Auditory systems of Heteromyidae: functional morphology and evolution of the middle ear.

Auditory Systems of Heteromyidae: Functional Morphology and Evolution of the Middle Ear DOUGLAS B . WEBSTER A N D MOLLY WEBSTER Kresyr H c ~ r r i n gRcsewrch Ltrhorcitory o j t h r South, Lonisiunu Sttrtr University Medical C e n t e r , N e w Orleans, Louisinnti

ABSTRACT Middle ears (515) from 26 species of the rodent family Heteromyidae - genera Dipodomys, Microdipodops, Perognathus, and Liomys -were studied both grossly and histologically, for qualitative and quantitative comparisons. Middle ear modifications characteristic of each genus are qualitatively described. Quantitative comparisons are made among the 26 species in the study. Some correlations between middle ear size and other measurements are discussed. The middle ear is an acoustical transformer that for best efficiency must match the impedance of the cochlea to the impedance of the air in the external auditory meatus. It accomplishes this by a pressure increase and a velocity decrease through the combined effects of the lever and areal ratios; however, because the important consideration is a matching of two impedances rather than an absolute pressure increase, the pressure transformer ratio is a less informative measure of the middle ear's efficiency than is the impedance transform ratio. The impedance transformer mechanism is explained (from a morphological point of view), and equations are presented. Dipodomys, Microdipodops, and Perognathus have a theoretical transmission (at the resonant frequency) of 9 4 1 0 0 % of the incident acoustical energy; Liomys, 7880%. The areal ratio of stapes footplate to 2/3 tympanic membrane is remarkably constant among the species, varying only from 0.04 to 0.07: in Dipodomys and Microdipodops this small ratio is due to the very large tympanic membrane; in Perognathus and Liomys it is due to the extremely small stapes footplate. The lever ratio of incus to malleus varies from 0.28 to 0.33 in Dipodomys and Microdipodops, from 0.37 to 0.46 in Perognathus, and from 0.55 to 0.60 in Liomys. In addition, the middle ear volumes and the morphology of tympanic membrane, ossicles, ligaments, and muscles, all combine to minimize both mass and stiffness. All these data suggest middle ear mechanisms which are very efficient over a broad frequency range. The middle ear modifications found in heteromyids are adaptive in predator avoidance, especially in areas of little natural cover; nevertheless, contrary to expectations, there is no firm relationship between habitat and the extent of these modifications in the 26 species. However, environment did apparently play an important role in the evolution of the family, and this is discussed.

The great diversity of middle ear morphology in the rodent family Heteromyidae has been evident since the study by Howell ('32) which described the gross anatomy of the middle ear of Dipodomys spectabilis and briefly compared it with that of three other heteromyid genera, Microdipodops, Perognathus, and Liomys. The structural diversity has been subsequently studied (Pye and Hinchcliffe, '68; Webster, '68, '69; Hinchcliffe and Pye, '69), but only in Dipodomys merriami and D. spectabilis J. MORPH., 246: 343-376

has the middle ear been described in detail (Webster, '61). In these two species the middle ear cavity is so greatly enlarged, primarily by increase and cavitation of the antrum and epitympanum, that the combined volume of the two middle ear cavities is larger than that of the cranial cavity (Webster, '65). A s demonstrated by cochlear microphonic (Webster, '62) and behavioral studies (Webster and Webster, '71, '72),these enlarged middle ear cavities enhance the transmission of low-fre-

343

344

DOUGLAS B . WEBSTER A N D MOLLY WEBSTER

quency sounds and aid predator avoidance. A cochlear microphonic study comparing various species of Dipodomys, Microdipodops, and Perognathus (Webster and Strother, '72) indicates that these three genera are most sensitive to low frequencies; however, those with smaller middle ears (Perognathus) are not as sensitive as those with larger middle ears (Dipodomys and Microdipodops). A diverse literature, summarized and elegantly analyzed by Dallos ('73), establishes that the frequency spectrum an animal hears, and its relative sensitivity to different frequencies within that spectrum, are to a great extent determined by middle ear morphology. Several studies in recent years have been concerned with the diversity of mammalian middle ear structure. Lay ('72), studying gerbilline middle and inner ears, correlated the diverse morphology of enlarged middle ear cavities with their functional characteristics as demonstrated by cochlear microphonics. Other studies, primarily anatomical, have described diverse mammalian middle ear structure and have suggested functional correlates (Simkin, '65; Oaks, '67; Hooper, '68; Segall, '69a,b, '70, '73). In this study, middle ear diversity is examined in a closely related rodent family with a welldocumented fossil record (Wood, '35; Reeder, '57; Shotwell, '67). A paper in preparation examines cochlear diversity. A companion paper (Webster, '75) gives a detailed description of the postnatal development of the middle and inner ear of Dipodomys merriami. In the present paper, Dipodomys - the subject of much of our previous work and of experimental work in other laboratories is used as a standard of comparison for the other genera, and is therefore presented with more detail and interpretation than was done previously (Webster, '61). As will be seen, different types of modifications are found in the different genera of this family. The selective pressures which may have directed the evolution of these modifications are discussed. MATERIALS AND METHODS

This study is based on 515 heteromyid ears from the southwestern United States and from Panama, representing 26 species of 4 genera (the genus Heteromys has not

been studied). A complete list of species, numbers, localities, and dates of capture are available from the authors upon request. A list of the genera and species studied is included in table 1. The taxonomic keys and classification system of Hall and Kelson ('59) were used throughout the study. Intact dried skulls were prepared from 42 specimens. Naso-occipital lengths, the greatest length from the anteriormost end of the nasals to the posteriormost end of the occipital bone, were measured on these skulls and also taken from Hall and Kelson ('59). Gross dissections and descriptions were done on 348 ears, and measurements were made as follows. First the middle ear volumes were determined on isolated temporal bones by drying them in a low-temperature oven, sealing all openings with white water-soluble paste, and replacing the air of the middle ear cavity with alcoholic eosin injected from a 1- or 2-cc tuberculin syringe graduated to the nearest 0.01 cc; volume was determined as the total injected fluid volume. This procedure was monitored with a Zeiss dissecting microscope, looking through the translucent walls of the middle ear cavity. Tiny pinprick holes allowed air, but not fluid, to escape. Then the paste was peeled off and the temporal bones were dried and dissected; if all the inner surfaces were stained with eosin, it indicated that the entire cavity had been filled with the measuring fluid. Repeated measurements on single specimens yielded minimal variation. Using the Zeiss dissecting microscope with an eyepiece micrometer, the diameter of the tympanic membrane was determined by making two measurements (accurate to 0.05 mm) at right angles to one another and taking the average. Although the heteromyid tympanic membrane is approximately circular, in some species it is slightly elliptical; routinely averaging the two measurements accommodated deviations from the circle. For surface area determinations the tympanic membrane was treated as a circular, flat surface, since the depth of the umbo cannot be consistently determined after the drying procedure. This results in conservative, but internally consistent, surface area estimates. Still using the ocular micrometer and

345

HETEROMYID MIDDLE EARS

the Zeiss dissecting microscope, the axis of rotation and the lengths of the manubrial and incudal lever arms were determined. The axis of rotation is a straight line extending from the tip of the anterior process of the malleus through the posterior tip of the short process of the incus. From this line, a perpendicular is dropped to the distal end of the manubrium of the malleus to determine the malleolar lever arm, and a second perpendicular, from the axis of rotation to the center of the lenticular process, to determine the incudal lever arm. The stapes was then dissected out of the oval window and the surface area of its footplate was measured; again, i t was treated as a flat plane even though in Dipodomys and Microdipodops it has a convex surface toward the vestibule. Impedance transform ratios (Dallos, '73) were determined. The theory and significance of the impedance transform ratio will be dealt with at length in the DISCUSSION. Briefly, it gives a measure of the middle ear's idealized impedance matching ability, as the older formulation of pressure transformer ratio (Wever and Lawrence, '54) describes its pressure increase. For histological preparation of 125 ears, anesthetized animals were perfused with saline followed by kaformacet or formalin; the cochlea and immediately surrounding portion of the middle ear, or, in 24 cases, the entire middle and inner ear, were fixed

in kaformacet or formalin, washed, dehy-

drated, and embedded in parafin (Webster, '61, for details), or in low-viscosity nitrocellulose (method of Guild, '68). Sections were stained with Mallory trichrome stain, or, in a few cases, with hematoxylin and eosin. RESULTS

Dipodomys temporal bone The adult temporal bone of Dipodomys, formed from the fused periotic and ectotympanic elements plus a small contribution from the styloid (Webster, '75), shows no suture lines; histologically the circumferential lamellae-type bone is continuous. It is bordered by parietal, occipital, basisphenoid, and squamosal bones (fig. l). Associated with the hypertrophy of the middle ear cavity is the thin, compact bone, with minimal internal vascularization, that comprises the temporal bone complex of the adult. Only along the borders where the cochlea is adjacent to or fused with the ectotympanic element are there tiny bits of osteon bone. The middle ear cavity is divided into three interconnecting parts (fig. 2). Ventrally there is the hypotympanum, bordered laterally by the tympanic membrane and extending anteriorly and medially to within 1 mm of the midline where the small Eustachian tube, normally closed, leads into the nasopharynx. Just posterior to where the cochlea bulges into the roof of

~-

Abbreviations A , antrum AE, lamina separating antrum and epitympanum As(f), anseriform fossa AL, annular ligament Bo, bone C, cochlea CCn, cochlear canaliculus Ce(0 cerebral fossa CT, chorda tympani nerve Ec, ectotympanic Ep, epitympanic F, facial nerve Fc, facial nerve canal Fr, frontal bone H, hypotympanum I, incus IAM, internal auditory meatus Ip, interparietal bone M, malleus M(m), manubrium of malleus ME, middle ear cavity Ms, smooth muscle

P, periotic Pa, parietal bone Pf(fl, parafloccular fossa S, stapes S(c), crura of stapes S(0, footplate of stapes SA, stapedial artery SA(b), bony spicule in area usually occupied by stapedial artery SA(f), foramen for stapedial artery SCh, horizontal semicircular canal SCha, ampulla of horizontal semicircular canal SCs, superior semicircular canal S G ( 0 , foramen for semilunar ganglion So, supraoccipital bone Sq, squamosal bone STP, sulcus for stapedial artery, tensor tympani, and greater superficial petrosal nerve TB, temporal bone TM, tympanic membrane Tt, tentorium V, vestibule VA, vestibular aqueduct opening

34 6


Fig. 1 Dorsal view of the skull of Dipodomys merriami with the left middle ear cavity dissected open. X 2.68.

~

~

~

Fig. 2 Ventrolateral vlew of Isolated left temporal bone of m p o d o m y s m e r n a m i , dissected to show the internal anatomy of the middle ear cavity. X 2.48.

the hypotympanum a foramen opens into the antral chamber. This chamber extends to the dorsal aspect of the skull and is enclosed by the posterior portion of the periotic bone. Dorsally the hypotympanum

communicates with the epitympanic chamber, which bulges dorsally and laterally to the surfaces of the skull and anteriorly into the orbit (fig. 1). The epitympanic and antral chambers, separated by an extremely thin bony lamina, extend laterally well past the tympanic membrane and form most of the roof and walls of the osseous external auditory meatus; their size makes this the widest part of the skull. A shallow sulcus on the dorsolateral surface of the periotic region indicates the position of the lamina separating epitympanic and antral chambers; it extends from the point of articulation with the supraoccipital bone dorsally, to the level of the opening of the external auditory meatus laterally (fig. 1). A deeper longitudinal sulcus on the lateral surface of the epitympanic chamber wall houses the thin suprameatal spine of the squamosal bone; it extends from the orbit to the superior margin of the opening of the external auditory meatus. The ectotympanic is overlapped laterally and anteriorly by a ventral extension of the epitympanic cham-

347


ber, and posteriorly and ventrally by two extensions of the antral chamber. The larger, posterior extension, which corresponds in position to the mastoid process of most mammals, is separated from the more dorsal portion of the antral chamber by a sulcus. Just anteriorly is the styloid process, a small ridge of bone, extending onto the ventral ectotympanic wall from just below and behind the external auditory meatus; in juvenile skulls it is solid, but in adults it is hollow and continuous with the antral chamber. On the ventral aspect of the ectotympanic, a line, arcing medially, marks the tympanic annulus. On the medial surface of the ectotympanic, adjacent to the posterior lacerate foramen, is the stapedial foramen through which the stapedial artery enters the middle ear cavity. A simple dissection removing the outer walls of the epitympanic, antral, and hypotympanic chambers reveals the deeper walls of the middle ear cavity; it can be seen that part of the hypertrophy of the cavity is caused by erosion of bone on the medial, deep surface of the cavity, which leaves extremely thin bone covering the skull and inner ear. The cochlea, which bulges prominently into the hypotympanic chamber roof, is enclosed in bone so thin that the underlying spiral ligament of each turn can be clearly seen. As the stapedial artery courses through the middle ear it is covered by a thin bony shell, The medial portion of this shell, which crosses the hypotympanic roof to the basal turn of the cochlea, is derived from the ectotympanic; the portion that passes through the crura of the stapes is formed by the periotic (fig. 4); the portion just anterior to the stapes is formed by fusion of the ectotympanic and the cochlear portion of the periotic. This anterior part of the canal also carries the greater superficial petrosal nerve (a branch of the facial), and, from the level of the cochleariform process anteriorly, the tensor tympani muscle. All three - stapedial artery, tensor tympani muscle, and greater superficial petrosal nerve - leave the middle ear in this canal, which then becomes a sulcus on the dorsal surface of the ectotympanic adjacent to the middle lacerate foramen. The facial nerve enters in the dorsal

Fig. 3 Medial view of isolated right temporal bone of D ipodomy s me r r inmi. X 2.48.

SA

Fig. 4 The stapedial artery of D i p o d o m y s agilis as it passes through the obturator foramen of the stapes. Note that the muscular walls are gone and the artery is lined only by endothelium and bone. Mallory stain. X 34.72.

anterior portion of the internal auditory meatus (fig. 3 ) and courses with the superior portion of the vestibular nerve. Where the latter leaves to innervate the superior and horizontal semicircular canals, the facial nerve enters its own bony canal; it runs just dorsal to the stapedial artery canal and ventral to the ampulla and proximal portion of the horizontal semicircular canal, passes between the horizontal semicircular canal and the stapes, and then courses ventrolaterally, adjacent to the posterior wall of the external auditory meatus. Finally the facial nerve leaves the middle ear cavity through

348

DOUGLAS B. WEBSTER AND MOLLY WEBSTER

the stylomastoid foramen, adjacent to the tip of the styloid process. The geniculate ganglion lies in the bony facial canal at the point where the greater superficial petrosal nerve originates, just anterior to the stapes and adjacent to the ampullae of superior and horizontal semicircular canals. Slightly distal to the geniculate ganglion, as the facial nerve passes the middle portion of the horizontal semicircular canal, a small nerve branches off and immediately innervates the stapedius muscle. The tiny chorda tympani nerve does not split off from the facial nerve until it is already past the level of the tympanic membrane; then it travels back within the facial canal and enters the middle ear cavity through the tiny posterior iter of the chorda tympani, just medial to the ectotympanic lamina which fills the notch of Rivinus (tympanic incisure). The chorda tympani then passes anteriorly just lateral to the base of the long process of the incus until it reaches the posterior face of the lamina of the manubrium. It travels down the posterior face of the lamina to the muscular process, makes a 180" turn around the tendon of the tensor tympani muscle, and passes up the anterior face of the lamina of the manubrium. When it reaches the neck of the malleus i t turns anteriorly again, pierces through the anterior process, and passes out of the middle ear through a tiny, tortuous canal, the iter chordae anterior. The medial wall of the antral chamber is formed completely by the periotic bone. A prominent dorsal convexity reflects the shape of the anseriform lobe of the cerebellum (fig. 3). Just ventral to the anseriform convexity and dorsal to the continuity between hypotympanum and antrum is an even more prominent convexity covering the paraflocculus; superimposed around it are the three semicircular canals. Lying deep in the groove between these two bulges is the posterior portion of the superior semicircular canal. The posterior semicircular canal extends from the posterior junction of the parafloccular and anseriform bulges, arcs out into the antral chamber, and arcs back ventrally toward the vestibule. Ventrally and anteriorly, the horizontal semicircular canal extends laterally well into the antrum and then disappears

into the lamina separating antral and epitympanic chambers. The anterior part of the medial wall of the epitympanic chamber covers the posterior part of the cerebral hemisphere (fig. 2), and thus abuts against the middle cranial fossa. The posterior part of the medial wall contains the anterior part of the convexity for the anseriform lobe, and a bit of the anterior wall of the parafloccular convexity, and thus borders the posterior cranial fossa. The entire posterior wall of the epitympanic chamber is lined by the septum separating i t from the antral chamber (fig. 2). The anterior semicircular canal passes anteriorly from this septum and then curves ventrally, enlarging at its ampulla and entering the vestibule (fig. 2). Somewhat deeper in the epitympanic recess is the ampulla of the horizontal semicircular canal (fig. 2). Ventrally, the epitympanic chamber communicates through a broad orifice with the lateral part of the hypotympanum; the head of the malleus and the body of the incus are located in this orifice (fig. 2). The lateral floor of the epitympanic chamber is formed posteriorly by the roof of the external auditory meatus, but more anteriorly by its own anterior ventral expansion in front of the meatus. In this expansion, and also in the dorsal part of the chamber, are several fine, thin, bony struts providing mechanical strength. From the medial aspect of the temporal bone the thin, bony tentorium extends medially between cerebrum and cerebellum (fig. 3 ) , with the semilunar ganglion and trigeminal nerve occupying a large opening in its ventromedial portion. Just lateral to this opening, on the dorsal surface of the ectotympanic, is a small portion of the thin cochlear wall. Dorsomedially behind the tentorium lies the internal auditory meatus; through its anterior opening pass the facial nerve and superior division of the vestibular ramus of the eighth cranial nerve, and through its posterior opening, the cochlear ramus and the inferior division of the vestibular ramus of the eighth cranial nerve (fig. 3). Immediately posterior to the internal auditory meatus is the tiny opening of the cochlear aqueduct, the cochlear canaliculus, and dorsolateral to the meatus, the deep subarcuate or parafloccular fossa. Just posterior to


this fossa is the narrow, slit-like opening for the vestibular aqueduct, which houses the endolymphatic sac. Dorsal to the parafloccular fossa is the broad, shallower fossa for the anseriform lobe. Anterior to the tentorium the medial surface of the temporal bone is relatively smooth, as is the overlying occipital portion of the cerebral hemisphere; on its surface lies the deep sulcus, already described, for the greater superficial petrosal nerve, stapedial artery, and tensor tympani muscle.

349

ear surfaces of the joint, and much less densely packed between them (fig. 5). Some of the fibers of the tiny stapedius muscle take origin from the bony wall of the horizontal semicircular canal, and others from the bony wall of the facial canal; the tendon of the stapedius inserts onto the tenuous posterior neck of the stapes. In the obturator foramen and for about a half millimeter on either side the muscular wall of the stapedial artery is entirely lost (fig. 4); there is only the bony canal and the artery's endothelial wall, Dipodomys auditory ossicles which is here tightly adherent to the bone. The morphology of the auditory ossicles The only suspensory ligaments of the ossiof Dipodomys sp. has already been thor- cles are the posterior ligament of the incus oughly described (Ryder, 1878; Cockerel1 and the anterior ligament of the malleus; et al., '14; Howell, '32; Webster, 'Sl), and through them runs the axis of rotation. is reviewed here only for comparison with Microdipodops the other heteromyid genera. The malleus The temporal bone and middle ear cavihas a broad head, almost no neck, and a spine-like anterior process from which a ties of Microdipodops are remarkably simithin lamina is continuous with the head lar to those of Dipodomys, the primary of the malleus. The process becomes ex- difference being that in Microdipodops tremely thinned (to about 9 pm) and is there is even more inflation relative to continuous with the anterior limb of the body size (figs. 6, 7, 8). This additional tympanic annulus. Ligamentous fibers run inflation occurs primarily in the periotic on each side of the spine. The manubrium portion of the temporal bone complex, and is slightly widened at its tip and flattened is slightly greater in the antrum than in along its lateral surface; it is completely the epitympanum. The epitympanum exembedded in the tympanic membrane from tends anteriorly well in front of the manit process brevis at the dorsal edge of the dibular fossa, overlapping this fossa on membrane to its tip at the umbo. A thin its lateral aspect; it extends ventrally in bony lamina extends medially from the front of the walls of the external auditory manubrium and, about half way between meatus, forming the anterior wall and process brevis and tip, gives rise to a part of the floor of the meatus. The ansmall muscular process on which the tensor tral chamber extends posteriorly far betympani attaches. Between the malleus yond the foramen magnum (fig. 6). Venand the incus is a complex articulating trolaterally it sends an especially large joint: the incus overlaps the malleus dorso- extension posterior to the bony external laterally and the malleus overlaps the incus ventrolaterally, while on the medial side there are the opposite relationships. The body and short process of the incus are stout; the articulating long process is extremely short, with the usual right angle turn at its distal end and then the expansion to the lenticular process. The stapes is extremely fragile; its crura are rod-like (fig. 4), but its footplate is hollowed out, with a convex surface bulging into the vestibule. The annular ligament is composed of very fine fibers between the wall of the oval window and the rim of the footplate. These fibers are densely Fig. 5 The annular ligament of the stapes of packed along the vestibular and middle D i p o d o m y s deserti. Mallory stain. x 155.

350

DOUGLAS B . WEBSTER AND MOLLY WEBSTER

Fig. 6 Dorsal view of the skull of Microdipodops pullidus with the left middle ear cavity dissected open. x 3.02.

Fig. 7 Ventrolateral view of isolated left temporal bone of Microdipodops megacephal us dissected to show internal anatomy of the middle ear cavity. X 3.35.

auditory meatus which forms part of its posterior floor. This ventral extension of the antral chamber is confluent with the hollowed-out styloid process, and together

Fig. 8 Medial view of isolated right temporal bone of Microdipodops me gac e phalus . X 3.35.

they form the very large tongue of the antrum on the ventral surface of the bulla (fig. 7). The suprameatal spine of the squamosal bone runs in a groove on the anterior border of the epitympanic chamber wall. It extends caudally almost, but


35 1

not quite, to the superior border of the unicrurate stapes (Pye and Hinchcliffe, orifice of the external auditory meatus. '68) is in error. Both tensor tympani and stapedius mus(In D i p o d o m y s the spine does reach this cles are present, and although they are border.) The Microdipodops malleus and incus less prominent in Microdipodops than in and their ligaments are similar to those in D i p o d o m y s they have similar origins and Dipodomys. The malleus has a slightly courses. The stapedial artery takes the longer and more prominent neck, and same route through the middle ear (fig. 7). therefore a somewhat longer lamina be- Its bony canal is lost in the obturator tween the anterior spine of the anterior foramen (fig. 9), and its walls are made process and the head of the malleus. The up of collagenous fibers lined by an exmalleoincudal joint is the same. The incus tremely thin endothelium with no smooth is similar, except that the long process is muscle. The routes of the facial nerve and its shorter and, instead of running parallel to the manubrium, is at an angle of about branches are also similar; the major dif45" with the malleus and so extends fur- ferences involve the relative sizes and anther caudally (fig. 7). The extremely fragile gles of components in the peripheral porstapes has much longer crura, associated tion, between the stylomastoid foramen with the greater relative inflation of the and the area just ventral to the horizontal middle ear cavity and the consequent semicircular canal. The route is almost greater distance between the lenticular vertical in Microdipodops, due to the process and the oval window. The stape- greater expansion of the antral chamber dial footplate and the annular ligament on whose border it must course. The bony are similar to those of D i p o d o m y s (fig. lo). facial nerve canal is incomplete where it The suggestion that Microdipodops has a lies adjacent to the stapedius muscle; a twig of the facial nerve branches off at this point to innervate the stapedius.

Fig. 9 The stapedial artery of M i c r o d i p o d o p s megacephalus as it passes through the obturator foramen of the stapes. Mallory stain, x 34.72.

Fig. 10 The annular ligament of the stapes of M i c r o d i p o d o p s p a l l i d u s . Mallory stain, x 155.

Perognathus The temporal bone of pocket mice, like those of kangaroo rats and kangaroo mice, is a complex formed by ectotympanic, periotic, and styloid elements and enclosing a middle ear space divided into a ventral hypotympanum, an anterior dorsal epitympanum, and a posterior dorsal antrum. In Perognathus, however, the temporal bone is less extensive (fig. 11). Ventromedially the two ectotympanic elements approach one another near the midline but do not meet. Posteriorly the antral wall either does not extend to the most posterior part of the skull or just barely does so. Similarly, neither antrum nor epitympanum extends to the dorsal surface of the skull, although each approaches it. Anteriorly the epitympanum barely reaches but does not impinge upon the back part of the orbit. The epitympanum does not extend in front of or ventral to the level of the external auditory meatus, and the entire anterior wall of the meatus is formed by the ectotympanic element (fig. 12). Consequently the adjacent squamosal, parietal, interparietal, and occipital bones are considerably larger in Perognathus, relative to skull size, than they are in

352


Fig. 11 Dorsal view of the skull of Perogntcthus ( P e m g n a t h u s ) f o r n o s u s with the left middle ear cavity dissected open. X 3.06.

Microdipodops or Dipodomys (fig. 11). The suprameatal spine of the squamosal is quite large and extends over the entire superior border of the external auditory meatus opening. The extremely short styloid process does not reach the inferior border of the meatal opening; therefore the stylomastoid foramen opens just posterior - rather than ventral - to the external meatus. On the external surface of the bulla there is no indication of the lamina separating epitympanum and antrum; a groove located more posteriorly is not related to the lamina but accommodates a branch of the cervical trunk vascularizing the external walls of antrum and epitympanum. Ventral to this a deep sulcus marks the juncture of the ectotympanic element and the antral portion of the periotic element; however, the bone is continuous and there is no suture line. All of the middle ear walls are of quite thick bone: the outer layer, next to the dermis and muscles, is of circumferential compact bone; the deep layer is of pneumatized trabecular-like bone, with a meshwork of almost microscopic air spaces con-

tinuous with and part of the middle ear cavity (figs. 11, 12). These trabeculae have essentially no vascularization; they are fine enough to be easily scraped away with a pair of delicate forceps in a fresh specimen or living animal. They are covered by mucous membrane continuous with that of the middle ear cavity, composed of thin squamous epithelium underlaid by a fine connective tissue layer. Such trabeculation surrounds hypotympanum, antrum, and epitympanum, making their enclosed areas considerably smaller than a superficial view of the temporal bone would indicate. This is particularly so in the epitympanum, which is little more than large enough to accommodate the head of the malleus and the body and short process of the incus (fig. 12). The epitympanum is continuous ventrally with the small hypotympanum which, posterior to the cochlea, is in turn continuous dorsally with the antrum. The antral space does expand considerably in the areas of posterior and horizon t a1 semicircular canals , but even there the bullar walls are of thick trabeculated bone. The only bone in the middle


ear cavity which is compact rather than heavy and trabeculated is that forming the canals for the stapedial artery and facial nerve, and the cochlear walls that are exposed in the hypotympanum. The ectotympanic, where it has grown dorsally, overlaps the lateral, medial, and apical surfaces of the cochlea; a suture line is

Fig. 12 Ventrolateral view of isolated left temporal bone of P e r o g n a t h u s ( P e r o g n a t h u s ) formos u s , dissected to show the internal anatomy of the middle ear cavity. X 4.03.

Fig. 13 Medial view of isolated right temporal bone o f P e r o g n a t h u s ( C h a e t o d i p u s ) p e n i c i l l a t u s . X 4.216.

353

present even in the adult, for this is the one area where periotic and ectotympanic elements do not fuse in Perognathus. The stapedial artery enters from the medial side of the ectotympanic and courses across in its bony canal to the base of the cochlea, as in Dipodomys and Microdipodops (fig. 12). The bony canal is interrupted as the stapedial artery passes between the crura; it recommences on the other side of the stapes, and turns anteriorly between the cochlear portion of the periotic and the adjoining ectotympanic. There it is joined by the tensor tympani muscle and its tendon, and by the greater superficial petrosal nerve; together they leave the middle ear cavity in this canal. On the medial surface of the periotic there is an extremely shallow subarcuate (or parafloccular) fossa, for the paraflocculus is very small in Perognathus (fig. 13). The other general features and relationships of the periotic of Perognathus are similar to those of the other two genera. The head of the malleus is less elongated in Perognathus than in Dipodomys and Microdipodops. The base of the anterior process is of extremely thin, transparent bone, and only its distal portion has a thickened spine. The neck and manubrium, including its lamina, are similar to those of Dipodomys. Compared to Dipodomys and Microdipodops, the long process of the incus is more nearly parallel with the manubrium; it is also much longer, relative to the rest of the incus and relative to the other two ossicles (fig. 12). The tensor tympani muscle attaches to the muscular process on the lamina of the manubrium; its course and morphology are similar to those described for the other two genera. The chorda tympani nerve makes a 180" turn around the muscular process of the malleus (fig. 16), as in Dipodomys and Microdipodops. The stapes is an extremely delicate bone; even its head, where it articulates with the lenticular process, is extremely fine and hollowed out toward the obturator foramen. The crura, instead of being rod-shaped in cross-section, are concave on the surfaces that face the obturator foramen; in cross-section they surround the stapedial artery like a pair of parentheses (figs. 14, 15). The footplate of the stapes is similarly fine and delicate. In most species it is

354


Fig. 14 The stapedial artery of Perognathus (Chaetodipus) penicillatus as it passes through the obturator foramen of the stapes. H E stain, X 3.472.

Fig. 16 Section showing the 180”-turn made by the chorda tympani nerve as it passes around the muscular process of the manubrium of the malleus; in this case in Perognathus (Chaetodipus) californicus. Mallory stain, X 50.22.

Fig. 15 The thin-walled stapedial artery of Perognuthus (Perognathus) longimembris as it passes through the obturator foramen of the stapes. Mallory stain, x 3.472.

Fig. 17 The very tenuous annular ligament of the stapes of Perognathus (Perognathus) longir n m b r i s . Mallory stain, X 155.

flat, but in some it is very slightly bullate, with its convex surface toward the vestibule. The extremely fine annular ligament is limited to sparse connective tissue fibers only on the tympanic side of the stapedo-vestibular joint (fig. 17). There is no stapedius muscle in the adult; in one of the more than 300 Perognathus ears a dried specimen of P . penicillatus examined grossly- there was a tiny tendon, but no sign of a muscle. The facial nerve and its branches have very similar routes in Perognathus and the other two genera, except that its more lateral portions remain horizontal rather than dipping into an almost vertical plane as occurs in more inflated middle ears. As previously mentioned, the stylomastoid foramen opens just behind, not ventral to, the opening of the external auditory meatus.

The genus Perognathus is divided into two subgenera (Hall and Kelson, ’59): Perognathus (smooth-haired pocket mice) and Chaetodipus (coarse-haired pocket mice). The intrageneric variation in the temporal bones of the group, greater than that in Dipodomys or Microdipodops, sorts itself out into two “pools” of characteristics which coincide, with minor exceptions, with this taxonomic distinction. In all species of the subgenus Chuetodip u s the entire temporal bone tends to be smaller and less prominent; the ectotympanics remain wider apart at the midventral line; the walls of the antral chamber do not protrude to the caudal edge of the skull; the epitympanic chamber walls are extremely small; the trabeculation impinges deeper into the hypotympanum, antrum, and epitympanum. However, the trabeculae are coarser and the air cells


Fig. 18 The fine bony trabeculae and a x cells of the walls of the middle ear cavity of Perognccthus (Perognathus)f l u v u s . Mallory stam, X 34.72.

Fig. 1 9 The coarser bony trabeculae and larger air cells of the walls of the middle ear cavity of

Peroynuthus ( C h a e t o d i p u s ) penicillatus. Mallory stain, X 34.72.

they enclose somewhat larger in Chaetod i p u s (figs. 18, 19). The stapedial artery of Chaetodipus has an extremely thick smooth muscle wall between its entrance from the medial surface of the ectotympanic and the obturator foramen. Just before it penetrates the obturator foramen, these muscular walls become extremely thin, and the bony walls of the stapedial artery canal thicken and end. Once past the obturator foramen the muscular walls remain relatively thin as the stapedial artery turns anteriorly and leaves the middle ear cavity (fig. 14). In the subgenus Perognathus the walls of the stapedial artery are relatively thin throughout; as in Chaetodipus, there is no bony covering in the obturator foramen (fig. 15). L i o my s The temporal bone of L i o m y s - like

355

those of D i p o d o m y s , Microdipodops, and Perognathus - is a complex made up of ectotympanic, periotic, and styloid elements, but in L w m y s i t is quite small relative to skull size and does not impinge nearly as much upon the adjacent squamosal, parietal, interparietal, occipital, and basisphenoid bones (fig. 20). Dorsal to the external auditory meatus the lateral wall of the skull is composed entirely of the squamosal bone, which articulates with the temporal bone at the level of the meatal opening. Extending along the lateral caudal surface of the external auditory meatus is the suprameatal spine of the squamosal, a thin flange of bone. More dorsally another thin flange of the squamosal extends caudally and overlaps the dorsal portion of the walls of the antral region (which does not form a true chamber in this genus). Because the squamosal is large and the temporal bone relatively small, the temporal bone nowhere directly articulates with the parietal. On the caudal surface of the skull is the extremely broad supraoccipital; at its lateral extent it articulates with the caudal aspect of that portion of the periotic which forms the walls of the antral region. The large paroccipital process of the exoccipital portion of the occipital overlaps the antrum. The lateral wall of the basioccipital articulates with the medial wall of the ectotympanic. The walls of the hypotympanum are formed similarly to those of the other three genera already described. The ectotympanic, which does not extend as far medially as in the other genera, articulates with the lateral surface of the exoccipital and posterior portion of the basisphenoid, leaving a space of fully 2 mm on the ventral surface between the two ectotympanic elements. Laterally, a relatively large, funnel-shaped portion of the ectotympanic forms the entire osseous part of the walls of the external auditory meatus. The annulus, supporting the tympanic membrane, can be seen only as a very fine arc along the ventral surface of the bulla. The annulus terminates in the region of the notch of Rivinus; however, as in the other heteromyids, a thin lamina of bone continues from i t to cover the area where one would expect the pars flaccida, thus forming an osseous lateral wall

356


~~~

~~

Fig 20 Dorsal view of the skull of L i o m y s zrro7ntus T h e temporal bone is barely visible from this view. X 2 54.

of the epitympanic recess. The cochlea, whose walls are formed from the periotic, bulges into the roof of the hypotympanum, formed otherwise by the ectotympanic. In the anterior hypotympanum, along the cochlea, the ectotympanic overlaps the periotic and forms a fine connective tissue suture; caudally, however, in the part of the periotic containing the vestibular portion of the inner ear, the ectotympanic and periotic fuse without sutures. The epitympanum is just large enough to house the head of the malleus and the body and short process of the incus (fig. 21). Ventrally it is continuous with the hypotympanum. Its walls are of a thin layer of dense bone, with the lateral wall formed by the ectotympanic and the other walls by the periotic element. Neither the epitympanum nor the hypotympanum contains trabeculation. Posteriorly the hypotympanum is continuous with the antrum, which is the largest portion of the Liomys middle ear; however, instead of being a true chamber, the antrum is composed of trabeculated bone lined with fine connective tissue and mucous membrane. Its trabeculation is coarser than that in Pero-

Fig. 21 Ventrolateral view of isolated left temporal bone of Liomys irroratus, dissected to show the internal anatomy of the middle ear cavity. X 4.402.

gnathus, with larger bony spicules and larger contained air chambers. The antrum is continuous only with the hypotympanum, and not with the epitympanic


357

Fig. 2 3 Stapes in the oval window of Liomys adserpsus. Mallory stain. x 34.72.

~~

~

Fig. 22 Medial view of isolated left temporal bone of Lzomys irrorntus X 4.402.

recess. The Liomys parafiocculus is very small, and there is no parafloccular fossa on the medial surface of the temporal bone; nor is there a bony tentorium separating posterior and middle cranial fossae (fig. 22). The stylomastoid foramen lies on the it is closer to the deeD medial end than x 155. to the superficial laterh end of the meatus. It is positioned at the junction of the arc-shaped crura, and a thin, flat footplate ventral part of the antral chamber, the (fig. 23). The annular ligament is extremeposterior medial portion of the external ly delicate, consisting of fine fibers sparsely auditory meatus wall, and the most lateral arranged along the middle-ear side of the portion of the hypotympanic wall. A deli- stapedo-vestibular articulation, similar ficate styloid process is present. bers along the vestibular border, and no With a few exceptions the auditory ossi- fibers in the space between (fig. 24). This cles of Liomys are very similar to those of articulation has the appearance of a fine Perognathus. The process for the tensor synovial joint, similar to that of Perognatympani muscle lies on the neck of the thus; it is less delicate, however, since in malleus rather than on its manubrium. Perognathus there are no fibers along the A s in Perognathus the tensor tympani mus- vestibular edge of the joint. In neither cle itself lies on the dorsolateral surface Liomys nor Perognathus is there a staof the cochlea in the canal between ec- pedius muscle. The adult Liomys, alone totympanic and periotic; and its tendon among the heteromyids studied, also lacks comes out through the cochleariform proc- a stapedial artery. There is a thin, rodess to insert onto the muscular process shaped bone (fig. 23) following the usual of the malleus. The long process of the route of the stapedial artery (from the incus is even longer in L w m y s than in medial surface of the hypotympanum along Perognathus, relative to other structures. its dorsal roof, over the basal turn of the The delicate stapes has almost no neck cochlea, and through the crura); this is region but is otherwise much like that of probably the remnant of the stapedial arPerognathus, with a hollowed-out head tery canal, which is present during developopening toward the obturator foramen, ment in all mammals where this has been

358


studied. The course of the facial nerve is similar to that in Perognathus; it is almost perfectly horizontal from the point where it enters the internal auditory meatus to where it exits through the stylomastoid foramen, with no vertical component.

Quantitative aspects While qualitative differences in temporal bone morphology distinguish the heteromyid genera, there are other, quantitative differences between species. A s described in MATERIALS A N D METHODS, therefore, middle ear volume, malleus and incus lever lengths, and tympanic membrane and stapedial footplate diameters

were measured in representatives of each species (table 1). In order to compare the middle ear with linear measurements, the cube root of its volume was determined. Because of the wide range of body sizes (7-8 grams for small Perognathus, to 120 f grams for large Dipodomys), it was desirable, for some calculations, to consider not the absolute size of the middle ear but its relative inflation. A skull measurement was preferable to body length or body mass as a conservative measure, because of the different body types (e.g., short and squat in Microdipodops, elongated in Liomys) and differences related to health and age. One of the few skull measurements not directly

TABLE 1

M i d d l e ear m e a s u r e m e n t s i n Heteromyidue Stapes footplate No. of ears

Species

Dipodomys agilis deserti merriami m i c r op s ordii panamintinus spectabilis stephensi

-

Rel. MEVl

TMD 1 (mm)

Length (mm)

Width (mm)

Malleus (mm)

Incus (mm)

12 14 25 14 12 18 20 16

0.51 1.41 0.47 0.52 0.53 0.43 1.00 0.60 0.68

0.25 0.27 0.29 0.29 0.25 0.23 0.28 0.26 0.27

5.41 7.10 5.23 5.49 5.30 5.24 6.34 5.53 5.69

1.42 1.80 1.33 1.41 1.45 1.41 1.65 1.43 1.48

0.79 0.98 0.72 0.79 0.81 0.75 0.87 0.80 0.81

3.16 3.85 2.93 3.07 3.09 3.02 3.61 3.12 3.22

0.91 1.21 0.86 0.94 1.03 0.95 1.08 0.92 0.98

24 16

0.31 0.38 0.34

0.31 0.31 0.31

5.07 5.09 5.08

1.33 1.31 1.32

0.74 0.69 0.72

2.61 2.64 2.62

0.74 0.73 0.74

6 2 20 8 16 2 8 26 4 21 4 10 18 2

0.06 0.09 0.11 0.05 0.05 0.05 0.07 0.06 0.04 0.05 0.06 0.07 0.04 0.03 0.06

0.20 0.23 0.18 0.15 0.15 0.21 0.24 0.17 0.16 0.19 0.22 0.18 0.15 0.13

3.59 3.30 3.56 2.80 2.76 2.77 3.01 3.15 2.67 2.95 2.81 3.08 2.77 2.58 3.04

0.73 0.73 0.79 0.69 0.66 0.70 0.74 0.71 0.60 0.69 0.64 0.72 0.64 0.58 0.70

0.44 0.43 0.42 0.35 0.34 0.39 0.44 0.38 0.35 0.37 0.35 0.41 0.33 0.32 0.38

2.02 1.78 1.96 1.58 1.63 1.68 1.73 1.76 1.45 1.62 1.65 1.79 1.55 1.40 1.71

0.78 0.85 0.73 0.73 0.63 0.67 0.76 0.64 0.66 0.61 0.73 0.67 0.62 0.73

2.62 2.57 2.60

0.67 0.61 0.65

0.40 0.39 0.40

1.50 1.46 1.48

0.83 0.88 0.85

X

Microdipodops m e ga c e p h a l us p a l l i du s

-

X

Perognathus amplus arenariu s baileyi californicus fallm flavesc e n s flavus formosus intemedius l o n g i me mbr i s merriami parvus pe n c i l l at us s p i na t us X

Liomys ad s e r p s u s irroratus

X

Lever arms

MEVl (cm3)

6 4

0.03 0.03 0.03

__-

0.18

0.10 0.11 0.10

0.82

MEV, middle ear volume; Rel. MEV, relative middle ear volume; TMD, tympanic membrane diameter. I

359


affected by middle ear inflation is naso- length and cube root of middle ear voloccipital length. Therefore, to determine ume: within genera the smaller the animal, relative middle ear volume, the cube root the larger the middle ear volume. These of the middle ear volume was divided by different relationships suggest two major, naso-occipital length. divergent lines of evolution within the f a In absolute terms the smallest middle ily H eteromyid ae. ears (0.03 cm3) are found in the two speThere is a close fit between the size of cies of Liomys ( L . adserpsus and L. irrora- the middle ear cavity and the diameter t u s ) and in Perognathus spinatus; the of the tympanic membrane (fig. 26), showlargest is in Dipodomys deserti (1.41 cm3). ing that evolution of middle ear inflation In terms of relative volume the smallest within these four genera was accompanied middle ears are in L w m y s and the largest by a similar enlargement of the tympanic in the two species of Microdipodops. Plot- membrane. There is also a close fit beting each species by naso-occipital length tween relative middle ear size and lever and cube root of middle ear volume gives arm ratio (fig. 27): this is a positive coralmost a scatter graph with little relation- relation if the ratio is expressed as malship between the values (fig. 25a). How- leuslincus, or negative if, as here, it is ever, further analysis reveals two popula- expressed as incudmalleus. The change tions among these four genera (fig. 25b). in lever ratio with increased inflation of In the ten species of Microdipodops and the middle ear is due partly to the inDipodomys, the genera with the largest crease in malleolar lever arm length that relative and absolute volumes and with- necessarily accompanies an increase in out trabeculation, there is a positive cor- tympanic membrane diameter, and partly relation between naso-occipital length and to a concomitant reduction of incudal lever cube root of middle ear volume; within arm length in animals with larger middle genera the larger the animal, the larger ear cavities. This reduction in incudal levthe relative middle ear volume. In L w m y s er arm length is effected by two factors: and Perognathus, the two genera with the long process of the incus is relatively trabeculated middle ears, there is a nega- shorter in Dipodomys and Microdipodops tive correlation between naso-occipital than it is in Perognathus and Liomys;

L

\

//

P

PP

y = 19 58x

+

P P

14.16

\

y = 3 8 . 8 1 ~+ 1-1.611 P and L. y = (-24 581x t 31.65

1 ,IL

0

a

o

P

8

Cube Root of Middle Ear Volume (mml

8

12

b

12

Cube Root of Middle Ear Volume (mm)

Fig. 25 Two interpretations of the relationship of middle ear volume to naso-occipital length. D, D i p o d o m y s ; L, L i o m y s ; M , Micsodipodops; P, Perognathus.


y

4

=

5 . 5 1 5 ~+ .19

8

12

Cube Root of Middle Ear Volume l m m )

Fig. 2 6

Relationship of tympanic membrane

to middle ear volume in 26 species of Heteromyi-

dae. D , Dipodomys; L, Liomys; M, Microdipodops; P, Perognathus.

\

moreover its angle of inclination relative to the axis of rotation is smaller in Dipodomys and Microdipodops than in the other two genera, which further reduces its effective length. The areal ratio is also correlated with relative inflation - negatively if the ratio is expressed as 2/3 tympanic membrane to stapes, or positively if, as here, it is expressed as stapes to 2/3 tympanic membrane. However, this relationship is a weak one (fig. 28a), although Microdipodops and Dipodomys cluster with high areal ratios and high relative infiation, and Perognathus tends to cluster with small areal ratios and less relative inflation; Liomys has an areal ratio like that of Dipodomys but less relative inflation than any Perognathus. If one again analyzes the four genera in two separate groups (fig. 28b), one finds two general negative correlations: one in Microdipodops-Dipodomys, and another (much weaker) in Perognathus-Liomys. We have also attempted to organize these species from the standpoint of their environment. Table 2 gives the relative middle ear inflation for each species studied, and a capsule notation (from Burt, '64) of the general habitat in which it is found. As the table indicates, there is no consistent relationship throughout the family between the environmental features considered here and middle ear volume. The problem of correlations between middle ear morphology and habitat is explored in the DISCUSSION. DISCUSSION

\

\ .1

.2

3

Relative Middle Ear Volume

Fig. 27 Relationship of lever arm ratio to relative middle ear volume in 26 species of Heteromyidae. D , D i p o d o m y s ; L, Liomys; M, Microdipodops; P, Perognathus.

General functional considerations Most recent anatomical studies of the mammalian middle ear have utilized the pressure transformer ratio (Wever and Lawrence, '54) as an index of middle ear efficiency. The formulation is the product of the lever ratio (manubrium lever arm/ incudal lever arm) and the areal ratio (2/3 area of tympanic membranelarea of stapedial footplate); it accurately represents the maximum pressure increase at the stapes relative to the tympanic membrane. In several studies (e.g., Henson, '61; Webster, '61;Oaks, '67; Lay, '72) it has been tacitly assumed that the greater this pressure increase, the more efficient the mid-

361


a

b



Fig. 28 Two interpretations of the relationship between the middle ear areal ratio and the relative middle ear volume in 26 species of Heteromyidae. D, Dipodomys; L, Liomys; M, Microdipodops; P, Perognathus. TABLE 2

Relative middle ear size and habitats ~

Species L. adserpsus L. irroratus P. spinatus P. californicus P. fallax P. penicillatus P. intennedius P. fonnosus P. baileyi P. parvus P. longimmbris P. amplus P. flavescens P. merriami P. arenarius D. panamintinus P. flavus D. ordii D. agilis D. stephensi D.deserti D. spectabilis D. microps D. merriami M. megacephalus M. pallidus 1

~~

Rel. MEV

1

0.10 0.11 0.13 0.15 0.15 0.15 0.16 0.17 0.18 0.18 0.19 0.20 0.21 0.22 0.23 0.23 0.24 0.25 0.25 0.26 0.27 0.28 0.29 0.29 0.31 0.31

Rel. MEV, relative middle ear volume.

Habitat (from Burt, '64)

dense grasslands dense thickets rocky slopes - sparse veg. dense chaparral on slopes sandy areas - heavy low veg. - weeds sandy desert floor - sparse veg. rocky slopes - sparse veg. rocky slopes - sparse veg. rocky slopes - sparse veg. sagebrush - piiion - dense veg. sagebrush - creosote - sand covered by pebbles scattered veg. - arid desert sparse veg. - sandy soil sparse veg. - sandy-gravelly soil fine rocky slopes - little veg. sandy to gravelly soil - scattered large veg. short grass prairies - sandy sandy to hard soil - discontinuous veg. sandy to gravelly washes in chaparral sandy to gravelly soil - sparse veg. fine sandy areas - very sparse veg. semiarid grassland - scattered brush sandy to gravelly soil - sparse sagebrush sandy to rocky soil - scattered veg. fine sandy soil - sagebrush fine sand - scattered brush

362


dle ear mechanism. When one considers the dynamics of the middle ear, however, it becomes obvious that this assumption is incorrect. We can add no new information to the highly technical presentations of middle ear functioning published in recent years by, for instance, Zwislocki ('65), Mdler ('72), and Dallos ('73). Instead, it is our aim to discuss the functional characteristics of the mammalian middle ear from a more descriptive point of view. The middle ear mechanism, in order to function most efficiently, must transform acoustical energy of the air in the external auditory meatus to acoustical energy of the fluids of the cochlea with a minimal loss of energy, The middle ear is therefore primarily a matching transformer of energy, not a pressure amplifier. In physical terms, it must match the acoustical impedance of the fluid-filled cochlea with the acoustical impedance of air. Acoustical impedance is a measure of a medium's characteristics for transmitting sound energy, and is related to both its density and its elasticity (or stiffness). Since air (as in the external auditory meatus) is much less dense and more elastic than fluid (as in the cochlea), the difference in their impedances is very large. The middle ear mechanism reduces the apparent impedance of the cochlea (when measured at the tympanic membrane) and therefore (partially) matches the impedances. Acoustical impedance is expressed as the ratio of sound pressure to volume velocity. The impedance matching of the middle ear affects both these factors. Pressure at the stapes is increased in two ways. First, the force striking the large tympanic membrane is concentrated onto the smaller footplate of the stapes; therefore the force per unit area - that is, pressure - is increased as the ratio of the two areas. Secondly, the manubrium of the malleus is longer than the long process of the incus; therefore pressure is increased as the ratio of the two lever arms. The total pressure increase at the stapes is the product of these two factors. Velocity at the stapes is decreased as pressure is increased, because of the nature of levers, and the amount of this decrease is determined by the lever ratio.

Velocity is not affected by the areal ratio. Mathematically this impedance matching function of the middle ear may be stated as in the formulation of Dallos ('73):

In this equation, Zd/Zs is the impedance transform ratio of tympanic membrane to stapes, As/2/3(Ad) is the areal ratio of stapedial footplate to 2/3 the tympanic membrane, and li/Z is the lever ratio of incus to malleus. Two-thirds of the tympanic membrane area is used, because experimental evidence indicates that only that much is effective in moving the malleus (Wever and Lawrence, '54; Tonndorf and Khanna, '71, discuss exceptions with highfrequency stimulation). The lever ratio is squared in this equation because it affects both pressure and velocity. Note that the lever and areal ratios are inverted here, compared to the way they were presented by Wever and Lawrence, because the present formulation deals with matching the impedance of the cochlea to that of the air, rather than with the increase of pressure from tympanic membrane to stapes. Tonndorf and Khanna ('71) have suggested that because excursions of the tympanic membrane are greater on either side of the manubrium than at the manubrium, there must be a caternary lever system with the tympanic membrane, and that this must be considered in calculating the impedance matching of the middle ear. We have omitted consideration of this since, for this type of lever to be effective, the tension exerted by the radial fibers of the tympanic membrane would have to be considerably greater than that observed by many investigators (e.g., Bekesy, '60). If the middle ear impedance transform ratio reduces the impedance at the tympanic membrane to exactly 41.5 dynes sec/cm3 (the acoustical impedance of air), then all the acoustical energy that strikes the tympanic membrane will theoretically be transmitted to the inner ear. However, if the acoustical impedance at the tympanic membrane is either greater than or less than 41.5 dynes seclcm3, then some of the energy at the tympanic membrane will be reflected and will not affect the inner ear. The fraction of acoustical en-

363


ergy theoretically transmitted (T) to the cochlea by the middle ear mechanism can be expressed by the equation presented by Dallos ('73):

'=[

4[Sl 1 f -Z d i ] ' 41.5

Note that when Zd equals 41.5 dynes sec/ cm3, then T = 1 ; all energy is transmitted and none is reflected. However, if % is either greater than or less than 41.5 dynes sec/cm3, then T < 1 and some of the energy is reflected at the tympanic membrane. The fraction of acoustical energy which is reflected is expressed as 1 - T. However, these calculations require that the acoustical impedance at the tympanic membrane (Zd) be known. While we cannot determine zd from physical measurements of the system, we do have the ratio Zd/Zs from the impedance transform ratio. Therefore, if one can estimate the acoustical impedance of the cochlea, one can calculate Zd, and then the fraction of acoustical energy theoretically transmitted. Zwislocki ('65) has calculated the acoustical impedance of the human cochlea as 5600 dynes seclcm3. This calculation, although based on some unproven assumptions and a different species, is the best estimate available for any species. If it is accepted as a good estimate for the human, it should also be legitimate as a first approximation for mammalian cochleae in general, since the primary factor that determines cochlear impedance is the viscous drag of the cochlear fluids against the walls of the scalae. Therefore we will use this figure for Zsin our calculations. A theoretical Zd can then be determined from the impedance transform equation. The obtained value of Zd can then be substituted into the above equation for T in order to estimate the fraction of energy theoretically transmitted to the cochlea for a particular species (assuming Zs= 5600 for all species). A curve can be drawn with these data, showing 100% transmission at 41.5 dynes sec/cm3, 96% transmission at 29 and 60 dynes seclcm3, 86% transmission at 19 and 90 dynes seclcm3, and so on. (Impedance transform ratios, Zds, and percent transmitted for hetero-

myids, cat, and human are presented in table 3 . ) However, these calculations represent the theoretical, best-possible performance of the middle ear mechanism in transforming acoustical energy from vibrations in air to vibrations in cochlear fluids. The mechanism can do no better than its physical measurements indicate, and in fact will not do as well, for all of the foregoing discussion is based on the assumption that the middle ear mechanism is a perfect machine, matching the two impedances with no loss of energy. In reality, of course, no mechanical device has such efficiency, and some of the energy absorbed by the tympanic membrane is lost: that is to say, the middle ear itself has impedance. The total impedance of the tympanoossicular-cochlear system is due to three factors, which affect energy flow: friction, mass, and stiffness. Mathematically, Dal10s ('73) has expressed the relationship among these factors as:

z=

J..+[2rfM-]

s

2

2ilf

where Z is the total impedance, R is the resistive (frictional) component, f is frequency, M is the mass component, and S is the stiffness component. Friction is a negligible factor in most mammalian middle ears, because of the delicate Buspension of the ossicles in air; it is an important factor in the cochlea, however, because of the viscous drag between the cochlear fluids and the walls of the scalae. In fact for practical purposes friction can be considered to supply the total impedance of the cochlea except at very low frequencies (Dallos, '73). Impedance due to friction - that is, resistive impedance - is not dependent on the frequency of sound but is constant at all frequencies. On the other hand, energy loss due to mass and stiffness, called the reactive portion of the impedance, is dependent on frequency. Because friction is minimal in the middle ear, the effects of mass and stiffness are dominant. Mass in the middle ear is contributed by the tympanic membrane and the ossicles; stiffness is contributed by many factors including the tympanic membrane, the ossicular ligaments, the muscles and their attachments,

364

DOUGLAS B . WEBSTER A N D MOLLY WEBSTER TABLE 3

Functional parameters of middle ears

zrl-

(cm3)

Area ratio Stapes 213TM

Lever ratio I M

12 14 25 14 12 18 20 16

0.51 1.41 0.47 0.52 0.53 0.43 1.oo 0.60 0.68

0.06 0.06 0.06 0.06 0.07 0.06 0.06 0.06 0.06

0.29 0.31 0.29 0.31 0.33 0.32 0.30 0.30 0.30

0.005

Microdipodops megacephalus pallidus -

24 16

0.31 0.38 0.34

0.06 0.06 0.06

Perognathus amplus arenarius baileyi californicus fallax flavesc e n s flavus formosus intermedius longimembris merriami parvus penicillatus spinatus -

6 2 20 8 16 2 8 26 4 21 4 10 18 2

0.06 0.09 0.11 0.05 0.05 0.05 0.07 0.06 0.04 0.05 0.06 0.07 0.04 0.03 0.06

6

0.03 0.03 0.03

No.

of

ears

Dipodomys agilis deserti merriami microps ordii panamintinus spectabilis stephensi X

X

X

Liomys adserpsus irroratus Cat

1

X

4

2

Human 2 2

-

MEVI

dynes

ITR

s

T

cm3

(W 1

0.005 0.006 0.008 0.006 0.005 0.005

29 32 28 31 42 36 30 30

97 98 96 98 100 99 98 97

0.28 0.28 0.28

0.005 0.004

28 25

96 94

0.04 0.05 0.04 0.05 0.05 0.06 0.06 0.04 0.05 0.05 0.05 0.05 0.05 0.05 0.05

0.39 0.46 0.43 0.46 0.45 0.38 0.39 0.43 0.44 0.41 0.37 0.41 0.43 0.44 0.42

0.006 0.010 0.008 0.011 0.010 0.008 0.009 0.008 0.009 0.008 0.006 0.008 0.009 0.009

33 55 45 63 45 48 47 52 45 36 47 49 50

99 98 100 96 98 100 99 100 99 100 99 100 99 99

0.06 0.06 0.06

0.55 0.60 0.57

0.019 0.021

107 116

80 78

0.05

0.50

0.012

67

94

0.035

193

60

2.00

1

0.006

55

MEV, middle ear volume; ITR,impedance transform ratio. See Dallos, '73, p. 113.

the annular ligament of the stapes, and the volume of the airy cushion of the middle ear cavity. As can be seen from the formula, mass and stiffness are reciprocally related: mass reactance increases and stiffness reactance decreases with increasing frequency (i.e., mass is more important than stiffness in impeding acoustical energy transfer at higher frequencies, while the reverse is true at lower frequencies). Moreover, since the total reactive portion is the difference between the mass and stiffness components, there is one frequency for

each animal at which these two factors cancel each other. At this frequency, the so-called resonant frequency, the total impedance of the middle ear is caused by friction, and therefore it approaches zero. (The impedance of the cochlea, which is not dependent on frequency, remains.) Considering the physical properties of the middle ear alone, at this resonant frequency the transfer of energy into the cochlea should be at its maximum and should approach the theoretical transfer indicated by the equations above. And in fact it has been shown in several mam-


mals that this resonant frequency corresponds with the most sensitive frequency as determined by physiological tests of hearing such as cochlear microphonics (Dallos, '70). Below this frequency, stiffness reactance of the middle ear dominates; above it, mass reactance dominates. That is, if mass is great, the hearing sensitivity curve will slope sharply above the best frequency; if stiffness is great, the curve will be steep below the best frequency; reduction of either factor will cause a flattening of that part of the sensitivity curve. In summary, there are four important points of interest in the functioning of the middle ear mechanism. (1) The transfer of acoustical energy from the air of the external auditory meatus to the fluids of the cochlea is accomplished through the combined action of areal and lever ratios in the middle ear, which functions as a transformer to match the impedances of these two media. The impedance transform ratio, derived from the areal and lever ratios, and the formulas in which it is used, indicate the ability of the middle ear to match the impedances. A perfect match would reduce the apparent impedance of the cochlea (when measured at the tympanic membrane) to that of the air, which is 41.5 dynes sec/cm3; if. this much reduction were accomplished by the middle ear, 100% of the acoustical energy striking the tympanic membrane would theoretically be transferred to the cochlea. (2) Because the middle ear is not a perfect machine, but has impedance of its own, it does not perform with 100% efficiency. Since its friction is minimal, however, it approaches the idealized, 100% figure at its so-called resonant frequency - but only there - where the effects of mass and stiffness cancel each other. The impedance formula, which shows the relationship between Z, R, M, S, and f, indicates, among other things, the amount of energy lost by the total tympano-ossicularcochlear system. (3) Because the total impedance transform ratio of the middle ear is determined by the product of the areal and lever ratios, a modification of either will change the impedance matching. However, a change in the lever ratio will have the

365

greater effect, because the lever ratio is squared in determining impedance transform ratios (although it is not squared in determining pressure transformer ratios). (4) Similarly, because of the reciprocal relationship of the mass and stiffness reactances in the impedance formula, a modification of either will affect the absolute impedance of the middle ear. However, the relationship between these factors will determine the resonant frequency, or area of greatest sensitivity. The amount of mass and stiffness present will influence sensitivity above and below that frequency. The impedance of the cochlea is due to friction, however, which is not dependent on frequency. Thus, the middle ear plays a dominant role in determining the shape of an animal's auditory sensitivity curve. Functional significance of heteromyid middle ears The structural diversity of the middle ear in Heteromyidae involves both the structures that contribute mass and stiffness (and thus determine the impedance of the middle ear itself), and the components of the ratios that determine the middle ear's impedance matching ability. Thus these modifications have important functional ramifications. Impedance of the s y s t e m Mass. The mass of the middle ear transformer is contributed by the tympanic membrane and the ossicles. The ossicles of heteromyids, like those of most small mammals, have little mass simply because of the animals' size. This small mass is even further reduced in Dipodomys and Microdipodops by the extreme thinning of the stapedial footplate, and in Perognat h u s by the reduction of the crura which appear in cross-section as thin arcs rather than as rods. Such small mass suggests reduced impedance of high frequencies. Stiffness. The thinning of the heteromyid tympanic membrane (which occurs especially in its middle connective tissue layer) reduces its stafness as well as its mass. The ligaments supporting the ossicles are reduced to two, the anterior ligament of the malleus and the posterior ligament of the incus; these are essential in all mammals since they form the poles of the axis of rotation and, particularly at

366


low frequencies, maintain the ossicles in the best configuration for transmitting sound to the inner ear (Bekesy, '41). That the additional ligaments which in many mammals are attached to the malleus are lost in heteromyids suggests a decrease in the stiffness of the heteromyid tympanoossicular system. Stiffness is also caused by the tendinous attachments of tensor tympani to malleus, and of stapedius to incus. The tensor tympani and its tendon are quite small in all heteromyids, while the stapedius is very fine in Dipodomys and Microdipodops and totally absent in Liomys and Perognathus, again suggesting loss of stiffness in the tympano-ossicular system. The stapedial footplate is attached to the rim of the oval window by the annular ligament, which in most mammals is a continuous group of collagenous fibers from the middle ear side to the vestibular side of the bone. In Dipodomys and Microdipodops, however, the annular ligament is extremely fragile, being composed of a group of fine fibers on each side with only a few fibers between them. This reduced annular ligament would further decrease the stiffness of the tympano-ossicular system. In L w m y s and Perognathus the annular ligament is even more reduced, suggesting even greater stiffness reduction. Finally, the middle ear volume itself plays a significant role in determining the stiffness of the system; the smaller the middle ear cavity, the stiffer the system should be. Moreover, the larger the surface area of the tympanic membrane that must move against this airy cushion, the greater the stiffness added by the middle ear cavity. In Dipodomys and Microdipodops, a large tympanic membrane is correlated with a large middle ear volume. The large tympanic membrane allows a high areal ratio (of tympanic membrane to stapes); the large middle ear volume keeps the stiffness reactance factor very small. In those species where the middle ear has not inflated so greatly (e.g., all Perognathus species), a more favorable areal ratio has been developed not by enlargement of the tympanic membrane but by reduction of the s t apedial footplate. The morphology of the heteromyid middle ear, therefore, suggests a great reduction in the stiffness of the sound-transmit-

ting apparatus. This can be interpreted as an adaptation for low-frequency sensitivity since the stiffness factor in impedance is inversely proportional to frequency. Auditory sensitivity. That at least D. merriami has extremely good low-frequency auditory sensitivity has been shown by several studies (Webster, '62; Dallos, '70; Vernon et al., '71; Webster and Strother, '72; Webster and Webster, '72). Dallos ('70), recording cochlear microphonics from differential electrodes in the basal turn of D. merriumi, cats, chinchillas, and guinea pigs, found that sensitivity to low frequencies (20-1000 Hz) was greater in D. merriami than in the other three. In the same study, Dallos measured the phase of the cochlear microphonic relative to the phase of the sound at the tympanic membrane; the measured phase angle is positive when stiffness predominates in the impedance function, negative when mass predominates, and zero at the resonant frequency where the effects of mass and stiffness cancel each other. In cats, chinchillas, and guinea pigs Dallos found both the most sensitive cochlear microphonics and 0" phase angles at or about 1000 Hz; in D. merriumi both were found at 500 Hz. These data confirm the good low-frequency sensitivity of D. merriumi, and also indicate reduction of stiffness, since stiffness dominates total reactance only below 500 Hz. Webster and Strother ('72) used cochlear microphonics to determine the auditory sensitivity of 13 heteromyid species (of Dipodomys, Microdipodops, and Perognathus). In all 13 species low-frequency response (125-500 Hz) was more sensitive than high-frequency response (4000-1 6,000 Hz). There was a strong correlation between middle ear volume and low-frequency sensitivity, but no correlation between middle ear volume and high-frequency sensitivity, indicating that the enlargement of the middle ear cavity decreases stiffness and enhances low-frequency reception but has no particular effect on high-frequency reception. Mass is also reduced in these rodents, however, as explained earlier, and in this cochlear microphonic study the reduction of both mass and stiffness was evident from the flatness of the sensitivity curves. Within each of the three genera there is


no more than a 35 dB difference between the most sensitive and the least sensitive frequency over the range of 75 Hz through 16,000 Hz. There are no published data for the auditory sensitivity of Liomys or Hetero m y s , and we have not been able to study the morphology of Heteromys. The few pictures and the brief description of Heteromys given by Pye and Hinchcliffe ('68; Hinchcliffe and Pye, '69) indicate that its middle ear structure is probably very similar to that of Liomys. In Liomys, the middle ear is relatively small and the transform ratio much less sensitive (compared to the other three heteromyid genera studied); it is to be concluded therefore that their auditory sensitivity is also less. However, they have only two ossicular ligaments, no stapedius muscle, and a reduced annular ligament. As has been discussed, these are all adaptations for low-frequency sensitivity. It is interesting to speculate on the possible effects of the different types of middle ear walls found in different genera. The hypertrophied, smooth-walled middle ear cavities of Dipodomys and Microdipodops clearly increase the volume of the dead air space enclosed behind the tympanic membrane, and decrease its stiffness for a tympanic membrane of a given size. There is no evidence concerning the possible significance of the compartmentalization formed by the walls of the middle ear cavity, which create narrow passages between antrum and hypotympanum, and between epitympanum and hypotympanum. In Perognathus and to a lesser extent in Liomys the walls of the middle ear cavity are heavily or finely trabeculated, and an undetermined portion of the total measured middle ear volume is comprised of extremely small, interconnected air cells. However, the diameters of these air cells and of their continuities with the open portions of the middle ear cavity are so small relative to even high-frequency wave lengths (e.g., 3.44 mm for a 100,000 Hz tone) that the air contained within the trabeculated wall cannot possibly contribute in any kinetic way to the dynamics of the middle ear cavity. Therefore the effective middle ear volumes of Perognat h u s and Liomys are smaller than those reported in table 1.

367

Pneumatized bone is found in birds, where i t has a lightening effect. This seems not an important consideration in Perognathus and Liomys since the pneumatization actually increases the mass over what it was in the unspecialized condition and over what it is in Dipodomys and Microdipodops. Pneumatized bone is also found in many parts of the periotic and mastoid portions of most human ears. Because pneumatization makes the temporal bone less dense than the surrounding bones, it introduces an impedance mismatch which would cause poor bone-conducted sound transmission to the temporal bone. However, it is difficult to postulate a reasonable adaptive value for insulation from bone-conducted sound in pocket mice. Since trabeculation of middle ear walls occurs during postnatal development of middle ear hypertrophy in Dipodomys m e r riami (Webster, '75), it could be that trabeculation is linked to the genetic changes causing increased middle ear volume. Assuming selective pressure for a functionally large middle ear (to reduce stiffness), it could follow that trabeculation develops in Perognathus and Liomys due to a limitation of genetic mechanisms, and is neither adaptive nor maladaptive in itself.

Impedance matching During the evolution of the heteromyid species, an increased middle ear volume has been correlated with an increased tympanic membrane diameter (and with it, an elongated manubrium of the malleus). This affects both the areal ratio and the lever ratio. In Dipodomys and Microdipodops the difference between the lever arms is further increased because the long process of the incus is set at an oblique angle to the axis of rotation, which makes it functionally even shorter. In Perognat h u s the lever arms are not unusual, but the footplate of the stapes is very much reduced; therefore, despite the relatively smaller middle ear and tympanic membrane, there is a large difference between the two areas. This has the effect of yielding pressure transformer ratios of similar values in these three genera, indicating similar pressure increases accomplished by different morphological means. However, because the lever ratio is squared in the impedance transform ratio, imped-

368


ance matching is greater for Dipodomys and Microdipodops than it is for Perognat h u s (fig. 29). All three genera have smaller impedance transform ratios and larger percent transmissions than either the human or the cat (table 3). In Liomys neither the areal ratio nor the lever arm ratio is larger than usual, and therefore the transform ratio is also unremarkable. Regarding the tympano-ossicular system alone, therefore, one could consider Liomys as representing the generalized heteromyid condition, with the specialized condition of a large areal ratio evolving in the line toward Perognathus, and that of a large lever ratio in the line toward Dipodomys and Microdipodops. Using impedance transform ratios and a cochlear resistive impedance of 5600 dynes sec/cm3 (Zwislocki, '65), we have calculated the impedance at the tympanic membrane and the percent of acoustic energy transferred to the cochlea in the heteromyid species in this study. In the genera Perognathus, Microdipodops, and Dipodomys, 94-100% of the sound energy striking the tympanic membrane would be transmitted to the cochlea; in L w m y s , only

,019

02'

1

78-80 % . These calculations, of course, apply only at the resonant frequency and furthermore assume that there is a negligible frictional or resistive component to the impedance of the tympano-ossicular system. It is clear that the impedance matching apparatus of Dipodomys, Perognathus, and Microdipodops is extremely efficient. When one further considers that in these rodents both the stiffness and the mass factors are minimized by the morphology of the middle ear, one would expect very sensitive hearing - not only at the system's resonant frequency but also over a broad range above and below this resonant frequency. This is consistent with both electrophysiological and behavioral data (Webster, '62; Vernon et al., '71; Webster and Strother, '72; Webster and Webster, '72). One of the most interesting implications of the functional study of the middle ear is the realization that too large a pressure increase is as bad as too small a pressure increase. Oaks ('67 and personal communication) and Lay ('72) have studied many non-heteromyid rodents with enlarged middle ear cavities. They calculated pressure transformer ratios, but not impedance transform ratios or the fractional transmission at the resonant frequency. Using their data we have made these calculations; the results are presented as a plot of calculated impedance at the tympanic membrane against fractional transmission of sound from external auditory meatus to cochlea (fig. 30). The data plotted include

N = 26 y I - . 0 5 IX+ ,0188 N = 24 y = ! - .03 IX+ ,0138 i

,009 007

,005

1 1 1 I

1

2

3

Relative Middle Far Volume

Fig. 29 Relationship of relative middle ear volume to impedance transform functions in 26 species of Heteromyidae. D, D i p o d o m y s ; L, L i o m y s ; M , M i c r o d i p o d o p s ; P, Perognathus.

10

20

40

70

110

170

Impedance at Tympanic Membrane In dynes reclcm3 !Zdi

Fig. 30 Graphic representation of the fractional transmission (at the resonant frequency) in the heteromyids studied here, and as computed for other rodents from the data of other investigators.

369


16 species measured by Lay, 33 species measured by Oaks, and 26 species reported here. Six species were measured by both Lay and Oaks; in all six cases, the measurements obtained by Oaks indicate a higher percentage of sound transmitted than do those obtained by Lay. This is partly because of the different measuring techniques: Oaks measured the tympanic membrane as a flat circle (as did we), while Lay measured it as a cone. Moreover Lay measured the areas from silicone casts of the middle ear cavities, and the ossicles directly but from different animals. While in fact the tympanic membrane is a cone and it should be more accurate to measure it as such, we have found in practice that this is not desirable. Measurements of the height of the cone are affected by several factors including drying artifacts and the degree of tension of the tensor tympani at death; as a result consistent measurements are difficult or impossible to obtain, and this is particularly so when specimens have undergone different treatments. However, for an earlier paper (Webster, '61) we did measure the tympanic membrane as a cone in living D. merriami. We have now used those measurements to calculate z d and percent transmission based on the tympanic membrane as a cone, and have compared them with our present calculations based on the tympanic membrane as a flat circle. In such a comparison the important value is the z d , as is clear from the plot presented in figure 30. Calculations based on our two sets of data for D. merriami yield Z d s that differ by 1.7 dynes seclcm3 (which for this

species makes a 3% difference in sound transmission). The Z d values for the species which were measured by both Oaks (in manuscript) and Lay ('72) are compared in table 4. Because the Zd is influenced by all components of the ratios in the impedance matching formula, we next looked at the measurements reported by Oaks and Lay. Their measurements for the ossicles differed only slightly. Their measurements of the stapedial footplate differed by an average 1 2 % , with Lay's being consistently smaller; Oaks states (in manuscript) that this may be because she used calipers, which were less accurate. Their measurements of the tympanic membrane also differed: 213 of the surface area measured by Lay's method (not including the accessory tympanic membrane) is about 1.5 to 2 times larger than the same measurement by Oaks' method. This can be compared with our two measurements of 213 the tympanic membrane area in Dipodomys merriami: 17.3 mm2 when it was measured as a cone, and 15.83 mm2 when it was measured as a flat circle. One wonders if the silicone rubber casts from which Lay made his measurements could either alter the morphology of the middle ear during insertion or shrink differentially during hardening. For whatever cause, however, Lay finds larger tympanic membranes and smaller stapedial footplates than Oaks finds in the species they both measured; that is, Lay's data yield larger pressure transformer ratios than Oaks'. The larger pressure transformer ratios (tympanic membrane to stapes) necessarily result in smaller im-

TABLE 4

Impedance at tympanic membrane calculated f r o m data of Lay ('72) and Oaks (inmanuscript)

Psammomys obesus Gerbillus pyramidum Meriones crassus (Egypt) Meriones crassus (Iran) M . unguiculatus Desmodillus auricularis Pachyurumys duprasi

Lay

oaks

Difference

16.24 22.40

34.16 46.48

17.92 24.08

22.40

10.64

36.96 36.40 41.44

18.48 20.16 21.28

"'>%: 12.8 18.48 16.24 20.16

11.76

370


pedance transform ratios (stapes to tympanic membrane). The smaller the impedance transform ratio, the smaller the impedance of the ear as measured at the tympanic membrane (Zd). When Zd is less than the impedance of air (41.5 dynes sec/ cm3), the efficiency of transmission falls off rapidly. A similar, but less rapid, fall off of transmission efficiency occurs when Zd is greater than the impedance of air (fig. 30, noting that the abscissa is a log scale). As shown on figure 30, many of the species from both this study and that of Oaks cluster around 100% transmission, indicating that, if the impedance of the cochlea is 5600 dynes sec/cm3 for all species, and if there is negligible frictional impedance in the middle ear, nearly 100% of the acoustical energy at the resonant frequency will be transmitted in many rodent species. Among the heteromyids, the species of the genera Microdipodops, Dipodomys, and Perognathus range from 94% to 100% transmission, while Liomys sp. have 78-80 % transmission. As is also shown on figure 30, the transmission efficiencies for rodents in these three studies exceed the 60 % transmission efficiency calculated for man (Dallos, '73), many by close to 40%. This makes a difference of about 4.4 dB in hearing sensitivity; in human hearing, where discrimination of speech and other complex patterns well above threshold is important, 4.4 dB is so insignificant that it is considered within the limits of measurement error. However, in desert rodents at least, hearing is critical at intensities close to threshold where a 3 or 4 dB difference ( 3 0 4 0 % transmission) could well mean the difference between detecting and not detecting a predator (Webster, '62; Webster and Webster, '71 ; Lay, '74).

Adaptive value of middle ear modifications and probable evolution of t h e middle ear in Heteromyidae Both electrophysiological and behavioral data have demonstrated that in D. merriami the auditory sensitivity for low frequencies (below 2000 Hz) is reduced by as much as 20 dB when the middle ear cavities are surgically reduced by approximately 70%, thus indicating that enlarged middle ear cavities facilitate low-frequency

reception (Webster, '62; Webster and Webster, '72). Correlated behavioral studies (Webster, '62; Webster and Webster, '71) have demonstrated that normal D. merria m i can effectively avoid the predatory strdces of rattlesnakes and owls and that blinded D. merriami can avoid those of rattlesnakes, but that bilateral reduction of middle ear volume combined with the inability to use vision makes these animals vulnerable to the strikes of rattlesnakes and owls; and that both these predators produce sounds below 2000 Hz just prior to their predatory strikes. We conclude that the enlarged middle ear cavities of Dipodomys merriami facilitate low-frequency reception by decreasing the stiffness reactance component of the tympano-ossicular system, and that this enhanced lowfrequency sensitivity is adaptive in predator avoidance. The selective pressure for such mechanisms to evolve would be particularly great for animals living in an area with very little natural cover, where sparse vegetation would both increase the need to forage and decrease the protection. Lay ('74) has shown that the gerbil, Meriones libycus can also avoid owl predation even when blinded. Many authors have noted that animals with large bullae inhabit dry areas and those with small bullae inhabit moister areas (e.g., Heim de Balsac, '36; Petter, '53, '61; Webster, '61, '62, '69, '70; Oaks, '67, MS in preparation; Lay, '72); they have frequently postulated strong correlations between aridity and middle ear size, related directly or indirectly to predator avoidance. Webster ('69), on the basis of data then available, stated that larger relative middle ear volumes are found in species in extremely arid environments than in less arid regions. However, now that we have extensive data on 26 heteromyid species it is evident that there are not such strong correlations. Some species are found in many different habitats, while others are narrowly restricted: Microdipodops sp. (0.31 relative inflation) and Dipodomys deserti (0.27) are found only in areas of very dry, shifting sand with very sparse vegetation; Perognathus Zongimembris (0.19) is sometimes sympatric with Microdipodops but is also found in sandy-rocky soil with much heavier vegetation; D. merriami (0.29) is

371


widespread and sympatric with heteromyids of widely differing degrees of relative inflation. Perognathus spinatus (0.13) is found only on slopes with rocky or coarse sandy soil and little vegetation; P. californicus (0.15) is found in dense cover on chaparral slopes, while P. penicillatus (0.15) is found in a variety of habitats including rocky slopes and sandy washes, and P. fallax (also 0.15) is found in several habitats from sparse vegetation and hard, rocky soil, to chaparral and loamy soil. Moreover, there is a great deal of sympatry, both among species with like middle ear inflation and among species with disparate middle ears: a few examples are presented in table 5. Many factors influence both species distribution and the suitability of an area for one or more particular species. Kenagy ('72), for example, has shown that while most heteromyids eat primarily seeds but include some seasonal green vegetation, D. microps thrives on a diet of saltbush leaves. This animal's chisel-shaped lower incisor teeth enable it to strip off the outer portion of halophytic leaves and eat only their low-electrolyte portions; thus it can coexist with the seed-eating D. merriami in areas of little food. Rosenzweig and Winakur ('69) and Rosenzweig ('73) found that density of foliage, particularly at various levels above ground, is important in species distribution. However, while P. peniciliatus and P. baileyi require similar hab-

itats with bushy vegetation, P. baileyi were taken on plots supporting jojoba and P . penicillatus on similar plots without jojoba. Moreover, D. merriami was rare or absent in otherwise suitable habitats which contained P. baileyi, which, they suggest, is because P. baileyi has a competitive advantage in food gathering. (However, we have found these species together.) They feel that the ability to escape predation is only one aspect of species distribution among desert rodents, and that competition for resources is another. On the other hand, Brown ('73) and Brown and Lieberman ('73), studying sympatry in granivorous rodents on sand dunes, found different patterns of resource utilization as the basis for coexistence. Sympatric species differed in size in a regular pattern, and tended to eat seeds of different sizes (although there was considerable overlap) and to forage at slightly different distances from shrubs. According to their findings, species of equivalent size replace one another but do not coexist. They attribute this and the large number of sympatric desert species to the particulate nature of seeds and to their year-round availability in desert habitats. Our areas 3 and 4 (table 5) were both sand dune communities supporting sympatric species of equivalent sizes. Our findings do not therefore wholly agree with those of Brown and Lieberman. In analyzing species and habitats many factors must be considered. For one, for-

TABLE 5

Selected e x a m p l e s of s y m p a t r y in Heteromyidae Areas Rel. MEV

M . pallidus D. m e r r i a m i

D. microps D. spectubilis D.deserti D.ordii P. f l a v u s P. l o n g i m e m b r i s P. p a m u s P.f o n n o s u s P. i n t e n n e d i u s P. f u l l a x P. penicillatus

1

N-0 1 1

0.31 0.29 0.29 0.28 0.27 0.25 0.24 0.19 0.18 0.17

1

2

X

X

X

X

X

X X

3

4

5

X

X X

X

X

41

X

33 17 19 23 23 21 24 22

X

X X

0.15 0.15

X

23 27 28 36

X

X

0.16

(mm)

X

X

Rel. MEV, relative middle ear volume; N-0, naso-occipital length. * A r e a 1, S a n Simon Valley, Ariz., 1965;2, San Simon Valley, 1967; 3, Penoyer Valley, Nev., 1971; 4,Schurz, Nev., 1968;5,Deepcanyon, Cal., 1969. 1

372


aging animals may cover a great deal of territory: Maza et al. (‘73) concluded that 86% of an animal’s activity occurs within a circle whose mean diameter is 62 m for P. formosus and 150 m for D. merriami, with the heaviest activity in the center of the circle. If one trapped an animal on the outer edges of its range, however, one might get a mistaken picture of its habitat. In any case, brief descriptions of habitats result in oversimplifications, as in table 2, and perhaps in overlooking the determining features of the area altogether. Unfortunately our data were not gathered in such a way as to allow a detailed analysis of species’ habitats. Nevertheless, as we examine our extensive field and trapping notes, collected in many southwestern states over seven summers, it is clear that, for the Heteromyidae at least, generalizations about increasing middle ear size being correlated with increasing aridity of habitat break down. However, although these generalizations about specific habitats do not hold in living species, environment in general apparently played a major role in the evolution of middle ear modifications. The paleontological history of Heteromyidae has been extensively studied by Wood (’35) and Reeder (’57). Reeder’s study correlated paleontology and paleobotany, and related heteromyid evolution to environmental selective pressures. From the earliest available fossil record heteromyids are divisible into three groups: one that gave rise to the living genera Heteromys and Liomys, another that gave rise to Dipodomys and Microdipodops, and a third that gave rise to Perognathus. The earliest species lived along streams in the then-subtropical area that is now Colorado and surrounding states. Their evolution continued coincident with the general rising of the western part of North America and the consequent development of large semi-arid and arid regions with discontinuous vegetation. Such environmental changes can have different effects on existing populations: they can cause extinction; they can prompt migration to favorable areas; or they can favor retention of genetic modifications that help adapt the organisms to the new environment. Fourteen extinct genera of Heteromyidae are known in the fossil record. Begin-

ning in the early Miocene, the L w m y s Heteromys lineage gradually moved southward- with the climate, as it wereremaining in subtropical to tropical regions to which they were already adapted and evolving the fewest middle ear modifications. The Perognathus lineage and the Dipodomys-Microdipodps lineage, encountering increasingly arid conditions during the Tertiary (Reeder, ’57), developed morphological modifications enhancing low-frequency sound reception. Many of the qualitative differences and similarities in heteromyid middle ear morphology are now more explainable (table 6). Three of the genera studied -Dipodo m y s , Microdipodops, and Perognathus have evolved similar functional characteristics involving two basically different groups of morphological modifications. Dipodomys and Microdipodops have in common smooth-walled middle ear cavities, with greatly inflated epitympanic, hypotympanic, and antral chambers; Dipodomys, undergoes trabeculation developmentally, but neither Dipodomys nor Microdipodops adults have any trabeculation. Both have retained the stapedius muscle. The Perogn a t h u s line responded to similar selective pressures in a different way: its middle ear cavity is not nearly as large, it has retained a great deal of trabeculation, and it has lost the stapedius muscle. Dipodom y s and Microdipodops have attained their spectacular impedance transform ratios primarily by an increase in the difference between the two ossicular lever arms; Perognathus, primarily by an increase in the difference between tympanic membrane and stapedial footplate areas (by developing a very small stapedial footplate). All three genera have most sensitive hearing in the low frequencies, indicating tympano-ossicular systems with low stiffness impedance; the greater sensitivity of Dipodomys and Microdipodops compared to that of Perognathus is probably due primarily to the larger middle ear volume. Liomys has a much more generalized middle ear structure. The antral portion is filled with trabeculation and does not form a chamber; the epitympanum and hypotympanum form quite small, untrabeculated chambers, The impedance ratio is similar to that in non-heteromyid rodents without inflated ears. The stapedius

373

HETEROMYID MIDDLE EARS TABLE 6

Qualitative middle ear characteristics by g e n u s Dipodomys

Microdipodops

Extent of annular ligament Adult stapedial A. Epitympanum Lever ratio Areal ratio Percent sound transmitted Antrum Hypotympanum Subarcuate fossa Stapedial crura Correlation of body size to bullae size 1

Perognathus

Heteromys

Liomys

I

no no antral

no no antral tympanic and vestibular sides no

full

full

no no antral epitympanic hypotympanic tympanic side

yes large large average

yes large large average

yes small small large

tympanic and vestibular sides no small small average

large large large large rod

large large large large rod

large small small small arc

average very small very small none arc

positive

positive

negative

negative

Bullate stapes Stapedius muscle Trabeculated bullae

? ? 3

?

Data from Pye and Hinchcliffe, '68; and Hinchcliffe and Pye, '69.

muscle and the stapedial artery are both lost. Although no experimental data on their auditory sensitivity are available, we suspect that Liomys (and Heteromys, which appears quite similar) does not have as great a low-frequency sensitivity as do the other heteromyid genera. Development of the middle ear in Dipodomys merriami involves the develop ment of trabeculation which then gives way to continually enlarging cavities (Webster, '75). One could imagine then that middle ear development simply stops at a n early stage in Liomys, before trabeculation is fully developed, and proceeds to the farthest stage in Microdipodops; the Heteromyidae could then be considered as an evolutionary continuum, from Liom y s through Perognathus and Dipodomys to Microdipodops. However, since almost all mammals have a stapedius muscle in the adult, and since in all mammals studied the stapes develops around the stapedial artery, the absence of these structures in Liomys must be regarded as a specialization. We suggest that the line of heteromyid evolution leading to the present-day Liom y s must have had little selective pressure for enlargement of the middle ear cavity, but significant pressure for loss of the stapedius muscle and stapedial artery. The divergent h e of heteromyid evolution leading to present-day Dipodomys and Mi-

crodipodops, on the other hand, must have experienced extreme selective pressure for enlargement of the middle ear cavity, but little or no selective pressure for loss of the stapedius muscle or stapedial artery. Selective pressure for an increased lever ratio in the Perognathus lineage was expressed not by a particularly expanded tympanic membrane but by a greatly reduced stapedial footplate. Furthermore, the middle ear of Liomys (and apparently Heteromys) is more similar to that of Perognathus than that of Dipodomys and Microdipodops; therefore we suggest that the common ancestor of Perognathus, Lio m y s , and Heteromys is more recent than the common ancestor of the DipodomysMicrodipodops lineage and any of the other three genera (fig. 31). Our interpretation of the evolutionary relationships agrees with Reeder's ('57), except that he suggested that the LiomysHeteromys lineage is more closely related to the Dipodomys-Microdipodops lineage than to the Perognathus lineage. A s table 6 documents, insofar as ear structure is concerned Liomys and Perognathus are extremely similar and quite unlike Dipodo m y s and Microdipodops. Hinchcliffe and Pye ('69), in their study of heteromyid ears, suggested that the family can be divided into two large taxaone containing Microdipodops and Dipodomys and the other Liomys, Heteromys, and Perog-

3 74

DOUGLAS B . WEBSTER AND MOLLY WEBSTER DIPODOMYS

Fig. 31 Suggested evolution of heteromyid rodents, based on our middle ear observations correlated with Reeder's ('57) paleontological and paleobotanical data. ACKNOWLEDGMENTS nathus. However, as Wood ('35) warned, parallelism is the overwhelmingly recurThis work was supported by research ring event in rodent evolution; its possible grants from National Institutes of Health occurrence everywhere obscures facile (NS-05800 and NS-11459). We are indebtdetermination of phylogenies. There are ed to the following persons and institunow karyotypic data on both Perognathus tions for direct and indirect assistance in (Patton, '67a,b) and Dipodomys (Fashing, the collection of animals: Dr. D. Bruce '73; Stock, '74) and data on protein vari- Dill (Director), Drs. W. Glen Bradley, Baration in Dipodomys (Johnson and Selan- bara Smigel, and Lars Soholt, and Messrs. der, '71). When similar information is Kendall Br aithw aite and David Wolf enberavailable for the other heteromyid genera, ger - all of the Desert Research Institute, the paleontological, chemical, morphologi- Boulder, Nev.; Mr. Lloyd Tevis, Deep Cancal, and karyotypic data combined should yon Desert Research Center (U. Cal., Riverpermit confident descriptions of the evo- side) at Palm Desert, Cal.; Mr. Vincent lutionary relations in the family. Roth, Southwestern Research Station (Am. Much less paleontological and other evo- Mus. Nat. Hist.) at Portal, Ariz. We are lutionary data are available for Old World particularly indebted to Dr. John K . Culgroups with enlarged middle ear cavities len, Jr., our colleague at Kresge Hearing (e.g., jerboas, gerbils, Pedetes). They are, Research Laboratory of the South, for however, found in generally arid regions many helpful discussions and for a critiwith little natural cover and presumably cal reading of the manuscript. were subject to the same selective pressures that operated in the evolution of Heteromyidae. In this family, the genetic LITERATURE CITED potential for middle ear specialization has Bekksy, G. von 1941 Uber die Messung der been utilized in those species evolving in Schwingungsamplitude der Gehorknochelchen mittels einer kapazitiven Sonde. Akust. Zeits., and adapted to arid regions, but has ex6: 1-16. Translated by E. G. Wever and r e pressed itself differently in Perognathus printed in Bekesy, G . von, Experiments in Hearthan it has in Dipodomys and Microdiing. McGraw-Hill Book Company, Inc., New podops. York, 1960, pp. 95-126.

HETEROMYID MIDDLE EARS Bekesy, G. von 1960 Experiments in Hearing. McGraw-Hill Book Company, Inc., New York. Brown, J. H. 1973 Species diversity of seedeating desert rodents in sand d u n e habitats. Ecology, 54: 775-787. Brown, J. H., and G. A . Lieberman 1973 R e source utilization and coexistence of seed-eating desert rodents in sand dune habitats. Ecology, 54: 788-797. Burt, W. H. 1964 A Field Guide to the Mammals. Houghton Mifflin Co., Boston. Cockerell, T. D. A., L. 1. Miller and M. Printz 1914 The auditory ossicles of American rodents. Bull. Am. Mus. Nat. Hist., 33: 347-378. Dallos, P. 1970 Low-frequency auditory characteristics: Species dependence. J . Acoust. SOC. Amer., 48: 489-499. 1973 The Auditory Periphery. Academic Press, Inc., New York. Fashing, N. J. 1973 Implications of karyotypic variation in the kangaroo rat, D i p o d o m y s heermunni. J . Mammal., 54: 1018-1020. Guild, S . R. 1968 Processing human temporal bones. I n : Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology. L. G. Luna, ed. Third cd. McGraw-Hill Book Company, Inc., New York, pp. 47-52. Hall, E. R., and K . R. Kelson 1959 Mammals of North America. Ronald Press, New York. Heim d e Balsac, H. 1936 BiogFgraphie des mammiferes et des oiseaux de 1’Afriquedu Nord. Bull. Biol. de France et de Belgique. Suppl. 21, 446 pp. Henson, 0. W., Jr. 1961 Some morphological and functional aspects of certain structures of the middle ear in bats and insectivores. Univ. Kans. Sci. Bull.. 4 2 : 151-255. Hinchcliffe, R., and A. Pye 1969 Variations in the middle ear of the Mammalia. J . Zool., Lond., 1.57.277-288. .-Hooper, E. T. 1968 Anatomy of middle-ear walls and cavities in nine species of microtine rodents. Occ. Pap. Mus. Zool. Univ. Mich., 657: 1-28. Howell, A. B. 1932 The saltatorial rodent Dipodomys: The functional and comparative anatomy of its muscular and osseous systems. Proc. Am. Acad. Arts Sci., 67: 377-536. Johnson, W . E., and R. K. Selander 1971 Protein variation and systematics in kangaroo rats (genus D i p o d o m y s ) . Syst. Zool., 20: 3 7 7 4 0 5 . Kenagy, G. J. 1972 Saltbush leaves: Excision of hypersaline tissue by a kangaroo rat. Science, 178: 1094-1096. Lay, D. M. 1972 The anatomy, physiology, functional significance and evolution of specialized hearing organs of gerbilline rodents. J. Morph., 138: 41-120. 1974 Differential predation on gerbils ( M e r i o n e s ) by the little owl, Athene h r n h m n . J. Mammal., 55: 608-614. Maza, B . G . , N. K. French and A . P. Aschwander 1973 Home range dynamics in a population of heteromyid rodents. J. Mammal., 54: 405425. M ~ l l e r A. , R . 1972 The middle ear. In: Foundations of Modern Auditory Theory. Vol. 2. J. v. Tobias, ed. Academic Press, Inc., New York, pp. 133-194. Oaks, E. C. 1967 Structure and function of ~~

~

3 75

inflated middle ears of rodents. Doctoral Dissert., Yale Univ. Patton, J. L. 1967a Chromosome studies of certain pocket mice, genus P e r o g n n t h u s (Rodentia: Heteromyidae). J . Mammal., 48: 27-37. 1967b Chromosomes and evolutionary trends in the pocket mouse subgenus Perognathus (Rodentia: Heteromyidae). Southw. Natur., 12: 4 2 9 4 3 8 . Petter, F. 1953 Remarques sur la signification des bulles tympaniques chez les mammiferes. C . R . Acad. Sci., 237: 848-849. 1961 Repartition geographique et ecologie des rongeurs desertiques de la region Palaearctique. Mammalia, Suppl., 219 pp, Pye, A,, and R. Hinchcliffe 1968 Structural variations in the mammalian middle ear. Med. Biol. Illust., 18: 122-127. Reeder, W. G . 1957 A review of Tertiary rodents of the family Heteromyidae. Doctoral Dissert., U. Mich. Rosenzweig, M. L. 1973 Habitat selection experiments with a pair of coexisting heteromyid rodent species. Ecology, 54: 111-1 17. Rosenzweig, M. L., and J. Winakur 1969 Population ecology of desert rodent communities: Habitats and environmental complexity. Ecology, SO: 558-572. Ryder, J . A. 1878 On the form of the stapes in D i p o d o m y s . Amer. Nat., 12: 125. Segall, W. 1969a The auditory ossicles (malleus, incus) and their relationships to the tympanic: In marsupials. Acta anat., 73: 1 7 6 191. 1969b The middle ear region of Dromiciops. Acta anat., 72: 48!+501. 1970 Morphological parallelisms of the bulla and auditory ossicles in some insectivores and marsupials. Fieldiana, Zool., 51 : 16% 205. 1973 Characteristics of the ear, especially the middle ear in fossorial mammals, compared with those in the Mctnidne. Acta anat., 86: 96-110. Shotwell, J. A . 1967 Late Tertiary geomyoid rodents of Oregon. Bull. Mus. Nat. Hist., Univ. Ore., No. 9, pp. 1-51. Simkin, G. N. 1965 Tipy slukhovykh polostei mlekopitayushchikh v svyazi s osobennostyami ikh obrava zhizni. Zool. Zhur., 44: 1538-1545. Stock, A. D . 1974 Chromosome evolution in the genus D i p o d o m y s and its taxonomic and phylogenetic implications. J . Mammal., 55: 505526. Tonndorf, J . , and S. M. Khanna 1971 The tympanic membrane as a part of the middle ear transformer. Acta Otolaryngol., 71: 177-180. Vernon, J., P. Herman and E. Peterson 1971 Cochlear potentials in the kangaroo rat, D i p o d o m y s m e r r i a m i . Physiol. Zool., 44: 112-118. Webster, D. B. 1961 The ear apparatus of the kangaroo rat, D i p o d o m y s . Am. J. Anat., 108: 123-147. 1962 A function of the enlarged middleear cavities of the kangaroo rat, D i p o d o m y s . Physiol. Zool., 35: 248-255. 1965 Ears of D i p o d o m y s . Nat. Hist., 74: 26-33. 1968 Comparative middle and inner

376


ear structure of Heteromyidae. Anat. Rec.,160. 447. 1969 Comparative middle ear morphology in Heteromyidae. Anat. Rec., 163: 281-282. 1970 T h e cochlear nuclei of Heteromyidae. Am. Zool., 10: 554-555. 1975 Auditory systems of Heteromyidae: Postnatal development of the ear of D i p o d o m y s merriami. J. Morph., 146: 377-394. Webster, D. B., and W. F. Strother 1972 Middle ear morphology and auditory sensitivity of heteromyid rodents. Am. Zool., 12: 727. Webster, D. B . , and M. Webster 1971 Adaptive value of hearing and vision in kangaroo r a t

predator avoidance. Brain, Behav. Evol., 4: 3 1 0-322. 1972 Kangaroo rat auditory thresholds before and after middle ear reduction. Brain, Behav. Evol., 5: 4 1 5 3 . Wever, E. G., and M. Lawrence 1954 Physiological Acoustics. Princeton University Press. Wood, A . E. 1935 Evolution and relationships of the heteromyid rodents. Ann. Carn. Mus., 24: 73-262. Zwislocki, J . 1965 Analysis of some auditory characteristics. I n : Handbook of Mathematical Psychology. Vol. 111. R. Luce, R. Bush and E. Galanter, eds. J o h n Wiley and Sons, Inc., pp. 1-97.

Auditory systems of Heteromyidae: postnatal development of the ear of Dipodomys merriami.

Functional morphology of the mucosa of the middle ear and Eustachian tube.

Evolution of the mammalian middle ear.

Ganglioneuroma of the External Auditory Canal and Middle Ear.

[Audiological evaluation of the middle ear implant--temporal auditory acuity].

The effects of body size on functional properties of middle ear systems of anuran amphibians.

Congenital middle ear anomalies: anatomical and functional results of surgery.

Evolution and Functional Morphology of the Proboscis in Kalyptorhynchia (Platyhelminthes).

Handheld tympanometer measurements in conscious dogs for the evaluation of the middle ear and auditory tube.

Clearance of middle ear effusions and middle ear pressures.

Arterial chemoradiotherapy for carcinomas of the external auditory canal and middle ear.

[Carcinoid tumor of the middle ear. Morphology, immunohistochemistry, clinical aspects and differential diagnosis].

Meckel's cartilage breakdown offers clues to mammalian middle ear evolution.

[Drainage of the middle ear].

Rhabdomyosarcoma of the middle ear and mastoid.

Resolving the evolution of the mammalian middle ear using Bayesian inference.

Navigation-guided transmodiolar approach for auditory nerve implantation via the middle ear in humans.

Details of human middle ear morphology based on micro-CT imaging of phosphotungstic acid stained samples.

Dissection of the Auditory Bulla in Postnatal Mice: Isolation of the Middle Ear Bones and Histological Analysis.

First branchial cleft fistula associated with external auditory canal stenosis and middle ear cholesteatoma.

Middle ear mass with facial weakness. Diffuse large B-cell lymphoma of the middle ear.

Diseases of the middle ear in childhood.

Middle ear muscles of the frog.

Burn injuries of the middle ear.