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AM. ZOOLOC.IST, 0:451 -460(1906).
Ear Structure and Function in Modern Mammals
DOUGLAS B. WEBSTER
Biology Department, New York University, Bronx, Xew York
SYNOPSIS: The acoustic portions of the mammalian ear display greater morphological diversitx
in peripheral than in central portions. In many mammals the pinna is of negligible auditory
significance. The tympano-ossicular system of all mammals sensitive to air-borne sounds must
transform air vibrations to fluid vibrations in the inner ear by matching the acoustical
impedances. Within the cochlea the energy of the fluid vibrations is transduced into nerve
impulses.
In highly specialized mammals the morphology of these transformer and transducer mechanisms is adapted for the reception of extreme frequencies. Echolocating bats and whales
possess different, but effective, specializations for the reception o( ultrasonic frequencies.
Moles and kangaroo rats, on the other hand, have specialized ear structures for the reception
of low frequencies.
mammals such as the deer, in which the
directionality of the pinna reflex suggests an
ability to "funnel in" sounds from a particular direction. However, prominent pinnae
are certainly not necessary for the accurate
localization of sound, as is exemplified by
owls, which, lacking pinnae, nevertheless
obtain food by extremely accurate sonic
localization (Payne, 1961).
As useful as the external ear apparently
is to some mammals in aiding audition, it
may have an even greater adaptive value
in maintaining homeothermy. The pinna,
with its large, vascularized surface area, is
an ideal mechanism for dissipating excess
body heat. Elephants rhythmically wave
their large thin pinnae on warm days, thus
increasing the rate of cooling of the blood
flowing through them (Young, 1957). Rabbits inhabiting warm climates have been
shown to have larger external ears than
EXTERNAL EAR
rabbits living in colder climates (Hamilton,
The diversity of forms of pinna in mam- 1939). Since the pinna reflex is absent in
mals is obvious, varying from no pinna at many mammals, it is possible that this organ
all in cetaceans and moles, to the huge flap- often serves primarily as a heat dissipator
like ears of proboscidians. The adaptive rather than as a hearing aid. It is not at
value of these structures is less obvious. Jt all unlikely, then, that the pinna may have
has usually been assumed that they have an come into being as homeothermy evolved,
auditory function, and indeed the auditory rather than as part of an evolving auditory
significance of the pinna is easily noted in system.
From the pinna, the external auditory
The original work reported in this paper was
meatus
carries air-borne vibrations to the
supported by grants NB04365 and NB05800 from
tympanic
membrane. Its irregular course,
the National Institutes of Health, and a grant
stiff hairs, and ceruminous glands all serve
from the National Science Foundation.
As is the case with most morphological
units, the ear displays greater phylogenetic
diversity in its peripheral portions than it
does in its central portions. At the grossest
level, the "labyrinth" or inner ear occurs in
all vertebrates; a distinct middle ear consisting of pharyngeal pouch and tympanic
membrane is found only in tetrapods; and
the "pinna" or external ear is peculiar to
mammals. Among living eutherian mammals, products of an adaptive radiation of
one hundred million years, this same generalization can be made: morphologically,
the inner ear is the most conservative and
the external ear the most varied. Because
there is this greater evolutionary plasticity
in distal portions, one expects, and finds,
greater adaptations to environmental pressures in the external and middle ears than
in the inner ear.
(451)
452
DOUGLAS B. WEBSTER
to protect the delicate tympanic membrane.
MIDDLE EAR
The middle ear is primarily a mechanical
device transforming air vibrations into vibrations strong enough to move the fluids
of the inner ear. Air-borne sounds are not
readily transmitted to a fluid medium, as
is illustrated by one's failure to hear sounds
produced in air when one's head is under
water. Jn such a situation the acoustic
energy is almost entirely reflected from the
water surface. The air-borne sound would
be heard if the acoustic impedance of the
air were matched with that of water, which
would require that the force per unit area
at the water surface be increased twentyfold. Such a pressure increase allows the
acoustic energy to be absorbed rather than
reflected. Similarly, in order for air-borne
vibrations efficiently to cause vibrations in
the fluids of the inner ear, the pressure must
be increased by a factor of twenty. The
middle ear of all tetrapods sensitive to airborne sounds performs this necessary function.
This impedance matching is made possible by the geometry and mechanics of
the tympanic membrane and three auditory
ossicles. Two simple and fundamentally
different mechanical processes effect the
pressure increase. First is a simple lever
system. The fulcrum of the lever is the
ossicles' axis of rotation, which runs through
the anterior ligament of the malleus and the
posterior ligament of the incus. The long
lever arm reaching the fulcrum is the manubrium of the malleus, attached along its
entire lateral surface to a radius of the tympanic membrane. The short lever arm is
the long process of the incus, running
roughly parallel to the manubrium of the
malleus and terminating with a medial
right-angle turn to articulate via its lenticular process with the head of the stapes
(Fig- 2).
When a condensation-wave strikes the
tympanic membrane, forcing it to move
medially, the malleus and incus must rotate along their axis of rotation, causing the
lenticular process of the incus to push the
stapes into the fenestra ovale of the cochlea.
The increase in force at the stapedial head
is a direct function of the different lengths
of the manubrium of the malleus and the
long process of the incus (the two lever
arms). However, in this, as in all lever
systems, an increase in force is coupled
with a corresponding decrease in amplitude of movement. The latter fact necessarily limits the effectiveness of the lever
system. If the entire twenty-fold increase in
pressure were produced through the lever
system, the equally great decrease in amplitude would essentially nullify all movement. Indeed, this lever system usually increases pressure about two-fold (VVever and
Lawrence, 1954) and it is quite rare that
it amplifies by more than a factor of five
(Henson, 1961).
The second mechanism increasing pressure at the fenestra ovale involves the relative surface areas of the tympanic membrane and the footplate of the stapes. Sound
pressure is collected by the tympanic membrane and, by way of the ossicular chain, is
concentrated onto the much smaller footplate of the stapes. This transfer of acoustic
energy from a large surface area to a small
one increases the force per unit area as a
ratio of the two surface areas involved.
In mammals, since only about two-thirds of
the tympanic membrane acts in moving the
malleus, this fraction must be taken as the
effective surface area of the tympanic membrane (YVever and Lawrence, 1954). Even
with this reduction, the calculated increase
in pressure at the fenestra ovale is, in the
mammals studied, at least fourteen-fold
(VVever and Lawrence, 1954; Henson, 1961).
The calculated effect of these two amplifying mechanisms is, in the mammals analyzed, at least sufficient to increase pressure
at the fenestra ovale by a factor of twenty
and, theoretically, would appear to allow
efficient transfer of acoustic energy to the
fluids of the cochlea. However, this analysis
of dynamics of the middle ear has unrealistically assumed that the mechanism works
with 100% efficiency. There is, of course,
resistance to tympano-ossicular movements,
MAMMALIAN EAR APPARATUS
I'"IG. 1. Organ ol Cxirti of the Mongolian gerbil,
Meriones imgiiiailatiis. B, basilar membrane; H,
cells of Hensen; IH, inner hair cells; OH, outer
hair cells; S, spiral ganglion cells; SV, stria vascu-
laris; T, tectorial membrane.
TIG. 2. Ventro-lateral view of the middle ear of
the guinea pig with tympanic membrane removed.
C, cochlea; I, incus; M, malleus.
454
DOUGLAS B. WEBSTER
which damps the system and reduces the
theoretical amplification of pressure. Briefly stated, the extent of this damping is determined by friction, elasticity, and mass.
Friction is determined by the attachments
and tonus of the intra-aural muscles, by
the geometry and stiffness of the ossicular
ligaments, and by the flexibility of the tympanic membranes and the annular ligament
of the fenestra ovale. Of these structures,
the intra-aural muscles are of prime importance since when they contract they
greatly increase damping in the entire apparatus. That the tensor tympani muscle,
attaching to the manubrium of the malleus,
and the stapedius muscle, inserting on the
neck of the stapes, act to protect the delicate
organ of Corti from damaging overstimulation from low frequency sounds has been
well established. Wiggers (1937) demonstrated that upon spontaneous contraction
of the intra-aural muscles, transmission
through the ossicular system of the guinea
pig was reduced for frequencies below 1000
cps, slightly enhanced for frequencies between 1300 and 1800 cps, and unaffected for
frequencies from 2000 cps to 2500 cps.
The elasticity of the system depends on
the same factors that affect friction, but in
addition is affected by the volume of the
closed middle ear cavity. An excessively
small middle ear cavity will damp movements of the tympanic membrane due to the
relatively small elasticity of a small enclosed air space (Webster, 1962).
The mass in this determination ol damping is the total weight of the tympanic
membrane and auditory ossicles, plus the
relationship of the system's center ol gravity
to its axis of rotation.
Time and space do not allow a detailed
analysis of the role of each structure affecting this complex damping mechanism, and
in any case there is considerable morphological variation. Suffice it to note here that
were the system not at least slightly damped,
resonance phenomena would occur which
would make hearing highly non-linear and
might also result in prolonged after-stimulation of the inner ear.
Considerable morphological diversity exists in the bones forming the walls of the
eutherian middle ear cavity. In primates
the middle ear is bounded almost entirely
by the petrous and mastoid portions of the
temporal bone. In most other eutherians
the middle ear is bounded largely by the
entotympanic and ectotympanic bones. In
the adult, these may be separate bones or
fused in various combinations to form bone
complexes. In some eutherians, e.g., elephant shrews (Keen and Grobbelaar, 1941),
the squamosal and alisphenoid also contribute to the walls of the middle ear cavity.
This structural diversity among living forms
suggests that the bony walls of the eutherian
middle ear evolved independently in several
lines during the Cenozoic Era.
INNER EAR
It is easier to describe the structures involved in the inner ear because far less
variation occurs here than in the middle or
external ears. The most obvious variation
in the inner ear is the number of turns of
the cochlear coil, which ranges from two
to five, apparently irrespective of auditory
characteristics such as frequency or intensity
ranges.
In all mammals studied, the cochlea has
essentially the same morphology. Along the
cochlear turns the two perilymphatic spaces
(scala vestibuli and scala tympani) course
above and below the endolymphatic space
(scala media). Vibrations arrive by way of
the stapes in the fenestra ovale at the base
of the scala vestibuli and are dissipated at
the membrane of the fenestra rotunda in
the base of the scala tympani. At the apex
of the cochlea the two perilymphatic
spaces conjoin at the helicotrema. Reissner's
membrane separates the perilymph of the
scala vestibuli from the endolymph of the
scala media.
In the past it has been assumed that the
perilymphatic fluid of the scala tympani
was bounded by the basilar membrane, but
more recent work has suggested that the
reticular lamina forms this boundary
(Davis, 1959). Thus, most of the organ of
Corti may lie in the scala tympani with
MAMMALIAN EAR APPARATUS
455
cndolympli only in the scala media between quency cause maximum movement where
Reissner's membrane and the reticular la- the basilar membrane is narrowest, namely
mina. The epithelium of the organ of in the basal portion. Tones of low frequenCorti rests upon the basilar membrane, cy cause maximal movement where the
which is narrowest in the basal turn and basilar membrane is widest—in the apical
widest at the apex of the cochlea. The turn (Bekesy, 1954). Therefore one can
supporting cells of Deiter, the pillar cells, create a frequency map along the course
cells of Hensen, and cells of Claudius rest of the cochlea and account at least qualitaupon this basilar membrane (Fig. 1). The tively for frequency analysis. Since the
hair cells—usually one row of inner hair movements of the basilar membrane follow
cells and three rows of outer hair cells—are the temporal course of the stapes, temporal
supported basally by Deiter's cells, which analysis of sounds is possible. The amplialso send up phalangeal processes parallel tude of movement of the basilar membrane
to the hair cells; these processes then extend is a function of the intensity of the sound,
over the hair cells to form part of the retic- so intensity information is also represented
ular lamina. The "hairs" of the hair cells by inner ear kinetics.
protrude through this reticular lamina and
Some of the most valuable clues to the
their distal portions contact the tectorial actual transducer function of the cochlea
membrane whose internal attachment is to come from the investigations of the biothe spiral limbus. Innervation is from the electrical properties of the cochlea (Davis,
bipolar cells of the spiral ganglion, located 1959. The scala media maintains a resting
within the modiolus. The dendrites of these endocochlear potential of approximately
cells extend out through the habenula 80 mV positive to other extracellular spaces
perforata where they lose all myelin and including the perilymphatic fluid spaces.
end in synaptic relationship to the hair This endocochlear potential is produced
cells. There is also ample evidence for ef- by the stria vascularis and is highly oxygenferent cochlear fibers originating in the dependent. Upon acoustic stimulation, a
superior olivary nucleus and terminating at second non-neural bioelectric potential—the
the hair cells (Rasmussen, 1953). Variation cochlear microphonic—can be recorded. Its
in the cellular morphology of the cochlea origin is from the vicinity of the hair cells,
is slight, usually affecting only the relative perhaps at the reticular lamina over the
sizes of the border cells of Hensen and hair cells (Davis, 1959). It consists of an
Claudius (Pritchard, 1876; Fernandez and alternating current whose wave form mimSchmidt, 1963).
ics that of the sound presented. Within
Whereas the middle ear can be regarded physiological limits, the strength of this poas a transformer mechanism changing air- tential is a function of the intensity of the
borne vibrations into fluid vibrations, the sound played—rarely exceeding 2 mV. It
cochlea must be regarded as a transducer exhibits no true threshold, is not an "allchanging the information from fluid vibra- or-none" phenomenon, and does not fatigue
tions into nerve impulses which accurately readily.
maintain frequency, temporal, and intensity
Two other bioelectric potentials, positive
information concerning sounds received.
and negative summating potentials, have
Frequency analysis within the cochlea been recorded from the cochlea during sonic
appears to be primarily related to the locus stimulation. They are expressed as changes
of maximal physical movement along the in the base-line of the cochlear microphonic
basilar membrane.
Fluid vibrations, — during sonic stimulation and are always
brought into the cochlea by the stapes, cause much smaller than the cochlear microtraveling waves along the spiral course of phonic itself. The summating potentials
the cochlea; these traveling waves move the also require more intense stimulation by
basilar membrane, organ of Corti, and sound. The mechanical event triggering
Reissner's membrane. Tones of high fre- the cochlear microphonic and summating
456
DOUGLAS B. WEBSTER
potentials is thought to be a shearing force
between the tectorial membrane and the
reticular lamina, necessarily bending the
"hairs" of the hair cells (Davis, 1959). This
shearing force is created whenever the basilar membrane vibrates, for the basilar
membrane pushes the cells resting on them
and causes a sliding against the tectorial
membrane, since the latter is firmly attached to the spiral limbus. The alternate
bending of the "hairs" of the hair cells may
well create an alternating modulation of
the cndocochlear potential, which may be
recorded as the cochlear microphonic. The
summating potentials occurring with more
intense stimulation may be caused by nonlinear characteristics of the basilar membrane which cause a predominant bending
in one direction or another (Davis, 1959).
The final bioelectrical potentials recorded
from the cochlea are the action potentials
of the eighth nerve which, of course, follow
the general characteristics of all nerves. It
has been speculated that the cochlear microphonic may directly depolarize the bare
nerve endings near the hair cells and thus
directly trigger the nerve impulses (Davis,
1954). This seems morphologically unlikely due to the elaborate synaptic endings on
the hair cells (Smith and Dempsey, 1957;
Spoendlin and Gacek, 1963), suggesting that
the hair cells have more than a mechanical
function via their "hairs." Experimental
work has substantiated this view, for it has
been demonstrated that after thermoelectric
cooling of the cochlea, the mass action potentials arc substantially decreased in amplitude and their latency is greatly increased.
The cochlear microphonic is also affected
but to a much less degree (Coats, 1965).
The above suggests the possibility of a
biochemical process intermediate between
the cochlear microphonic and the action
potentials. Any such biochemical phenomenon would require an energy source. Histochemical studies have shown that the
oxidative enzymes of the cochlear duct are
concentrated in the stria vascularis and the
hair cells (Plotz and Perlman, 1955; Vosteen, 1960; Spoendlin and Balogh, 1963).
Therefore an energy source is available.
Where one finds a chemical triggering of
nerve impulses, one further expects to find
esterase activity, such as the acetyl cholinesterases at motor synapses and end plates.
In the cochlea, all the activity of acetyl
cholinesterase appears to be concerned with
the endings of the olivocochlear bundle, not
with the sensory neurons (Schuknecht, el
at., 1959). Our own histochemical studies
have shown a concentration of esterases in
borh the hair cells and in the cells of Hensen. These are not cholinesterases but are
non-specific, probably aliphatic, esterases.
The possibility exists, therefore, that the
cochlear microphonic may trigger the release of a transmitter substance from the
hair cells, which in turn triggers the nerve
impulse, and—further—that this transmitter
substance may be deactivated rapidly by
esterases.
The basic structures and their means of
functioning, to transmit acoustic energy
through the middle and inner ears and then
to transduce it into nerve impulses at the
organ of Corti, are basically the same in
most mammals. As stated earlier, when
variation in the basic pattern does occur
it is more often in the peripheral than in
the central portions of the ear. The greatest
degree of these variations is found in mammals which have become adapted to extreme
environments where selective pressure has
been the most severe. Therefore, to appreciate the range of variation in both structure and function among eutherian mammals, the adaptations of fossorial mammals
(moles), aquatic mammals (porpoises), aerial mammals (bats), and specialized desert
mammals (kangaroo rats) will be discussed.
EARS OF MOLES
The mole, in its underground habitat,
would be expected to depend more on
low frequencies than high frequencies, since
high frequencies are readily absorbed by
loose dirt (Henson, 1961). It may even
be more adaptive for the mole to hear
substrate vibrations than air-borne vibrations. The mole completely lacks a pinna
but does possess an external auditory
meatus. The bony complex forming the
-157
MAMMALIAN EAR APPARATUS
walls of the middle ear cavity is fused to
the adjacent skull bones (Henson, 1961).
This may be of some significance since in
most mammals the tympanic bulla and
otic bones are only loosely articulated with
the rest of the skull. Strong articulation
with the rest of the skeleton may improve
the ear's sensitivity to bone-conducted vibrations.
T h e mole has a relatively large tympanic
membrane and auditory ossicles. T h e malleus is connected to the tympanic membrane
not only via the length of the nianubrium
but also by means of the large anterior process and the lateral process. T h e tympanic
plate of the malleus shows an osseous and
cartilaginous connection with the ectotympanic and squamosal. Instead of the usual modest superior ligament of the malleus,
there is an extensive superior ligament
attaching along the head of the malleus and
the head and short process of the incus. T h e
articular surface between the malleus and
incus is nearly flat instead of having the
usual concave and convex superior and inferior facets. Concerning the intra-aural
muscles, the tensor tympani is lacking and
the stapedius is only poorly developed. T h e
ossicular mechanical advantage is 2.2:1,
and the ratio of surface area of tympanic
membrane to surface area of stapedial footplate is 14:1 (Henson, 1961). Therefore, assuming that only two-thirds of the tympanic
membrane acts in moving the malleus, the
total theoretical mechanical advantage is
21.1:1. This would appear to provide sufficient impedance matching, except that the
middle ear is more highly damped than
usual due to the strong articulating processes and ligaments of the ossicles, which
must considerably reduce the real mechanical advantage. Therefore, although the appropriate behavioral and physiological data
are lacking, the mole would appear to have
relatively poor reception of air-borne
sounds, especially for high frequencies.
However, the system is morphologically well
suited—due to its strong osseus articulation—for the reception of bone-conducted
sound which would, of course, have con-
siderable adaptive value in the mole's subterranean environment.
EARS OF WHALES
Cetacea are unusual among mammals in
being wholly adapted to an aquatic environment. Furthermore, cetaceans have
been shown to utilize ultrasonic echolocation in the water, much as bats do in air,
with emitted frequencies ranging up to
80 Kc (Kellogg, 1961). Morphologically,
the auditory portions both of the ear and of
the central nervous system are highly specialized in cetaceans. There is no pinna,
but the long, narrow, external auditory
meatus is lined throughout its tortuous
course not only by epithelium but also by
cartilages and skeletal muscles representing
vestiges of the normal mammalian pinna.
In baleen whales the external auditory
meatus is plugged by a waxy substance
throughout at least part of its course (Fraser and Purves, 1960).
The tympano-petrous portion of the ear
is attached to the remainder of the skull by
ligaments only and thus lies quite separate,
surrounded by a complex pneumatic system. This "air-foam insulation" effectively
damps vibrations coming to the ear from
any route except through the external auditory meatus. The meatus terminates medially at the highly modified, massive tympanic membrane. This membrane, instead
of being the usual "flat cone," is shaped
more like a filled ice-cream cone and is
made up largely of tough connective tissue.
The height of the cone is several times
the length of the malleus. Only the apex
of the cone attaches to the malleus and
that only to the distal tip of the manubrium, to form an acute angle of about' 30°
with the manubrium. The manubrinin is
firmly attached via its anterior process to
the tympanic annulus and articulated in
much the normal fashion to the incus,
which, in turn, has a normal articulation
with the stapes (Fraser and Purves, I960).
Functionally, the cetacean external ear
and middle ear must transport vibrations
from the external fluid medium to the
DOUGLAS B. WF.BSTER
459
MAMMALIAN EAR APPARATUS
FIG. 3. Diagram of the middle ear of a pilot whale,
Globicejthala melaena. C, cochlea; EAM, external
auditory meatus; I, incus; M, malleus; S, stapes;
TL, tympanic ligament: TT, tensor tympani.
(Drawn from photograph in Fraser and Purves,
1960.)
FIG. 4. Doisal view of the skull of the kangaroo
rat, Dipodomys merriami. I, iiuerparietal; M,
mastoid; P, parietal; S, supraoccipital.
fluids of the inner ear; in this case there is
no problem of impedance matching-. However, for accurate echo-location, the system
must provide for accurate localization of
sound and the reception of the very small
amplitudes of ultrasonic vibrations. This
problem might be complicated by the possibility of sound entering the ear through all
parts of the body in an aquatic medium.
However, in the case of cetaceans, the "airfoam insulation" around the tympano-petrous bone provides acoustical isolation of
the two ears from all sources except the tympanic membrane. Acoustical amplification
is provided by the tympanic membrane,
usually referred to in cetaceans as the tympanic ligament, which acts as a fourth auditory ossicle (Fig. 3). It is much longer than
the manubrium of the malleus, and it attaches to the malleus at an acute angle;
this, pushing like a ratchet crank against
the malleus, causes a great increase
in amplitude of movement at the tip of the
manubrium. The manubrium of the malleus is about the same length as the long
process of the incus and so causes no change
of pressure or amplitude. Therefore, a
lever system increases the amplitude 30-fold
with a correspondingly decreased pressure.
This decrease would cause a serious transmission problem were it not that the effective surface area of the tympanic ligament
is over 30 times larger than the surface
area of the footplate of the stapes. In this
manner the amplitude of movements is
greatly increased while the pressure remains
approximately the same, allowing for adequate transfer of vibrations from one fluid
medium to another (Fraser and Purves,
1960).
In the cetacean cochlea, the morphological modifications are not so extreme. In
the first turn of the cochlea the basilar
membrane is extremely narrow, as would be
expected for the reception of ultrasonics.
Other cochlear pecularities include unusually large cells of Claudius and large, heavilymyelinated fibers of the cochlear division of
the eighth cranial nerve. The functional
significance of the latter modifications remains to be explored.
EARS OF BATS
The Chiroptera are the only order of
flying mammals. Cetaceans are the largest
mammals and chiropterans among the
smallest, yet both orders are adapted for
the reception of ultrasonics and both can
navigate by echolocation. The ability of
bats, by echolocation, to avoid fine wires and
to catch small flying insects is widely known
(Griffin, 1958). Less widely known are the
morphological adaptations which make
these feats possible.
The size of the pinna in echolating bats
is highly variable—from mouse-like proportions to external ears much longer than
the head itself. In large-eared bats, individual parts of the pinna are often further
hypertrophied, especially the tragus. Griffin
(1958) has suggested that these large external ears may play an important role in determining directionality of sound and/or
in tuning the ear to specific high frequencies whose wave lengths are approximately
the length of the tragus in some bats.
The morphology of the middle ear of
echolocating bats is not as variable as that
of the external car. The following data
from Henson (1961) illustrate the adaptations of the middle ear for the reception of
ultrasonics. The tympanic membrane has the
normal mammalian form but, in bats using
high ultrasonics, it is very small—having a
surface area of less than 3 mm2. The pars
flaccida is reduced in size to only the small
portion attached to the lateral process of
the malleus. The manubrium of the malleus is unusually long and often spatulated
460
DOUGLAS B. WEBSTER
MAMMALIAN EAR APPARATUS
461
FIG. 5. Dorsal view of lefl mastoicl sinuses oE
the kangaioo rat, Dipodomys merriami. A, anterior
mastoicl sinus; I, incus; M, malleus; P, posterior
mastoid sinus; S, semicircular canals.
FIG. 6. Ventral view of the middle ear of the
kangaioo rat, Dipodomys merriami, with tympanic
membrane removed. C, cochlea; I, incus; M, malleus; R, round window; s, stapes; ST, stapedial
artery; T, tensor timpani.
only in the distal portion. The attachment
of the tympanic membrane to the malleus
is firmer at the spatulated portion than at
the more proximal parts. This stronger attachment at the umbo causes the malleus to
be moved primarily by the portion of the
tympanic membrane which undergoes the
largest amplitudes. The anterior process of
the malleus is finely ankylosed with the
tympanic bone, and the malleo-incudal joint
is particularly complex, with superior and
inferior facets at sharp angles to each other.
The long process of the incus is relatively
short and articulates distally with a particularly small stapes. The ossicular mechanical advantage, determined by the relative
lengths of the malleolar manubrium and
the long process of the incus, varies from
4:1 in CAossophaga and Rhinolophus to
5:1 in Natnlus (Henson, 1961). Therefore
the ossicles allow considerable increase in
force at the stapes, but with a corresponding reduction in amplitude of movement.
The ratio of surface area of tympanic membrane to that of the stapedial footplate
varies from 16:1 in Natalus to 13:1 in
('•lossopliaga and Myotis. Therefore, assuming that only two-thirds of the tympanic
membrane acts in moving the ossicles, the
increase in pressure at the footplate of the
stapes varies in bats using ultrasonics from
56.3:1 in Rhinolophus to 91.6:1 in Myotis.
These very high transformer ratios, combined with the small mass of the tympanoossicular system, admirably adapt the middle ear for transmission of ultrasonic vibrations (Henson, 1961).
A major physical problem involved in
all echolocating animals is that the emitted
sound must not so overstimulate the ear
that the ear cannot detect the much weaker
echoes. In cetaceans this damping is apparently solved by "air-foam" spaces insulating the tympano-petrous bone from the
bones and tissues of the rest of the body. In
bats, no such insulating device is available.
However bats possess extremely large intraaural muscles in relation to the size of their
middle ears. Hartridge (1945) has suggested that during each emitted pulse these
muscles contract, thereby damping the middle ear to such an extent that the inner
ear is ony minimally stimulated. This
theory has been substantiated by Henson
(1965). Using bats with chronic electrodes
implanted in the stapedius muscles, he
found that immediately prior to each emitted pulse the stapedius muscle contracts
strongly, relaxing during the duration of
the pulse. Cochlear microphonic recordings indicated that larger electrical responses are elicited by the echoes than by the
emitted pulse. At pulse rates over 140/sec,
the stapedius remained contracted during a
series of emitted pulses. The data suggested
that only the stapedius and not the tensor
tympani is involved in this adaptive reflex.
As is generally the case, the inner ear
of the bat is less altered than the middle
and external ears. The first turn of the
cochlea is relatively large and contains a very
narrow basilar membrane, as would be expected for ultrasonic reception and as is
also the case in cetaceans. The zona pectinata of the basilar membrane contains a
large hyaline mass which, it has been suggested, has an auditory significance. Possibly this allows the zona tecta to vibrate
independently in response to high frequency
stimulation (Griffin, 1958).
EARS OF KANGAROO RATS
Desert regions offer an environment perhaps as severe to mammals as the water, air,
and subterranean environments already discussed. In the desert regions of central
Asia, northern Africa, and southwestern
North America, distantly related desert rodents are found with similarly highly modi-
462
8
DOUGLAS B. WEBSTER
MAMMALIAN EAR APPARATUS
163
FIC. 7. Cochlcai duct of the kangaroo rat, Dipodomys merriami. B, basilar membrane; OC, organ
of Corti; RM, Reissner's membrane; SG, spiral
ganglion; SV, stria vascularis; T, tectorial membrane.
FIG. 8. Organ of Corti of the kangaroo rat,
Dipodomys merriami. C, cells oC Claudius; D, cells
of Deiter; H, cells of Hensen; IH, inner hair cells;
OH, outer hair cells; R, elevated reticular lamina;
T, tectorial membrane; ZP, zona pectinata of basilar membrane; ZT, zona tecta of basilar membrane.
fied auditory apparati. Gerbils, jerboas,
and kangaroo rats all have hypertrophied
middle ear cavities in association with nocturnal habits, saltatorial locomotion, and
the ability to survive on a diet containing
little or no free water.
Of these rodents possessing specialized
auditory systems, the kangaroo rat, Dipodomys, has been most extensively studied
(Webster, 1961, 1962), and its morphology
and physiology will be discussed here. The
pinnae are of modest size and show no unusual characteristics. The external auditory meatus is unique only in that the ceruminous glands lining it are of a sebaceous
nature instead of being modified tubular
glands—an obvious adaptation for the conservation of water.
The middle ears arc, grossly, the most
prominent cranial specialization, distorting
the entire shape of the skull and extending
to the dorsal surface. In dorsal view, the
skull is roughly triangular in shape, with
the bulla walls forming most of the base
of the triangle (Fig. 4). The greatest part
of these inflated middle ears is caused by
the hypertrophy of the usually modest mastoid region. Because of the mastoid's large
size, the supraoccipital is reduced to a narrow bone in the midline, the interparietal
is almost "squeezed" out of existence, the
parietal is pushed forward, and the squamosal is reduced to a small bone in the
posterior wall of the orbit.
Internally, the cavity of the middle ear is
larger than the cranial cavity, and 82% of
its volume is the mastoid portion. The remaining 18% is the entotympanic portion,
enlarged primarily by an antero-medial inflation reaching to the pharynx where the
Eustachian tube is more a tiny foramen
than a true tube.
This entire middle ear cavity is incompletely subdivided into three portions: an
anterior mastoid sinus (49% of the total
volume) is separated by a thin bony lamina
from a posterior mastoid sinus (33% of the
total volume) (Fig. 5). Each of these sinuses
communicates ventrally with the entotympanic cavity (18% of the total volume, as
described above). The medial and ventral
portions of the petrous bone are partially
eroded, leaving the outlines of the semicircular canals bulging prominently into the
mastoid sinuses and the cochlea bulging
into the entotympanic cavity (Fig. 5).
The tympanic membrane is shaped like
a flat cone. In a 40 g Dipodomys merriami
the diameter is 5.5 mm and the height is
1.0 mm; the surface area of the tympanic
membrane is thus 25.9 mm2. The spatulate
manubrium of the malleus is embedded in
a dorsal radius of the tympanic membrane.
The head of the malleus and body of the
incus lie in the foramen connecting the entotympanic cavity with the anterior mastoid
sinus. The axis of rotation, as in most
mammals, runs through the anterior ligament of the malleus and posterior ligament
of the incus. The anterior process of the
malleus is attached to the tympanic bone
by an extremely tenuous ankylosis. The
short process of the incus is attached to the
petrous by a fine, two part, posterior ligament (Fig. 6). In the kangaroo rat both
the superior and lateral ligaments of the
malleus are completely lacking. The malleo-incudal joint is a firm complex joint
with superior and inferior facets meeting at
a sharp angle. A typical amphiplanar joint
exists between the lenticular process of the
incus and the head of the stapes. The
stapedial footplate is bullate in shape and
has a surface area of 0.60 mm2. There is
nothing unusual about either of the intraaural muscles.
Functionally, the relative lengths of the
manubrium of the malleus and long proc-
464
DOUGLAS B. WEBSTER
ess ol the incus give an increase in mechanical force of 3.38:1, and the effective ratio
of the surface area of the tympanic membrane to that of the footplate of the stapes
imparts a pressure increase of 28.7:1. Therefore the theoretical total transformationfactor is 97.2:1. Not only is this a large
transformation-factor, but the tympanoossicular system is only very lightly damped.
With both the superior and lateral malleolar ligaments lacking, the ossicles are delicately suspended along their axis of rotation. Further, the large size of the cavity
of the middle ear greatly decreases the
damping of the tympanic membrane by
giving a large "air space" for it to push
against. The large size of this air space is
particularly important for small mammals
with large tympanic membranes. By having large middle ear cavities, the relative
compression caused by movements of the
tympanic membrane is greatly decreased.
Cochlear microphonic studies on Dipodornys merriami and D. spectabilis have
shown that maximum responses occur to
stimulations between 1000 cps and 3000 cps,
indicating a hearing range of unusually
low frequencies for such a small mammal.
Within this most-sensitive frequency range,
three distinct "peaks" of hearing are indicated at 1400 cps, 1800-2200 cps, and 2600
cps. Following surgery, by which the volume of the middle ear was reduced by as
much as 75% without touching the tympano-ossicular system, the amplitude of the
cochlear microphonics is greatly reduced—
particularly in the 1000-3000 cps range. Even
with this reduction, the three peaks mentioned are still discernible, although greatly
attenuated. Upon restoring the middle car
to its normal volume, the original spectrum
of microphonics at full strength is also restored. The auditory significance of the
hypertrophied middle ear is therefore apparent.
In field studies, normal kangaroo rats
and kangaroo rats with experimentally-reduced middle ear volume were subjected to
predation by owls and rattlesnakes. With
both predators, normal and control kangaroo rats were far more successful in avoid-
ing predation than were the animals with
reduced middle ear volume. Sonagraph
analysis of the sounds produced during
predation demonstrated sounds within the
range from 1000 cps to 3000 cps. Data therefore exist indicating both the functional
characteristics and the adaptive value of
the enlarged middle ear cavities of kangaroo
rats.
The structure ol the cochlea of the kangaroo rat also shows some specializations. A
hyaline mass appears in the zona pectinata
of the basilar membrane, as it does in the
bat; however this hyaline mass is relatively
larger than in the bat (Figs. 7 and 8) .
Furthermore, the hyaline mass is smallest
in the first turn of the cochlea and becomes
larger in more apical turns. The converse
is true in the bat.
In the organ of Corti itself, the cells of
Hensen are most extraordinary. They are
flask-shaped with long cytoplasmic processes which form an elevated reticular
lamina (Figs. 7 and 8). The nuclei are
centrally placed and contain considerable
chromatin material. These cells, instead of
resting in the basilar membrane, are supported by the innermost cells of Claudius.
Along the cochlear duct, the cells of Hensen increase in size until the third turn
where they reach a total height ol 110 ^.
In the last 114 turns of the cochlea, their
height slowly diminishes to 76 ^. Therefore
the organ of Corti is most modified in the
most apical turns, where one would expect
reception of relatively low frequencies. The
function of these modified cells is not
known, but it may be ol more than casual
interest that histochemical studies demonstrate a lack of oxidative respiratory enzymes and a large concentration of nonspecific esterase in them (Figs. 9 and 10). As
mentioned earlier, esterases may be important in the initiation of nerve impulses in
the eighth nerve.
SUMMARY
The typical mammalian external ear and,
to a greater extent, middle ear are morphologically adapted for efficient transformation of air-borne vibrations of the external
10 FIG. 9. Succinic dehydrogenase activity in the
cochlea of the kangaroo rat, Dipotlomys merriawi.
H, cells of Hensen; IH, inner hair cells; OH, outer
hair cells; SO, spiral ganglion; SL, spiral ligament;
SS, external spiral sulcus; SV, stria vascularis.
'i.
I-IC;. 10. General esterase activity in
the cochlea
of the kangaroo rat, Dipodomss merria mi. H, cells
of Hcnsen; IH, inner hair cell; OH, outer hair
cells; RM, Reissnei's membrane; SL, spiral ligamenl; SS, external spiral sulcus; SV, str a vascularis
DOUGLAS B. WEBSTER
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functional aspects of certain structures of the
niediuni into Iluid-borne vibrations of the
inner ear. T h e inner ear is equally well
constructed for the transduction of fluid
vibrations into nerve impulses of the cochlear nerve while maintaining the frequency,
intensity, and temporal information intact.
Morphological diversity is greatest in the
external ear, and least in the inner ear,
conforming to the general evolutionary law
that the parts of an organism in the most intimate contact with external environment
manifest the greatest evolutionary plasticity.
Mammals living in extreme environmentsaquatic, subterranean, aerial, and deserthave specialized auditory organs adapted to
their harsh habitats.