fluid in the cochlea. However, a very compliant membrane covers the round window, so the fluid pressure at this point is nearly zero. Therefore the total pressure is divided into an even and an odd solution (Peterson and Bogert 1950), as indicated in Figure 7. The even distribution must cause a compression of the fluid. This corresponds to a wave that travels with the speed of sound in the fluid, which is relatively fast. The odd solution produces net pressure acting on the partition that causes an elastic deformation of the flexible portion of the partition, the basilar membrane (BM). This interacts with the fluid motion, causing a wave that is relatively slow. This slow wave is the traveling wave first observed in the guinea pig by Bksy (1952). Because the BM is narrow at the stapes and wide at the apex, there is a gradient in stiffness of the partition, which causes 24

the traveling wave to have a long wavelength near the stapes, then build up to a maximum as the wavelength becomes short. In the very short wavelength region, the viscosity of the fluid causes this wave to die out exponentially. The traveling wave is so slow, relative to the fast wave, that the fast wave can often be approximated as instantaneous, i.e., for incompressible fluid. For simplicity, we consider the properties of the partition to be continuous. The actual tissue consists of discrete elements. As shown by Bksy (1960, p. 510) by models with coupled, discrete elements, behavior similar to that of a continuous system can be obtained. This holds, of course for wavelengths of response that are long in comparison with the spacing between elements. Many authors use discrete systems directly for advantage in computation and/or construction. The description in Figure 7 for the spatial distribution for a fixed frequency also holds for the waves seen at a fixed point as frequency varies. For frequencies less than the best frequency (BF), the slow wave has long wavelength, and for frequencies greater than BF, the slow wave decays to negligible magnitude, leaving only the fast wave.

Figure 7: Simple tapered box model for the pressure in the cochlea. The fluid regions scala vestibuli (SV) and scala tympani (ST) with tapered areas are divided by the partition containing the elastic basilar membrane (BM). At the apex the partition has an opening, the helicotrema. The input sound pressure acts at the round window (stapes). The response for a single frequency is divided into an even (symmetric) solution with equal pressure in SV and ST, and an odd (asymmetric) solution with the pressures in SV and ST of opposite sign. The symmetric solution causes a compression of the fluid, so the wave travels with the speed of sound in saline, which is the fast wave in the upper drawing. In contrast, the asymmetric solution has a net pressure on the partition, which causes a displacement of the BM that slows the wave considerably. This is the slow wave in the lower drawing. Because of the taper of the BM the stiffness changes and the slow wave has a wavelength that is long near the input but becomes short near the region of maximum amplitude. The driving frequency is the best frequency (BF) for this place. In the region of short wavelength, the fluid motion is 3-D, with a pressure that is maximum on the BM and decays exponentially with both the distance from the BM and the distance toward the apex. The round window is compliant, so the total

25

fluid pressure at that location is nearly zero. Thus at the input end, the pressures from the slow and fast wave must cancel in ST and so are equal in magnitude.

The first direct evidence for this behavior is provided by the measurement of pressure in the gerbil (Olson 1998) at a distance 1.2 mm from the stapes. Some of the experimental values are shown in Figure 8, along with calculated values from a 3-D cochlear model to be discussed later. Near BF the pressure is strongly dependent on the distance from the BM, with much larger values near the BM (Figure 8a). This shows the 3-D behavior of the fluid in the short wavelength region. For low frequencies, the pressures at the different distances from the BM converge, showing the long wavelength region. The phase response shows the near cancellation of the waves for low frequencies (Figure 8b). For higher frequencies the slow wave dominates, and the rapid accumulation in phase is characteristic of a traveling wave. For even higher frequencies, the traveling wave disappears, so all that is left is the fast wave with constant phase, which at different distances from the BM differ by one cycle, so these are in fact the same. The phase measurements show that far from the BM (305 m) the traveling wave quickly disappears, while the points closer (3 228 m) all have the same phase. In contrast, the calculation shows differences at these points. This may be due to the large pressure probe interfering with the fluid motion, which is only simulated in the calculation by taking the average of the pressure at nine points in the 100 m diameter of the probe. This is for 80 dB SPL input eardrum pressure. The measured pressure shows a constant value for high frequency equal to 100 dB SPL. This corresponds to the 80 dB input to the eardrum, with a 26 dB gain through the middle ear, and a 6 dB drop because the fast wave has half the amplitude of the vestibular pressure at the stapes.
Figure 8 (a): Pressure magnitude in the cochlea at the distance 1.2 mm from the stapes in ST measured in the gerbil (Olson 1998) and calculated (Baker 2000). For frequencies higher than BF (> 40 kHz), the slow wave is negligible and only the fast wave remains (Figure 7). For low frequencies, the fast and slow waves nearly cancel in ST. Near BF (25 kHz), the fast wave dominates, with 3-D fluid motion that has much higher pressure near the BM. The discrete points x show the measurements at the distances from the BM of 3 and 305 m, while the calculated values, shown by the continuous curves, include distances in between. Figure 8(b): Pressure phase relative to the simultaneously measured scala vestibule pressure at the base of the cochlea. For frequencies above BF (> 40 kHz), only the fast wave remains. The plateaus differ by one cycle, which shows that the fast wave is uniform with distance from the BM and exactly in phase with the eardrum pressure. For low frequency, the phases at the different distances from the BM are

26

also the same, corresponding to the fast wave and the long wavelength region of the slow wave. For frequency approaching BF (25 kHz), the slow wave dominates and shows the rapid decrease in phase signifying the traveling wave.

2. Partition resonance
At one time or another almost every component of the cochlea has been suggested as a key tuned resonator that will cause a significant local response for a given frequency (the BF in Figure 7). The basilar membrane (BM) is the thin compliant portion of the partition that divides the two fluid ducts in Figure 7. The component for which the tuning can be best related to the physical dimensions is the pectinate zone of the BM. Mathematical treatments of the BM include both bending stiffness and tension in addition to their interaction with the surrounding fluid. From the mathematical formulation, the frequency range and the place to frequency map of the cochlea given the anatomical dimensions with material properties can be predicted.

a) Plate
A cross section of the basilar membrane is sketched in Figure 9. For many mammals, the BM pectinate zone consists of a sandwich of collagen fibers in the radial (y) direction embedded in amorphous ground substance. For the same amount of material thickness, the sandwich provides increased bending stiffness. For simplicity, the details of the sandwich are omitted, and only the motion in the cross section (yz plane) is considered. For such a plate, the equation of motion in response to an applied pressure is:
D !4 w !2 w !2 w " T + # t = "2 pF P P !y 4 !y 2 !t 2
(Eq. 6)

in which w is the displacement of the plate, T is the tension, !P is the plate density, tP is the plate thickness, pF is the pressure in the fluid above the plate, which is doubled in Eq. 3 6 for fluid above and below the plate, and the bending stiffness is D = f Et P 12 , where E is the Youngs modulus of the fibers and f is the volume fraction of the fibers. For hinged edges at y = 0 and b, the solution is:
w = We j! t sin ny
n =! /b
(Eq. 7)

in which W is the amplitude and $ the frequency. For static loading and for zero tension, the results for the volume stiffness and point load stiffness are:

27

K Vol =

2 pF ! = Dn5 bw 8

kPtL =

P 48 Dd = W b3

(Eq. 8)

where w is the average displacement, and P is the magnitude of a load on a probe at the center with diameter d. With all terms retained, Eq. 6 gives the impedance, the relation !: between the pressure and velocity v = w

Dn4 + Tn2 ! tP "P# 2 2 pF =! v j#

(Eq. 9)

Figure 9: Cross section consisting of an elastic plate in vacuum with tension T. The plate thickness is t and the width between the support points is b. The resonant 1/ 2 frequency is proportional to T / tb 2 . The dashed line shows position of the plate. the

( ( ))

deformed

Figure 10: Cross section consisting of an elastic plate in infinite fluid. When the density of plate and fluid are the same, the plate density is negligible, and the resonant frequency is proportional to

(ft

b5

1/2

where f is the volume fraction of

BM fibers.

b) Fluid
The BM is mainly covered with soft cells that are in contact with extra-cellular fluid. For the effect of the mass on the pressure distribution, there is little difference between fluid, soft cells or a gel. As demonstrated by Bksy (1960, p. 445) in an experimental model there is no change in localization when the fluid is replaced by gel. Consequently, for modeling, the soft cells are often replaced by fluid. Both have similar acoustical properties. The motion of an inviscid, incompressible fluid (or gel) is governed by the well-known Laplaces equation:
! 2" ! 2" + =0 !2 y !2 z
(Eq. 10)

in which ! is the displacement potential. The z-displacement and pressure are:

!" w= !z

# 2$ pF = ! "F 2 #t

(Eq. 11)

The solution giving the compatible displacement with the plate (Eq. 7) is:

28

!="
which gives the ratio of pressure to velocity:

W j# t " nz e sin ny n

(Eq. 12)

pF "# = ! F = j "F# teffective v in

t effective =

1 = b /! n

(Eq. 13)

Thus the inviscid, incompressible fluid has only the effect of a mass attached to the plate, with the effective thickness t effective , about a third of the plate width b. Soft cells or a gel, representing the organ of Corti, also satisfy the same equation, so Eq. 13 holds for the fluid consisting of a thin or thick layer of soft cells and fluid. The difference between the fluid with and without cells attached to the plate lies in the viscous correction, not the effective mass.

c) Plate and fluid

Equating the impedance of the plate (Eq. 9) to the impedance of the fluid (Eq. 13) gives the resonant frequency:

!2 =

Dn4 + Tn2 "P tP + 2 "F n

(Eq. 14)

Helmholtz (1868) proposed that the transverse fibers of the BM behaved as strings under tension in air, as in a harp. This corresponds to setting the bending stiffness D and the fluid inertia !F to zero in Eq. 14. A sketch of this is in Figure 9 and the result for the first resonant frequency is:
frequencyTension 1" T % = $ 2 # !P tb2 ' &
1/ 2

(Eq. 15)

However, there is not much evidence for high tension in the BM and the density of the surrounding fluid is nearly the same as the BM. Consequently, the plate density term in Eq. 14 is negligible. Setting the tension T and the plate density !P to zero in Eq. 14 gives the resonant frequency:
frequency Bending 1 # Dn5 & = ( 2! % $ 2 "F '
1/ 2

1 # E! 5 & = ( 2! % $ 24 "F '

1/ 2

# ft 3 & % b5 ( $ '

1/ 2

(Eq. 16)

With the BM dimensions and density of fibers (Cabezudo 1978) Eq. 16 provides a reasonable frequency range for several mammals (Steele and Zais 1983). The formula also works for recent measurements of the gerbil (Emadi et al. 2004). The wide frequency bandwidth capability for the bending (Eq. 16) compared to the tension (Eq. 15) is shown in Table 4. With a nominal Youngs modulus of elasticity for collagen, the frequencies computed from Eq. 16 are close to the range for the guinea pig. In contrast, a variation of tension by 104 would be required for the tension model to work, which is not

29

justified by the modest change in the dimensions of the BM support. Shown in Table 4 is the width g of the spiral ligament. The tension is assumed to be proportional to g, and the tension frequency is set equal to the bending frequency at the apex for comparison. The conclusion is that it is bending stiffness that determines the frequency localization on the BM.
Table 4. Frequency range capability of BM pectinate zone (for guinea pig) for bending stiffness and tension stiffness.

Elastic modulus E BM fiber vol fract f BM width b BM thickness t Spiral ligament width g Frequency tension Frequency bending

Base 1 GPa 0.08 80 m 7 m 200 m 247 Hz 52,000 Hz

Apex 1 GPa 0.01 180 m 1 m 40 m 130 Hz 130 Hz

Ratio 1 7 0.44 7 5 1.9 400

3. Vestibular fluid pressure to BM displacement

The equations for the slow wave, (Figure 7) in the model with symmetric SV and ST without Reissners membrane (e.g., Peterson and Bogert 1950; Zwislocki 1953) can be written as:

! !2 ( Ap ) = " #F 2 Q !x !t
! 1 Q = "#A = " 2 pBM !x K Vol

(Eq. 17)

(Eq. 18)

The distance along the BM from the stapes is x, the average pressure in SV is p , the pressure acting on the BM is pBM , the volume displacement of fluid in SV is Q, the area of SV is A(x), and the area displacement of the partition is !A = bw . Equation 17 follows directly Newtons second law of motion (Eq. 1) while Eq. 18 is a statement about conservation of mass in a segment of scalae. The equations above are valid for 1-D, 2-D and 3-D description for the fluid flow by incorporating the dimensionality into the pressure pBM acting on the BM.

a) One-dimensional (1-D) approximation

For long wavelengths, the pressure is nearly constant on the cross section, so the approximation is pBM = p , and the system is a standard transmission line wave equation. For a single frequency, with all variables changing with e j! t , this reduces to:

d2 ( Ap ) + m 2 ( x, ! ) ( Ap ) = 0 2 dx

(Eq. 19)

30

where the coefficient is:

2 "! 2 m ( x, ! ) = AK Vol ( x )
2

(Eq. 20)

which can be identified as the local wave number. The wavelength is proportional to the reciprocal of the wave number. For the cochlea, K Vol decreases with distance from the stapes, so m increases with distance, meaning that the wavelength becomes short. Because of the simple interpretation, the 1-D approximation continues to be the most widely used for cochlear modeling. Zwislocki (1953) and then later Dallos (1973) provide the history of the development. To improve the results, damping and mass are added to the stiffness, as in Eq. 2. However, these values have no physical basis, so this must be considered as a phenomenological model. Another approach is to ignore the physical basis completely and determine the complex wave number m ( x, ! ) from measurements of BM displacement phase and amplitude, and the neural response, so that Eq. 19 will produce the measured response. This is often used in studies of the function of higher neural centers, for which a simple but reasonable input from the cochlea, described by Eq. 19, is desired. Flanagan and Bird (1962) developed this approach using Bksys post mortem measurements of the GP cochlear response. Of interest is their use of the Hilbert transform to show that the measurements are consistent for a causal and stable system. Zweig (1991) further developed the approach for the in vivo measurements of Rhode (1971) in squirrel monkey and obtained self-consistent effective BM impedance. Although the physical behavior is 3-D, the traveling wave can indeed be described by an equation of the form Eq. 19. So the choice is to fit the wave number from the measurements of the response or compute it from the actual stiffness and mass properties of the BM with the 3-D fluid motion. Since measurements are difficult and restricted, there is interest in improving and verifying the capability for the direct calculation. De Boer (2006) provides a recent perspective on the issues.

b) Two-dimensional (2-D) approximation

To place the cochlear model on a physical basis, more details of the fluid motion must be considered (Ranke 1950; Berkley and Lesser 1973; Neely 1981). When the wavelength is short for large m, the 1-D approximation is not valid because the pressure on the BM is much larger than the average pressure, as indicated in the measurements (Figure 8). The 2-D approximation (from Laplaces equation in the xz plane) is:
! 1 pBM mH = !" p Tanh ( mH ) # mH for for mH < 1 long wavelength mH > 1 short wavelength
(Eq. 21)

in which H is the height of SV. With this, Eq. 19 is the same, but the wave number is:
2 !" 2 mH m = AK Vol ( x ) Tanh ( mH )
2

(Eq. 22)

For the square SV, A = H2, and this can be rewritten as:

31

2 !" 2 , mHTanh ( mH ) = K Vol ( x )

(Eq. 23)

which has the approximation:

)# 2 ! " 2 & 1/2 F +% ' +$ K Vol ( x ) ( mH ! * 2 + 2 ! F" + K ( x) Vol , for for mH < 1 long wavelength
(Eq. 24)

mH > 1 short wavelength

Thus in the long wavelength region, the wave number is proportional to the frequency, which is the characteristic of non-dispersive waves. For the short wavelength region, the wave number is quadratic with the frequency, which indicates dispersion. At the point of partition resonance defined by Eq. 16, this has the value:

mH !

8 !

(partition "resonance")

(Eq. 25)

A dimensionless form of Eq. 23 is:

! = m
in which
! = mH , m

!2 8 " ! ! Tanhm
$ 8 K vol ' =& % " 2#F ) (
1/2

(Eq. 26)

! = ! / ! ref , ! ref !

! = xH . x

The behavior indicated in the sketch of the slow wave in Figure 7 comes from Eq. 23. Near the stapes, where x is small, the stiffness is large, so the wave number is small, i.e., the wavelength is long. As x increases, the wave number increases. The short wavelength region begins when mH = 1, after which the wave number increases more rapidly. A little past the beginning of the short wavelength region mH reaches the value shown in Eq. 25. So when the fluidelastic behavior is considered, Eq. 16 is seen to be a transition point at which the wavelength really becomes short, rather than any local resonance similar to the strings of a harp. When the wavelength becomes rather short, the damping due to the fluid viscosity increases exponentially. It is therefore only a rough approximation to the actual BF. When the fluid viscosity increases, the BF shifts to the base, and when the cross-sectional area A of the scalae decreases, the BF shifts to the apex, with a less rapid decay of the amplitude (Lim 2000).

c) Three-dimensional (3-D) model and viscosity

The extension to the 3-D analysis of the fluid, including the effect of viscosity, is straightforward but tedious. The pressure at the basilar membrane of the 3-D fluid is included by making pBM in Eq. 21 a function of not just scalae height H, but also the scalae width W. Since the first development (Steele and Taber 1979), several authors have used various approaches. Advances include the proof that Eq. 19 is valid for 3-D 32

without any assumption on the form of the solution; only the dispersion relation of Eq. 23 is modified (Baker 2000; Lim 2000; Lim and Steele 2002). The viscosity of the fluid adds imaginary components to Eq. 23, so the wave number m becomes complex. Incorporation of the 3-D fluid becomes critical for capturing both the magnitude and phase behaviour of basilar membrane response with physical parameters (Kolston 2000).

d) Validation with physical modeling

A comparison of the 1-D, 2-D and 3-D calculations is shown in Figure 11. For this calculation only the physical properties of fluid and partition measured by Helle are used. The gain in accuracy with 3-D is well worth the slight extra effort of calculating the wave number m from the 3-D generalization of Eq. 23. For the 1-D model to have the correct BF, either the stiffness or mass must be modified from the physical value by a substantial amount.
Figure 11: Amplitude of BM for frequency 848 Hz in an experimental model (Helle 1974). This is a box model of the cochlea, six times human size, with an isotropic polymeric BM. The measured points are shown by ! . The computations from 1-D, 2-D, and 3-D approximations show that the 3-D captures the behavior best (Steele and Taber 1979). Helle measured all properties, so there are no free parameters.

In recent times, several laboratories have used micromachining to obtain life-sized box models of the cochlea. Traveling waves are found in models with fluid of the viscosity of saline for (1) fluid on one side and the partition stiffness dominated by tension (White and Grosh 2005) and (2) fluid on both sides and the stiffness dominated by bending with 9000 ribs to simulate the orthotropic construction in the real cochlea (Wittbrodt et al. 2006). In the latter work, each of four different membrane thicknesses yields reasonable agreement between the calculation from the physical properties and the frequency localization from the 3-D WKB calculation discussed in the next section. So finally there is solid evidence that the 3-D fluid motion in the cochlea is captured properly by the transmission line Eq. 19 with the 3-D determination of wave number.

4. Solution methods
With the advances in computing power, a direct finite difference computation for the full 3-D cochlea is appealing. The problem is in the dimensions. With the typical cochlear length 30 times the width, and the BM only 1/10 of the width, and the fluid viscous boundary layer 1/10 of the width of the BM, a fixed mesh requires millions of degrees of freedom. Therefore, even full use of parallel processing (Givelberg and Bunn 2003) requires many hours of computing time for limited results for a linear model, that did have the advantage of being coiled and with viscosity of the fluid. Kiefer, et al. (2006) offer the model closest to the actual geometry of the human cochlea with the full 3-D

33

coiling. However, they use inviscid fluid, which greatly reduces the computing challenge. In comparison, the 1-D model Eq. 19 can be solved by a variety of numerical methods. Most efficient is an asymptotic method often referred to as WKB. For this, the solution of Eq. 19 is written as:
j ! t " # x ,! Ap ! P ( x, ! ) e ( ( ))

(Eq. 27)

in which P ( x, ! ) is the amplitude function, and the exponential term provides the traveling wave with the phase given by

! ( x, " ) =

# m ( x," ) dx
x 0

(Eq. 28)

The viscosity of the fluid contributes a negative imaginary part of the wave number m, which causes the exponential decrease in amplitude of the traveling wave in the short wavelength region. This approach was first used by Ranke (1950) on a 2-D model for the cochlea. The viscous boundary layer of fluid adds an additional term to Eq. 26: !2 8 " ! = m (Eq. 29) #1/2 ! Tanhm ! /m ! # 1 + j"$ !2

in which the viscosity parameter is:

! = " ref H 2 #F / . The viscosity of the fluid is . Generally, the term ! is large, so the expansion for the wave number is:
! ! m ) !2 & ! 3/2 8" 8" 1 + 1 $ j ( ) ( 1/2 + ...+ # ' # ( 2% ) *
(Eq. 30)

which shows that the fluid viscosity adds to the effective mass with the positive real part of the correction term, and provides the damping with the negative imaginary part. The ! < 1 but becomes significant for ! ! > 1 , causing the rapid high damping is small for ! frequency decay in amplitude. A comparison of the 3-D calculation and measurements in the chinchilla is in Figure 12. The BM displacement is divided by the stapes displacement, so a linear system would have the response independent of input amplitude. This is not the case for frequencies near the maximum. However, for amplitudes greater than 80 dB SPL, the responses converge, indicating a linear passive behavior, described well by Eq. 19 with the 3-D extension of Eq. 22. Particularly note the phase in Figure 12(b), which corresponds to Eq. 24, linear in frequency for low frequency and quadratic in frequency for frequency approaching BF and higher. This clearly shows the transition of wavelength from long to short near BF. The phase has some dependence on amplitude near BF, but is remarkably insensitive considering the huge change in the amplitude of the input sound.

34

Figure 12(a): Amplitude of BM displacement measured in chinchilla (Ruggero et al. 1997) and computed with 3-D model with saturating feed forward (Lim and Steele 2002). The amplitude is normalized to the stapes displacement. Experimental points are shown for 20 and 80 dB SPL. The active process increases the relative amplitude for low input sound levels. Figure 12(b): Phase relative to the stapes velocity of BM displacement measured (Ruggero et al. 1997) and computed (Lim and Steele 2002), corrected by Y.J. Yoon. The phase is generally insensitive to amplitude. For low frequency, the phase is nearly linear with frequency (long wavelength 1-D). Approaching BF (10 kHz), the phase becomes quadratic, reflecting the dispersive 3-D behavior.

A third region that appears in the BM measurements but not in the neural response is the plateau in amplitude and phase just beginning at 13 kHz in Figure 12a. This is yet to receive an explanation, but some consider this as evidence for the existence of additional waves. There may well be more than just the fast and a slow wave shown in Figure 7. The form of Eq. 27 is also convenient for transients, since the energy for the wave of a given frequency arrives from the stapes at the point x in the time given by:
t arr ( x, ! ) = " " # ( x, ! ) = "! "!

$ m ( x,! ) dx
x 0

(Eq. 31)

This approximation can be used to estimate the neural delay (Anderson et al. 1971). Thus from Figure 12(b) the low frequencies have a constant low slope of phase, indicating a fast arrival independent of frequency. For higher frequencies, the slope increases in magnitude, indicating an increasingly longer time of arrival at this point and a dispersion of the signal. Note that the slopes depend on the location along the cochlea. We note that the passive cochlea is a causal and stable system. Eq. 31 is the group delay of the transfer function relating the response at a point to the input at the stapes. An important attribute of the auditory system is high frequency resolution of auditory neurons (Kiang et al. 1965). The source of the high resolution, measured as bandwidth of the response from the peak, is in the basilar membrane response (Narayan et al. 1998). The sharp frequency resolution helps reject noise outside the bandwidth of interest for a specific neuron. Thus the sharp resolution is important for increasing the signal-to-noise 35

ratio, particularly at low levels. It is well accepted that the bandwidth of the basilar membrane increases as the level increases (Rhode 1971, see Figure 12) and this is now believed to be due to non-linearity in the organ of Corti mechanics. Many consider this due to the active process that is significant at low levels. For high levels the BM response is linear and described well by the mechanics of the passive box model.

F. Organ of Corti Fluid pressure to neural excitation

The inner ear provides the neural excitation for acousto-mechanical stimuli. Key to this are receptor cells (hair cells), which transduce mechanical force on cilia (hairs) on one end of the cell into increased firing of neurons via synapses near the other end. (See chapter 2.) The hearing organs provides the sensation for the higher frequencies needed for sound localization and speech reception. Man has an upper frequency of 20 kHz, while some bats and toothed whales extend to over 150 kHz. As discussed in the previous section, the box model of the cochlea, consisting only of fluid and BM, results in the localizing of the BM displacement and fluid pressure to a certain region for a certain frequency. In the cochlea, the organ of Corti (OC) is attached to the BM and contains the receptor cells. This is the additional system needed to transfer the BM displacement to force delivered to the cilia. In addition, the OC provides an active input of energy into the traveling wave for low sound levels, which greatly increases the sensitivity and frequency resolution of the basilar membrane displacement and neural excitation. In non-mammalian vertebrates, receptor cells achieve much of their frequency selectivity through the operation of electrical resonance. The ion channels in the basolateral membrane of each cell constitute a miniature electrical circuit that tunes the cell to a specific frequency of mechanical input. However, the mammalian OHC has the unique property of high frequency electromotility, defined as a change in the cell length in response to a change in the electric potential difference across the cell membrane (Brownell et al. 1985). The potential difference across the cell membrane is the result of intracellular voltage depolarization due to ion flow in the stereocilia. Ion channels in the stereocilia are mechanically opened when there is displacement of the bundle in the excitatory direction. The mechanical opening of the ion channels in the inner ear is significantly faster than the cascade of chemical signals required for example in the retina. Therefore, while the sensory receptor hair cells are all mechano-receptive in the three types of organs in the inner ear, the means for accomplishing their excitation for hearing are much more elaborate. Consequently, the cochlea remains more mysterious than the vestibular system on many levels. As a small example, the most striking geometric feature of coiling of the mammalian cochlea has yet to be adequately explained. Packaging is certainly a consideration. However, West (1985) finds correlation between hearing and coiling in land animals, while Cai et al. (2005) compute the low frequency mechanical effects of coiling and in current work find remarkable correlation of coiling and hearing in sea mammals.

1. Multi-scale organ of Corti model

The modeling of the OC with the inclusion of more complete anatomical details has received increasing attention in recent years. Kolston (1999) developed the first detailed model, in which the components of the OC are simplified to a rectangular grid and the fluid viscosity neglected. He obtained the traveling waves in a significant length of the 36

cochlea. The calculation is by the finite element method (FEM), which is now the prevalent method for structures and for fluid-structure interaction. Cai et al. (2004) and Andoh and Wada (2004) use this to consider more realistic geometry for the cross section, but use an approximation for the effect of the longitudinal motion, which is significant for higher frequencies. Another approach is to calculate the stiffness properties of the components of the OC first, and then incorporate the fluid motion in the various compartments of the OC. The components are shown in Figure 13 (Steele and Puria 2005). It is safe to say that the complete solution for the transformation of the basilar membrane motion to hair cell excitation for entire cochlea with a reasonable representation for the OC for all frequencies of excitation is yet to be attained. In the sections that follow, an approach to understanding the complex transduction that takes place in the organ of Corti is presented. The model is based on known anatomy and known material properties with assumptions about the method of feed-forward of outer hair cell force for active amplification. In another chapter of this handbook, Neely and Kim summarize other methods for active amplification that have been proposed.
Figure 13. Shell model for guinea pig apex (yz plane). The dashed lines show the undeformed configuration, while the solid lines show the deformed configuration due to static pressure loading toward ST, greatly amplified. The radial and axial distances are in mm. The labels are: SV scala vestibule, ST scala tympani, IS inner sulcus, C Cortilymph, TM tectorial membrane, IP inner pillar, OP outer pillar, BM basilar membrane, IHC inner hair cells, OHC outer hair cells, HS Hensens stripe, and L1 sub-tectorial membrane fluid region.

2. Outer hair cell motility: push-pull of BM

Many features of the geometry of the OC have been made clear from detailed measurements in the guinea pig and by a large physical model (Voldrich and Ulehlova 1987). The inclination of the OHC in the radial cross section is evident in Figures 13 and 14. The inclination in the longitudinal direction is shown in Figure 14. The synaptic end of the OHC is supported by Deiters cell. Each cell has an intracellular axial column consisting of microtubules, referred to as Deiters rod in Figure 14. One end of the rod cups the end of the OHC and the other end is attached to the BM. The Deiters rod provides the dominant axial stiffness of the cell. In birds and other non-mammals there is no motility and no stiff connection between the receptor cells and the BM. The cup of 37

Deiters rod at the synaptic end of the OHC also has an attachment to the reticular lamina (RL) with a phalangeal process, shown in Figure 14. The process also consists of microtubules. Thus the triangular arrangement of OHC, RL and Deiters process provides a frame of significant elastic stiffness. The OHC is motile (Chapter 10), so a shear of the cilia in the direction to cause hyper-polarization of the cell causes an expansion of the cell, which causes a push down on the BM through the rod. The interesting feature is that the shear on the cilia at the distance from the stapes given by x causes a push on the BM at the distance x + !x . Generally an active system with sensors and actuators that deliver energy to the system, which affects the input-output relation, is called feedback. For a system consisting of an input and output connected by a chain of processes, a sensor at one point that causes actuation at a preceding point in the chain, is called feed-backward, while a sensor that causes actuation at a subsequent point in the chain is called feed-forward. The structure of the OC, shown in Figure 14 is elastic with the multiple attachments, so the elongation of a single OHC causes a ripple effect of loading of the BM in both directions. DeBoer and Nuttall (2003) use a novel approach and take this into account with an array of impedances at different distances. The amplitudes of these feed-forward and feed-backward elements are computed for a best fit with the experimental measurements of BM response, using the 3-D calculation for the fluid. Here we offer a direct physical interpretation of a simpler version. Another feature is that the fibers of the BM are in a sandwich in the pectinate zone (PZ), then flatten to one layer in the arcuate zone (AZ) between the outer pillar (OP) and the inner pillar (IP). Since the bending stiffness D of a plate depends on the cube of the thickness, the BM AZ has roughly 1/27 of the stiffness of the PZ. Thus the OP offers significant support of the BM. Consequently, a simple model is the following sequence: A downward pressure on the PZ, consisting of a positive fluid pressure in SV pF and an effective pressure from the Deiters rods pR causes a shear force on the OP

foot of magnitude ( 2 pF + pR ) b / 2 at the distance x from the stapes. The shear on the OP foot is roughly equal to the shear on the OHC cilia, if the details of the OC fluid-elastic motion are ignored. The shear is in the inhibitory direction and causes expansion of the OHC. The tendency of the OHC to expand causes a compressive force in Deiters rods, which is a downward force on the BM represented by the effective pressure pR .

However, this occurs at the distance x + !x . An equal and opposite force acts upward on the RL. Since this is more compliant, the displacement is more than for the BM, as shown in measurements in the cochlea and by calculations with the model in Figure 13. This upward displacement of the RL causes a tension in the phalangeal process, and an upward pull of the Deiters rod. The equation for this is:

pR ( x + !x, t ) = " # $ 2 pF ( x, t ) + pR ( x, t ) % & ' "2 # $ 2 pF ( x + !x2 , t ) + pR ( x + !x2 , t ) % &

(Eq. 32)

Thus the rod at the point x + %x is compressed by the OHC whose apex is at the point x 38

by an amount proportional to the total pressure on the membrane, fluid plus rod, at x. So this is a positive feed-forward with the amplitude #. The rod is also pulled by the phalangeal process by an amount proportional to the total pressure on the membrane at point x + %x2. So this is a negative feed-backward.
Figure 14: Side view of OHC showing the inclination (xz plane). The end is supported by the cup of Deiters cell, which has a rod providing mechanical attachment to the BM and a phalangeal process providing attachment to the RL. Inward shear of the stereocilia at the point x causes hyperpolarization of the OHC, which causes an elongation of the OHC, resulting in upward displacement of the RL and downward displacement of the BM. Because of the OHC inclination, this is a downward push on the Deiters rod at the point x +% x , feed-forward. Because of the inclination of the phalangeal process, this rod will be pulled upward by an elongation of the OHC at the point x +% x2 which is a negative feed-backward. The horizontal projection of OHC plus process is % x2 .

If the solution is used in the form Eq. 27 with the assumption that %x2 and %x are small, then Eq. 32 becomes:
pR e! jm "x = # [ 2 pF + pR ] ! # 2 [ 2 pF + pR ] e! jm "x2
(Eq. 33)

with which the rod pressure pR can be written in terms of the fluid pressure, so the total pressure becomes:

2 pF + pR =

1 ! "e

jm #x

+ " 2 e! jm ( #x2 ! #x )

2 pF

(Eq. 34)

Adding this feed-forward and feed-backward to the previous Eq. 29 for the dimensionless wave number yields:
! = m 8 ! % tanh m ! /m ! # 1 + j"$ !2 &

!2 " #1/2 ! ! ! ! *x ! %1 # ) e jm + ) 2 e# jm ( *x2 # *x ) ' ) ' ( (&

(Eq. 35)

Expanding this for small values as for Eq. 30 gives the real and imaginary parts:

39

!)! Re( m

* 8 2' 1 8 2 ! )1 + ! + % & %2 , # # ! " " 2#$ ) , ( +

(Eq. 36)

2 1 % 8 ! 2( . 1 ! ) ! "' $ * 0 ! " , 2 ( -x ! 2 " -x ! )3 Im( m " ,-x &# ) 0 ! 3 / 2$+ 2

(Eq. 37)

Thus the feed-forward and negative feed-backward tend to cancel in the real part. However, the positive feed-forward and the negative feed-backward add to decrease the damping due to the fluid viscosity. In calculations it is far better to use the complete relation Eq. 35 and solve for the wave number iteratively. Results from this are shown in ! , the spatial integral of which gives the phase, is not Figure 15. The real part of m ! has sensitive to the values for the parameters. However, the imaginary part of m dramatically different behavior. For the passive case, with both feed-forward and feedbackward set to zero, the fluid viscosity provides the only damping. This is rather ! < 1 ) but increases rapidly for higher negligible for frequencies less than BF, ( ! frequencies, and gives the rapid high frequency decay in Figure 12a. When feed-forward is turned on with # = 0.08, Eq. 37 shows that the damping is decreased, but the full ! actually is positive for a range solution in Figure 15 shows that the imaginary part of m of frequencies above BF. This can be interpreted as a negative damping due to the input of energy from the OHC motility. When the negative feed-backward is added, the ! is decreased and sharpened. positive range of the imaginary part of m With the approximation Eq. 32, the details of the OC can be neglected and the transmission line model Eq. 19 used. The effect is just a modification in the BM volume stiffness:
K Vol ( x ) !" " K Vol ( x ) 1 # $ ( x )e jm ( x ,% ) &x + $ 2 ( x )e# jm ( x ,% )( &x2 # &x )

(Eq. 38)

Near CF, the change in impedance is due to an apical shift in resonance for the lowlevel active case, but the phase change is small (Yoon et al. 2006). This indicates that the zero crossings of the time domain response for the high level passive case and the low level active case will be nearly invariant. This suggests that force generation by OHCs in the feed-forward formalism satisfies the near-invariance of fine time structure of the organ of Corti response predicted by Shera (2001). The modification of BM stiffness is also valid in 1-D approximation (Eq. 20) and the 2-D formulation (Eq. 23) with the caveat that the stiffness may not be physical as discussed above. Thus the feed-forward causes a decrease in the effective partition stiffness and a negative damping. This is significant in the short wavelength region and corresponds to a significant input of energy into the traveling wave. For very short wavelength, however, the fluid viscosity dominates. The results for the 1-D model for #2 = 0 (Geisler and Sang 1995) are excellent. The motility of the OHC saturates, which is represented by multiplying the factor # with a saturating function dependent on amplitude. The result for the dependence of the BM amplitude on input sound amplitude for the 3-D model of the chinchilla cochlea is in Figure 12. The simulation results compare very well with other experimental

40

measurements, capturing several nonlinear features observed in basilar membrane responses. These include compression of response with stimulus level, two-tone suppressions, and generation of harmonic distortion and distortion products (Lim and Steele 2002). Transient click response has also been considered (Lim and Steele 2003). The simulation results exhibit some of the characteristic nonlinear behavior of the basilar membrane commonly observed in experimental measurements, such as significant amplification and sustained "ringing" in the transient response at low stimulus level. The simple feed-forward mechanism is able to capture the properties of the active process in the cochlea without a second filter or resonance. All parameters are biologically based, with the feed-forward needing only the inclination of the cells, assumed to be 30, and the maximum value of # taken as 0.35 for the 3-D calculation, which is modest.

a)

b)

! from Eq. 35. The curves FF + FB are for the ! as a function of frequency ! Figure 15: Wave number m feed-forward due to the OHC inclination and the negative feed-backward due to the reverse

! = 0.02 , !x ! 2 = 0.07 ! = 0.08 , ! = 10 5 , !x ! 2 = 0.02 . The curves FF are with the effect of the feed-backward set to zero, ! 2 = 0 . The curves passive are for both active effects turned off, ! 2 = 0 and ! = 0 . Finally the curves reverse FF are ! = "0.02 and ! 2 = 0 . (a) The real part for the traveling wave moving toward the stapes with !x ! > 1 and little sensitivity to feed-forward or feed-backward. (b) The shows rapid accumulation for !
inclination of the phalangeal processes, with parameters imaginary part provides the effective damping of the wave, which is highly sensitive. The feedforward push of the OHC causes a region of positive values, i.e., negative damping. The addition of the feed-backward pull of the phalangeal processes increases and sharpens the negative damping. For a wave in the reverse direction, the damping is increased by both effects. So the forward and backward waves are not the same.

The advantage of the distributed feed-forward system should be appreciated. All the sensors and actuators are turned on, without the need for a Maxwells demon to turn on the amplification where it is needed (Shera and Guinan 1999). For the long wavelength region, it has the effect of a small shift in the stiffness of the partition, but near BF, the negative damping is turned on with amplification of the signal of 40 dB or more. Then past BF there is little effect, and the high frequency fall off is the same as for the passive (Figure 12a). The assumption is that the OHC motility functions cycle by cycle without 41

restriction on frequency, i.e., # is independent of frequency. Whether the OHC actually performs this is a subject of current investigation in several laboratories.

3. Time delay vs. feed-forward

Similar to deBoer and Nuttall (2003) we ask for the time delay that would have the same effect as the spatial feed-forward and feed-backward. With a time delay %t in the pressure delivered to the BM from the OHC, Eq. 32 is replaced by:
pR ( x, t + !t ) = " # $ 2 pF ( x, t ) + pR ( x, t ) % &
(Eq. 39)

The wave number-frequency relation Eq. 35 is then:

! = m !2 8 " ! % Tanhm ! /m ! # 1 + j"$ !2 &

#1/2

! ! *t ' %1 # ) e# j" ' ( (&

(Eq. 40)

! = " ref !t . Expanding the wave number for in which the dimensionless time delay is !t ! > 1 as for Eq. 35 gives the real and imaginary parts: small " and !
!)! Re( m * 8 2' 1 8 2 !, , ! )1 + ! + % cos # ! &t # # ! " " 2#$ ) , ( +
. (Eq. 41)

+ 8 2( 1 8 2 !! * ! + & sin $ ! 't !)!" $ Im( m $ ! # # * ) 2$% ,

(Eq. 42)

Since " is positive, a small time delay increases the damping. The time delay must be ! > " for a decrease in the damping that corresponds to an energy input tuned with !t ! < 0 , to obtain negative ! " 1 . Another possibility is to make !t to the wave around BF ! damping for small time delay without tuning. However, this is a noncausal event, since what occurs at future time is having an effect at present time, as pointed out by DeBoer and Nuttall (2003) with a different approach. The stability can be examined by considering, not a cochlea, but a simpler system consisting of a tube with constant properties over a finite length with zero condition at the ! . The solution Eq. 27, with forward and backward waves provides the transfer !=L end x ! to the input pressure at x ! = 0: function relating pressure at the general point x
!x ! ! ) e! jm p(x ! e B( ) = ! ! jm ! ! BL !L p (0) 1 ! e! jm ! jm ! ! jm ! !!L !L x

(Eq. 43)

where mB is the wave-number for the backward traveling wave, defined by Eq. 35 with the signs of %x and %x2 changed. The poles are the zeros of the denominator at:
! ! +m ! B = 2 k! / L m
(Eq. 44)

in which k is an integer. For each k, this equation may be solved for the complex frequency. If the imaginary part of the frequency is negative, the solution is unstable in time. Remarkably, the feed-forward and feed-backward terms tend to cancel in the imaginary part, as can be seen by substituting the expansions Eqs. 36 and 37 into Eq. 44. 42

Direct numerical calculations for the solution of Eq. 44 support this, so it appears that the spatial delay expressed by the feed-forward and feed-backward provides a stable system. Even when the imaginary part of the wave number is positive, as shown in Figure 15, the system remains stable. There is a limit to this, since for the gains ! " ! 2 # 1 , the stiffness becomes zero for small frequency. A precise determination of the stability boundaries has not been carried out, but the gains used in Figure 15 can be increased by a factor of 3.9 until instability occurs. The zeros of the transfer function are the zeros of the numerator at:

!"x ! +m ! B = 2 k! / L ! m

(Eq. 45)

which also have positive imaginary parts. So within certain limits, the feed-forward system with a substantial gain in amplitude is stable and causal. This can be extended to the cochlea with variable properties. The condition Eq. 44 becomes

! ( m + m )dx = 2 k"
B 0

(Eq. 46)

which is more difficult to compute, but clearly with the same features. In contrast, the forward and backward wave numbers are the same for the time delay system. Consequently, the solutions of Eq. 39 show instability in time when the imaginary part Eq. 42 is positive. Generally, feedback models incorporating time delay require additional components to prevent undesirable behavior. The measurements of Frank, et al. (1999) show no time delay between the motile force and transmembrane potential. Therefore it appears most plausible that the frame structure in Figure 14 is for the purpose of the feed-forward and negative feed-backward of energy into the traveling wave. Information on the exact inclination of the OHC and phalangeal process is lacking, but micrographs usually show a configuration similar to Figure 14. The one careful examination of this is from Karavitaki (2002), who finds in gerbil that the RL is nearly perpendicular to the OHC. Thus !x is nearly zero. However, the !x2 is apparently equal to several OHC diameters, so the push-pull system works well.

4. Inner hair cell excitation

In the preceding discussion an approximate relation Eq. 40 is extracted from the physics of the OC, leaving only a modification of the BM model. Subsequently the details of the OC are avoided. However, the purpose of the OC is to provide the proper excitation of the inner hair cells (IHC). The IHC cilia are not attached to the overlying tectorial membrane and are subject to the mechanical force of the fluid motion, which is dependent on the response of the entire structure of the OC. Consequently, the modeling of the OC is the subject of numerous recent studies. Bhnke and Arnold (1998) provide the most detailed FEM model, but without fluid. Kolston (1999) has inviscid fluid but with geometric simplification of the OC structure. Hubbard, et al. (2003), Grosh et al. (2004), and Mountain and Hubbard (2006) use other geometric simplifications. Cai and Chadwick (2002), Andoh and Wada (2004), and Steele and Puria (2005) use detailed FEM models with realistic geometry and stiffness properties for the components. As discussed by these authors, there is growing awareness that the flow of the fluid in the regions of the OC is important. Billone and Raynor (1973) provide perhaps the first 43

careful analysis of the flow around the IHC cilia. One must keep in mind that in the hearing organ in lizards, there is considerable variety but always a group of receptor cells without a TM and with tall cilia free in the fluid. Freeman and Weiss (1990) have extensively investigated the mechanical behavior of these cilia through the relevant frequency range (1 3 kHz). It is of interest that the neural tuning and otoacoustic emissions from these receptor cells are similar to mammalian for the same frequency (Manley 2006), without the TM, OHC motility, Deiters cells, etc, that seem to be so important for mammals. For mammals a feature recently established by Edge et al. (1998) is the proximity of the Hensen stripe, a protrusion of the tectorial membrane, to the tip of the IHC cilia, as indicated in Figure 15. Nowotny and Gummer (2006) provide a breakthrough with measurements of the lower surface of the TM and the upper surface of the RL during electrical stimulation. They find that these surfaces do not remain parallel, as usually assumed. The calculation for the full elastic structure shows this as well. As can be seen in Figure 13, the region L1, near the IHC cilia between the TM and RL opens with displacement of the BM toward ST. This tends to pull fluid in from the IS past the IHC cilia. Just how much depends on the relative stiffness of the TM and the proximity of the HS. Putting this together gives the effects on the phase of IHC excitation given in Table 5. The phase measured in neurons from the IHC in the middle and upper turns typically show for low frequency something close to Case 2, with a change toward Case 1 as frequency increases (Cheatham and Dallos 1999). In the base with a relatively stiffer TM, Ruggero et al. (2000) report values similar to Cases 3 and 4. Table 5 Effects on phase of IHC tip link tension for BM motion toward ST, for which the pillar head and base of cilium move radially outward. Cases 1 and 2 prevail for soft TM, while Cases 3 and 4 prevail for stiff TM.
Case Cause Mechanism Effect on IHC neurons Phase

1 2

Small gap with HS (or high frequency), cilium nearly sticks to HS Large gap with HS and TM (or lower frequency), cilium is pulled through fluid Small gap with HS, area of region L1 increases, cilium nearly sticks to HS, so L1 has negative pressure Large gap with HS, area of region L1 increases, so fluid flows from IS into L1

Tip lags the base, causing decrease in tip link tension in phase with BM displacement Tip lags the base, causing decrease in tip link tension in phase with BM velocity Outward pressure on cilium, causing increase in tip link tension in phase with BM displacement Outward pressure on cilium, causing increase in tip link tension in phase with BM velocity

Inhibition Inhibition

0 90

Excitation

180

Excitation

270

44

Figure 16. Close view of IHC cilia for guinea pig apex. The Hensen stripe (HS) is the triangle attached to the tectorial membrane above. The dashed lines show the undeformed configuration, with the tip of the IHC cilia near the HS. The solid lines show the deformed configuration due to static pressure loading toward ST, greatly amplified. The radial and axial distances are in mm.

A strong mechanical nonlinearity comes from the restricted flow between the cilia, tectorial membrane and Hensen stripe (Steele and Puria 2005). A result for this is in Figure 17, which shows the tension in the tip link compared to the driving pressure, positive in ST. Two peaks of the tension occur in each cycle of the pressure for a pressure level corresponding to around 90 dB SPL. For lower sound pressure, the peak out of phase with the pressure dominates, and for higher sound pressure only the peak in phase with the pressure remains. This is remarkably close to the behavior of auditory neurons sometimes observed (Kiang 1990). A common expectation is that velocity of the BM toward ST will cause the IHC cilia to be swept by the fluid in the inhibitory direction (to the left in Figure 13). However, it seems that almost any phase of excitation is possible, depending on the specific geometry and relative stiffness properties. In the static response shown in Figure 13, the subtectorial fluid region L1 is seen to open with BM displacement toward ST. This will cause a fluid flow into L1 from the inner sulcus (IS) that will bend the cilia in the excitatory direction. BM motion toward SV then is inhibitory. However, as the amplitude increases, the tall cilia are constrained by the Hensen stripe while the RL still moves to the left in Figure 13. This causes tension in the tip links seen as the in-phase peak in Figure 17.
Figure 17: Nonlinear solution for the force in the tip link at the guinea pig base at 100 Hz. Around 90 dB SPL, two peaks of force (nonlinear curve) occur per cycle of ST pressure (cosine curve). This offers a possible explanation for the 180 change in phase and peak splitting sometimes observed in auditory nerve fibers (Kiang 1990).

45

G. Summary of some issues

Rapid development in measurement and computational technique related to auditory biomechanics is ongoing. Perhaps the following issues soon will be completely resolved.

1. Motion of tympanic membrane for high frequency

The simple model for middle ear has the tympanic membrane acting as a rigid, massless piston. However, instead of piston behavior, surface displacement measurements revealed multiple modes of vibration for frequencies above a few kHz (Tonndorf and Khanna 1972). This has provoked considerable discussion. A recent explanation offered in a preceding section is that the nonsymmetic material and geometric properties of the membrane provide mistuning without strong resonances. The consequence is a fairly uniform transmission of the pressure for the entire frequency range without the need for woofer or tweeter. Full validation for this notion is in progress.

2. Motion of ossicular chain for high frequency

The nonmammalian vertebrates have a simple columella that transmits the tympanic membrane motion to the inner ear. In contrast the mammals have the three-bone ossicular chain. In the simple model, this is represented by a simple lever with fixed pivot point. However, measurements show that this is not the behavior for frequencies above a few kHz (Decraemer, et al. 2003). The pivot point depends on frequency and the stapes wobbles, instead of directly providing a volume displacement of the cochlear fluid. The expectation is that this somehow permits the extension of the frequency range, but an explanation is totally lacking.

3. Bone conduction
Hearing by bone conduction is of high clinical significance. There are many measurements showing that the volume displacements of oval and round window are exactly out of phase for air conducted acoustic excitation, consistent with the two modes shown in Figure 7. All existing theory indicates that this is also the case for boneconducted sound. However, measurements by Stenfeld et al. (2004) indicate that this is not the case for bone conduction. Indeed for some frequencies, the two windows are in phase. Thus there must be compliance in the cochlea not yet explained (often referred to as a third window). Dehiscence of the semi-circular canals has been clinically shown to produce a third window (Chien et al. 2007; Merchant et al. 2007; Minor et al. 2003). Sohmer and Freeman (2004) demonstrate that bone vibration generates acoustic pressure in the brain that can generate auditory response. Estimates on the flow properties of the cochlear and vestibular aqueducts indicate that the compliance is too low to offer a reasonable acoustic pathway. Again an explanation is totally lacking.

4. Traveling wave
The traveling wave observed in the GP cochlea by Bksy (1960) was not anticipated by any theoretical consideration. There remain contrary opinions, e.g., Sohmer and Freeman (2004) consider their measurements as evidence against the existence of the traveling wave. The traveling wave does not occur in lizards and turtles, but most likely 46

occurs in bird. For mammals, the evidence for the existence of the traveling wave seems overwhelming. We mention the direct in vivo observation of waves by Ren (2002), the close relation of BM displacement and neural excitation found in the same animal by Narayan et al. (1998), and the agreement in theory with the traveling wave and experiment for the BM motion (Figure 12). This disagreement should be at an end.

5. Motility vs. beating

In non-mammalian hearing organs, there are no arches of Corti, Deiters cells, nor inner sulcus as shown in Figure 13. Furthermore the cells similar to the OHCs cannot have somatic motility. Nevertheless, in the responsive frequency range, the neural tuning is as sharp as in mammals, and evoked and spontaneous emissions occur very similar to those in mammals (Manley 2006). Crawford and Fettiplace (1985) discovered that the cilia on turtle hair cells have spontaneous activity, i.e., they beat without external excitation. This mechanotransducer (MET) channel phenomenon is described as a Hopf bifurcation (Choe, et al. 1998). In all vertebrates, the cilia and transduction channels are similar. Is the energy of the active process generated by MET instability or somatic motility of the cell, or is it a combination? This is a subject of current investigation (e.g., Chan and Hudspeth 2005). Frank et al. (1999), discovered that the ratio of OHC motile force to transmembrane voltage remains constant to nearly 100 kHz without time delay, which supports the notion that motility is a unique feature of the OHC and must be important for mammalian hearing. Indeed the recent results on rat cochleas by Kennedy et al. (2006) offer evidence that both MET resonance and somatic motility are interacting.

6. OHC roll off

The feed-forward (and negative feed-backward) discussed here depends on the force of motility of the OHC to be independent of frequency. However, the electrical properties of the OHC appear to be such that for a fixed amplitude of shear force on the cilia, there is a significant decrease in the intracellular potential at a frequency much less than the BF. Several laboratories propose more detailed analysis of intracellular or extracellular behavior that would maintain the effect of the motility for high frequency. Without a more elaborate cell model, Baker (2000) and Grosh et al. (2004) use models with correct physical values for the electrical and mechanical properties of the OHC, but with resonant TM, and find that the effect of the motility for high frequency is preserved.

7. TM properties- resonant TM?

Many authors have used OC models with a strong resonance of the TM (e.g., Allen 1980). Several laboratories have measured the properties of the TM, most recently Gueta et al. (2006) and Masaki et al. (2006). Details are different, but the general conclusion is that the TM is rather soft tissue, with an elastic Youngs modulus in the range 0.5 30 kPa. Zwicker (1972) points out that squirrel monkey and pig have a great difference in TM size. Such a difference for animals that have roughly the same frequency range makes a resonant TM seem unlikely. Nowotny and Gummer (2006) measure the TM response due to electrical stimulation and find no resonance for frequencies through BF. So there

47

are indications that the TM does not have a strong resonance.

8. Multiple traveling wave modes

The common box model has the fast and slow waves indicted in Figure 7. However, each of the fluid spaces in the OC (Figure 13) can support an independent wave. Karavitaki (2002) offers measurements of motion of the OC that support the notion of multiple waves. As discussed by deBoer (2006) recent models, e.g., Zhang et al. (1997) and Mountain and Hubbard (2006), have such capability. The goal remains for a model of the OC with physically realistic geometric and stiffness properties and with 3-D viscous fluid, that can simulate the environment of the cilia for all frequencies. The expectation is that waves in the IS and tunnel space do play a significant role.

9. Stiffness change along the cochlea

Almost every component of the cochlear cross section has at one time or another been proposed as the fundamental resonance element. Most probably agree with Bksy (1960) that the BM has the strongest stiffness gradient and is the most likely candidate. The calculation in Table 4 shows that the modest variation in values of width, thickness, and fiber volume fraction of the pectinate zone work together to explain the frequency range of the GP cochlea. The change in the volume stiffness is five orders of magnitude. However, the direct measurement of the GP cochlea by Bksy (1960) shows a change of three orders of magnitude, with a reasonable extrapolation to four orders of magnitude. Similarly, Zhang et al. (1997) find that the point load stiffness variation is inadequate to explain the frequency range in gerbil. With a different preparation, however, Emadi et al. (2004) find much more compliance in the apical region, which seems to fit the theoretical values from the geometry. The conclusion is that the soft cells covering the BM make point load or volume compliance measurements difficult to interpret. As is often the case, a combination of theoretical and experimental approaches is needed.

H. General summary
There are many acoustical and mechanical transformations performed by outer ear, middle ear and cochlear structures. The components in the mammalian ear are more elaborate than those in non-mammalian vertebrates, with the advantage of a subsequently extended frequency range. The anatomically intricate complexity of the mammalian ear ultimately results in greater functional capabilities. Some of quantifiable variables are sensitivity, frequency bandwidth, frequency resolution, dynamic range and sound localization. The structures that lead to these capabilities do so given the available biological materials, space constraints within the skull, and limitations imposed by biophysics. Several fundamental biophysical principles provide the means for obtaining the proper mechanical forcing of receptor cells in the inner ear. Each of the transformation steps can be described by a basic principle that can be readily understood using computational biomechanics. The objective of each transformation is to preserve the sound relevant to the species for the stated functionality. Each implementation is, however, much more complicated and involves biomechanical principles that are not all well characterized, yet

48

to be implemented in any man-made device, and not free from controversy. Less controversial is the spatially dependent transformation of sound by the pinna and the ear canal. The next step is the impedance alleviation between the air and fluid of the cochlea, which requires an area change provided by the eardrum to stapes footplate. It is not possible to have a rigid, massless piston for this, so the tympanic membrane is an elaborate vibrating system with mistuning of the different radial sectors, each with significant resonances for frequencies over about 2 kHz. The ensemble, however, delivers a fairly smooth pressure to the ossicular chain. In the ossicular chain, the principle of a lever advantage is also readily grasped, but the chain does not behave as a simple lever for higher frequencies (> 2kHz). An adequate understanding of how the pressure is transmitted to the cochlea is yet to be attained. In the cochlea, the local resonance at BF is easily calculated for the BM immersed in fluid and soft cells. The reality of transmission of the pressure to this point involves the fast wave and the slow traveling wave, with its long and short wavelengths. The BF is not really a resonance in the sense of a set of tuned strings, but rather a point of transition to very short wavelengths. The actual BF location depends on fluid viscosity, width of the partition with respect to the BM, and sound level. The enhancement of the traveling wave by the active process for low levels of sound remains a subject of contention. The simplest model of feed-forward provided by the geometry and the motility of the OHC appears to explain much. Such a distributed system of sensors and actuators is effective in enhancing the BM response near BF. Finally, the transformation from BM motion to excitation of the IHC has the simple explanation of cilia being dragged through fluid. The details of the environment of the cilia and the proximity of the Hensen stripe make the actual cilia-fluid response much more complicated. Calculations for low frequency have a resemblance to measurements in IHC and in the neurons of the auditory nerve. However the full effect of the complex geometry for the full range of frequency and amplitude is yet to be examined. It is safe to predict that other mechanical design features are present in the OC to obtain the proper excitation of the IHC, which are not yet anticipated. The interplay between physiological measurements and bio-computational models helps to elucidate the knowns from the unknowns and thus provides a path towards greater understanding.

49

Acknowledgements
Many thanks to Gerald Popelka, Stefan Heller, and to the editor Peter Dallos for helpful comments and suggestions on earlier drafts. This work was supported in part by grant R01 DC 05960 from the National Institute of Deafness and other Communication Disorders of the National Institutes of Health and by grant RGP0051 from the Human Frontiers of Science Program.

50

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The work for the absolute threshold of hearing

-18

(p

/ !c " Area " Time is easiest to estimate at the

tympanic membrane and it is about 6x10 J for the energy for humans, using a threshold of hearing of p = 15 Pa (-3 dB SPL), pars tensa Area = 55 mm2, ! = 1.18 kg/m3, c = 344 m/s, Time = 0.2 sec. If we assume that there is a loss of a factor of two between the middle ear and hair cell detectors, the threshold of hearing becomes about 3x10-18 J.

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ii

A dark-adopted eye requires 90 photons within 0.1 sec to perceive a flash. However, the estimate is that only 10% of the photons entering the eye actually reach the cones, so that gives about 10 photons necessary for the perception (Hecht, et al. 1942). The energy of a single photon in the middle of the visible spectrum

( !c / ! ) is 4x10

-19

J, using ! = 6.6 ! 10 Js , c = 3 ! 10 m/s , and ! = 500 " 10 m . Therefore, for 10

-34 8 -9

photons the energy is 4x10-18 J.

iii

It has been observed for some time that the threshold of hearing in subjects can has jumps in it. However, the mechanism behind this behaviour is not well understood and may well be related to non-linear properties of the cochlea at low level and internal reflections leading to standing waves.
iv

Here it is assumed that the middle ear cavity pressure at the round window is negligible which is the case in normal ears. In pathological ears the pressure at the oval and round windows maybe more comparable, due to acoustic coupling, and thus the important determining variable there is the pressure difference between the two windows (Merchant et al., 1997).
v

The specific impedance was calculated as the measured cochlear input impedance Zc times the footplate area. In humans the average magnitude of Zc is 21/2x21x109 kg/sec-m4 and the average footplate area is 3.21x10-6 m2 (Aibara et al. 2001). The 21/2 is to convert the peak velocity to rms velocity.
vi

The one exception to this is the recent finding that the concave-eared torrent frog species listen to mating calls that are pres
vii

The reciprocal of this can is found in loudspeaker designs. If one takes an isolated loud-speaker (the output driver) it would operate as a dipole generating nearly equal opposite signals from the two sides that would tend to cancel in the far field. To increase the acoustic output of a speaker driver, it is almost always placed in a cabinet that prevents cancellation from the opposite phase.

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