Mammalian middle ear mechanics: A review

Abstract

The middle ear is part of the ear in all terrestrial vertebrates. It provides an interface between two media, air and fluid. How does it work? In mammals, the middle ear is traditionally described as increasing gain due to Helmholtz's hydraulic analogy and the lever action of the malleus-incus complex: in effect, an impedance transformer. The conical shape of the eardrum and a frequency-dependent synovial joint function for the ossicles suggest a greater complexity of function than the traditional view. Here we review acoustico-mechanical measurements of middle ear function and the development of middle ear models based on these measurements. We observe that an impedance-matching mechanism (reducing reflection) rather than an impedance transformer (providing gain) best explains experimental findings. We conclude by considering some outstanding questions about middle ear function, recognizing that we are still learning how the middle ear works.

Keywords: eardrum; kinematics, mechanics; ligaments; middle ear; muscles; ossicles; synovial joints.

FIGURE 1

(A) Image of the ear in cross-section by Max Brödel. The outer ear consists of the pinna and the ear canal, the middle ear of the tympanic membrane, the middle ear cavity, ossicles, and various ligaments and muscles. The three middle ear ossicles transmit the acoustic energy to the cochlea, responsible for hearing. Nerve fibers connect the inner ear via the eighth cranial nerve to the brainstem. The eustachian tube ventilates the middle ear. (B) Modified image by Bertolini and Leutert (1982), showing a magnified view of the middle ear. Essential to holding the chain of ossicles in place are the ligaments. The image shows the lateral mallear ligament (LML), superior mallear ligament (SML), superior incudal ligament (SIL), and the posterior incudal ligament (PIL).

FIGURE 2

This figure was previously published in Brister et al. (2020a). The image of the middle ear is taken from the tympanic membrane of a right ear. Above the solid black line is pars flaccida, and below pars tensa. The umbo forms the tip of the manubrium. The reflection called the cone of light points toward the nose.

FIGURE 3

The skin of the ear canal forms the outer layer of the eardrum, and the mucous lining of the middle ear cleft forms the inner layer. The ultrastructure of the tympanic membrane shows the superficial radial and deeper circumferential fibers (Locke, 2013) made of collagen types I, II, and III (Stenfeldt et al., 2006).

FIGURE 4

(A) Human malleus, (B) incus, and (C) stapes (D) Schematic representation of the attachment of the major middle ear ligaments.

FIGURE 5

Synchrotron x-ray microtomography image from the left ear’s incudostapedial joint (ISJ) and stapediovestibular joint (SVJ) in a mouse. It shows the stem and cap of the lenticular process, the long process, and the head and neck of the stapes.

FIGURE 6

Panel (A) shows the incudomalleolar joint and articulating surfaces of a mouse ear. A synovial-fluid-filled gap between malleus and incus exists (Ihrle et al. (2017). Panels (B) and (C) were taken from (Rosowski et al., 2020) and modified. The malleus (M), incus (I), stapes (S), anterior mallear ligament (AML), and posterior incudal ligament (PIL) are shown. The dotted lines show two axes of ossicular rotation, one in panel (B) and one in panel (C). The axis in (B) is axis 1 at low frequencies in the freely-mobile ear (Helmholtz, 1868; Fleischer, 1978; Puria and Steele, 2010); panel (C) shows the freely-mobile ear with the high-frequency axis 2 of rotation.

FIGURE 7

This plot is from Cheng et al. (2013), showing the change in vibration patterns and phase of vibrations of the tympanic membrane obtained with holographic measurements.

FIGURE 8

Three ossicular motion modes are described by Rosowski et al. (2020); reprinted with permission. (A) lateral and (B) posterior view of the anterior-posterior rotational axis (C) lateral and (D) posterior view of the whole-body translation, and (E) lateral and (F) posterior view of the superior-inferior rotational axis.

FIGURE 9

Electric analog of the middle ear; reprinted with permission from Zwislocki (1962). Electric elements are L for inductance, R for resistance, and C for capacitance. Elements with subscripts a, p, m, and t represent the middle ear cavities, those with d represent a portion of the tympanic membrane, and those with o represent the mallear complex.

FIGURE 10

(A) Finite element model (FEM) of the middle and inner ear. Developed by Gan et al. (2007b). (B) Connection of the middle ear with the inner ear. Model derived pressure gain of Gan et al. (2007b) compared with others in the literature, showing (C) magnitude and (D) phase angle. Modified from Gan et al. (2007b).

FIGURE 11

Characteristic ossicular motions described by Homma et al. (2009), reprinted with permission: (A) the first mode under air conduction, and (B) the second mode under bone conduction.

FIGURE 12

Input impedance of the stapes and cochlea decreases in magnitude and angle with drainage of the cochlea, demonstrating that inner ear fluid plays a crucial role in the transmission of sound. Interestingly, refilling the cochlea allows regaining input impedance angle but not magnitude. Thus cochlear fluid contributes predominantly as a resistive element to the ear input impedance. Reprinted with permission from Ravicz, M. E, et al. (2000).

FIGURE 13

Penetration depth and resolution of different imaging modalities, reprinted with permission from (Popescu et al., 2011).