Proc. Nati. Acad. Sci. USA Vol. 76, No. 6, pp. 3031-3033, June 1979
Physiological Sciences
Middle ear muscles of the frog (amphibian ear/hearing)
ERNEST GLEN WEVER Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08544
Contributed by E. C. Wever, March 28, 1979
The anuran middle ear in its complete form includes two skeletal elements, the columella and operculum, each occupying a portion of the oval window of the otic capsule and each provided with a middle ear muscle. The two elements have an interlocking arrangement of a form that makes it possible for these muscles to exercise a high degree of control of sound transmission from tympanic membrane to inner ear receptors. From the anatomical relations it is inferred that the two muscles operate as antagonists so that contraction of the opercular muscle and relaxation of the columellar muscle leave the columella free to move in and out of the oval window in response to sound vibrations, whereas a contraction of the columellar muscle and relaxation of the opercular muscle tend to immobilize the columella and reduce the transmission inward. The frog thus achieves a degree of control of sound reception that probably is unmatched among vertebrate ears. The purpose of the middle ear mechanism is no doubt the protection of the inner ear receptors (the amphibian and basilar papillae) from overstimulation by sounds, including the animal's own cries and the intense clamor produced by a group of frogs calling in chorus. Gaupp (1) in his monumental treatment of the Anatomie des Frosches in 1896 first figured and named the opercular muscle in the anuran middle ear. He described this muscle as a derivative of the levator scapulae superior, which is a strong bundle running from the prootic region to the ventral surface of the suprascapula and serving to retract this cartilage. Gaupp was not the first to see the opercular muscle; Eiselt (2) in a thorough historical search found mention of it by Blainville as early as 1822 as a part of the shoulder musculature, and Huschke shortly thereafter spoke of this muscle as a homolog of the stapedius muscle of mammals. However, most subsequent writers on the anuran middle ear have referred to Gaupp's account and have agreed with him concerning the derivation of the muscle from the levator scapulae superior. A muscle that usually is regarded as corresponding to this one, and likewise called the opercular muscle, is present in the urodeles. However, the third Order of amphibians, the Gymnophiona or caecilians, lack this muscle along with the operculum itself. Numerous treatments of the middle ear mechanism in frogs have repeated Gaupp's descriptions of both the operculum and its muscle with little variation, but sometimes consideration has been given to the possible function of this mechanism in the hearing process. Earlier theorizing dealt extensively with this problem in urodeles, and a curious hypothesis was advanced involving the transmission of substrate vibrations through the forelegs, with the opercular muscle providing the path from shoulder region to ear. Much less attention has been given to the function of the middle ear in frogs, though it usually is assumed that the opercular muscle produces a damping of vibrations transmitted inward along the columella. De Burlet (3), in a general review of the vertebrate middle ear, offered a more ABSTRACT
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. 3031
specific suggestion for the anurans in which he compared the opercular muscle with the tensor tympani of mammals and supposed that this muscle on contraction conveys its restraints through the linkage of operculum and columella to the tympanic membrane and thus produces a flattening (and hence a stiffening) of its surface. Present observations The anatomy of the frog's middle ear has been studied in a variety of species as a part of a general examination of the ear and hearing in the amphibia. This study was stimulated by the observation of large variations in the ear's sensitivity, as measured in terms of its electrical potential in response to sounds. These variations were especially prominent in lightly anesthetized animals and at times amounted to as much as 40 db-a 100-fold variation in terms of the sound pressure required for a given electrical output. The variations continued in spite of a strict maintenance of experimental conditions, such as body temperature, the moist condition of the skin, and respiration, and pointed to the existence of some kind of internal control mechanism. Observations were made both by dissection under the binocular microscope and by the use of serial sections. The sectioning used the three standard planes (frontal, transverse, and sagittal) and sometimes also an oblique anterolateral plane that reveals the columellar connections with special clarity. The structure to be described was investigated in greatest detail in the ranids, but has been noted also in other anurans (all those examined thus far) in which the middle ear is fully developed. These observations show that the classical description of the anuran middle ear is seriously inadequate. The levator scapulae superior does not simply send off a branch that serves as the opercular muscle, as the usual accounts suggest. In the ear region there are three muscles that are essentially independent. These are the opercular muscle, the columellar muscle, and the levator scapulae superior, represented for Rana utricularia in Fig. 1. The opercular muscle is the one previously described under this name, but, as shown, it bears no special relation to the levator scapulae superior. It has a distinct place of origin on the anteromedial undersurface of the suprascapula, and runs directly to an insertion on the operculum. The fibers of this muscle have a certain distinctive character; they are noticeably smaller in cross section than those of the other muscles in the vicinity, they have a more translucent appearance on visual examination, and with certain histological treatments they stain differently from the others. These features make the muscle readily identifiable in serial sections. The difference in fiber size between opercular and columellar muscles is evident in Fig. 2. The columellar muscle has its place of origin on the suprascapula posterolateral to that of the opercular muscle. It runs parallel to the opercular muscle, but independent of it, to a li-
3032
Physiological Sciences: Wever
Proc. Natl. Acad. Sci. USA 76 (1979)
Otic capsule
7/ ( iluell' Hyoid process the three muscles have been representation, For clarity in specimen. a dissected FIG. 1. The middle ear region in R. utricularia, drawn from artificially separated at their upper ends. (Scale, X12.)
gamentary attachment to an extended process of the columellar footplate. The form of this attachment varies regionally from a short, blunt ligament as seen in Fig. 3 to a long, thin band as seen in Fig. 4. The levator scapulae superior has a still more posterolateral attachment on the suprascapula, and runs to the lateral surface of the otic capsule as commonly described. This muscle in R. utricularia is only a little larger than the opercular muscle and is noticeably smaller than the columellar muscle. Earlier observers evidently did not recognize the distinct character of the columellar muscle and regarded it and the levator together as one bundle. It is of interest that Eiselt (2), in one of his drawings
Otic capsule
-
Coluniella
of "the operculocolumellar apparatus" of R. ridibunda (his figure 6, plate 2), clearly portrayed two muscles in addition to the opercular muscle, but had both attached to the otic capsule and designated both as "levator scapulae superior" though one of these in his illustration definitely makes contact with the columella. The fibers of the columellar and levator muscles are of similar cross section, usually of the order of 4-6 times the size of the opercular fibers. Though these two bundles run parallel and are closely adjacent over much of their courses, they can be followed over their separate paths both in direct examination under the microscope and in serial sections. They are identified by their different terminations, and in dissection they can be separated from one another with great ease with a fine needle. The lock mechanism Both the columellar footplate and the operculum are of complex form and take a variety of appearances when sectioned. In general, the cartilaginous pars interna of the columella expands greatly within the lateral chamber of the otic capsule (see Figs. 2 and 4) and often nearly fills this cavity. A deep notch is present in this element, as shown in Fig. 4, that usually appears between C
pe rculC'I Ira>
i (}peersuIt -v
OpercUlar
II SC
If.
OpercLOEar UIIWSC^f\
C :L e d Lr
C : Li m1elI a r lliC '.'i II"
ColUrmellar rL'.LJSCle FIG. 2. The middle ear region seen in a sagittal section of a specimen of R. catesbeiana at a level at which the opercular muscle is well represented. Only a portion of the columellar muscle is shown. The ligament partially separating the two muscles belongs to the columellar muscle and at a more ventral level connects to the colu-
mella. (Scale, X10.)
t
!
Columellar muscle
FIG. 3. The relationships between operculum and columella and their muscles as seen in a section cut in an oblique anterolateral plane in a specimen of R. pipiens. Note the distinct attachment of the columellar ligament to the extended process of the columella. (Scale, X17.)
Physiological Sciences:
Proc. Natl. Acad. Sci. USA 76 (1979)
Wever
3033
Otic cavity
FIG. 4. A sagittal section in the ear region of a specimen of R. catesbeiana showing the relationships between columella, operculum, and the columellar muscle. Only a few fibers of the opercular muscle may be seen in the opercular ligament; the bulk of this muscle lies dorsal to the level shown. (Scale, X10.)
the cartilaginous pars interna and the distal portion of the more-or-less osseous pars media or sometimes (as shown here) lies within the pars interna itself. Extending into this notch is an anteriorly extended process of the lateral end of the operculum. This process fits the more posterior contours of the notch rather closely, but usually does not extend all the way into the anterior depths of the notch. Its end is attached there by a bundle of fine strands that appear to be elastic fibers. The action of this mechanism is conceived as follows. A contraction of the columellar muscle pulls the footplate in a posterior direction and holds the nosepiece of the operculum firmly in the notch. Because the operculum is attached to the otic capsule at its medial end and can only swing about an axis at this end by reason of the flexibility of the cartilage, the contraction of the columellar muscle causes the two parts to be firmly locked together, and in-and-out movements of the columella are restrained. The ligamentary band from the columellar muscle running along the posterior surface of the operculum tends to push this element anteriorly while pulling the footplate posteriorly, increasing the security of the lock. Then, contrariwise, a relaxation of the columellar muscle and a contraction of the opercular muscle pulls the opercular nosepiece
partway out of the notch and frees the columella from its restraint. Sometimes there is a double notch between operculum and columella; in addition to the condition shown in Fig. 4, there is a posterior extension of a portion of the pars interna that fits into a depression in the operculum. Thirarrangement increases further the resistance encountered by the columella in its vibratory motion whenever the columellar muscle is activated. The action described is postulated on a basis of the mechanical arrangement and can account for the variations in sensitivity found in the responses of the frog's ear to sounds, but direct physiological evidence is still to be obtained. This research was supported by a grant from the National Institutes of Health. 1. Gaupp, E. (1896) A. Ecker's & R. Wiedersheim's Anatomie des Frosches (F. Vieweg & Sohn, Braunschweig, Germany), pp. 104-105. 2. Eiselt, J. (1941) Arch. Naturges 10, 179-219. 3. De Burlet, H. M. (1926) in Handbuch der vergleichenden Anatomie der Wirbeltiere, eds. Bolk, L., Goeppert, E., Kallius, E. & Lubosch, W. (Urban & Schwarzenberg, Berlin), Vol. 2, Part 2, pp. 1381-1432.
Physiological Sciences
Middle ear muscles of the frog (amphibian ear/hearing)
ERNEST GLEN WEVER Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08544
Contributed by E. C. Wever, March 28, 1979
The anuran middle ear in its complete form includes two skeletal elements, the columella and operculum, each occupying a portion of the oval window of the otic capsule and each provided with a middle ear muscle. The two elements have an interlocking arrangement of a form that makes it possible for these muscles to exercise a high degree of control of sound transmission from tympanic membrane to inner ear receptors. From the anatomical relations it is inferred that the two muscles operate as antagonists so that contraction of the opercular muscle and relaxation of the columellar muscle leave the columella free to move in and out of the oval window in response to sound vibrations, whereas a contraction of the columellar muscle and relaxation of the opercular muscle tend to immobilize the columella and reduce the transmission inward. The frog thus achieves a degree of control of sound reception that probably is unmatched among vertebrate ears. The purpose of the middle ear mechanism is no doubt the protection of the inner ear receptors (the amphibian and basilar papillae) from overstimulation by sounds, including the animal's own cries and the intense clamor produced by a group of frogs calling in chorus. Gaupp (1) in his monumental treatment of the Anatomie des Frosches in 1896 first figured and named the opercular muscle in the anuran middle ear. He described this muscle as a derivative of the levator scapulae superior, which is a strong bundle running from the prootic region to the ventral surface of the suprascapula and serving to retract this cartilage. Gaupp was not the first to see the opercular muscle; Eiselt (2) in a thorough historical search found mention of it by Blainville as early as 1822 as a part of the shoulder musculature, and Huschke shortly thereafter spoke of this muscle as a homolog of the stapedius muscle of mammals. However, most subsequent writers on the anuran middle ear have referred to Gaupp's account and have agreed with him concerning the derivation of the muscle from the levator scapulae superior. A muscle that usually is regarded as corresponding to this one, and likewise called the opercular muscle, is present in the urodeles. However, the third Order of amphibians, the Gymnophiona or caecilians, lack this muscle along with the operculum itself. Numerous treatments of the middle ear mechanism in frogs have repeated Gaupp's descriptions of both the operculum and its muscle with little variation, but sometimes consideration has been given to the possible function of this mechanism in the hearing process. Earlier theorizing dealt extensively with this problem in urodeles, and a curious hypothesis was advanced involving the transmission of substrate vibrations through the forelegs, with the opercular muscle providing the path from shoulder region to ear. Much less attention has been given to the function of the middle ear in frogs, though it usually is assumed that the opercular muscle produces a damping of vibrations transmitted inward along the columella. De Burlet (3), in a general review of the vertebrate middle ear, offered a more ABSTRACT
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. 3031
specific suggestion for the anurans in which he compared the opercular muscle with the tensor tympani of mammals and supposed that this muscle on contraction conveys its restraints through the linkage of operculum and columella to the tympanic membrane and thus produces a flattening (and hence a stiffening) of its surface. Present observations The anatomy of the frog's middle ear has been studied in a variety of species as a part of a general examination of the ear and hearing in the amphibia. This study was stimulated by the observation of large variations in the ear's sensitivity, as measured in terms of its electrical potential in response to sounds. These variations were especially prominent in lightly anesthetized animals and at times amounted to as much as 40 db-a 100-fold variation in terms of the sound pressure required for a given electrical output. The variations continued in spite of a strict maintenance of experimental conditions, such as body temperature, the moist condition of the skin, and respiration, and pointed to the existence of some kind of internal control mechanism. Observations were made both by dissection under the binocular microscope and by the use of serial sections. The sectioning used the three standard planes (frontal, transverse, and sagittal) and sometimes also an oblique anterolateral plane that reveals the columellar connections with special clarity. The structure to be described was investigated in greatest detail in the ranids, but has been noted also in other anurans (all those examined thus far) in which the middle ear is fully developed. These observations show that the classical description of the anuran middle ear is seriously inadequate. The levator scapulae superior does not simply send off a branch that serves as the opercular muscle, as the usual accounts suggest. In the ear region there are three muscles that are essentially independent. These are the opercular muscle, the columellar muscle, and the levator scapulae superior, represented for Rana utricularia in Fig. 1. The opercular muscle is the one previously described under this name, but, as shown, it bears no special relation to the levator scapulae superior. It has a distinct place of origin on the anteromedial undersurface of the suprascapula, and runs directly to an insertion on the operculum. The fibers of this muscle have a certain distinctive character; they are noticeably smaller in cross section than those of the other muscles in the vicinity, they have a more translucent appearance on visual examination, and with certain histological treatments they stain differently from the others. These features make the muscle readily identifiable in serial sections. The difference in fiber size between opercular and columellar muscles is evident in Fig. 2. The columellar muscle has its place of origin on the suprascapula posterolateral to that of the opercular muscle. It runs parallel to the opercular muscle, but independent of it, to a li-
3032
Physiological Sciences: Wever
Proc. Natl. Acad. Sci. USA 76 (1979)
Otic capsule
7/ ( iluell' Hyoid process the three muscles have been representation, For clarity in specimen. a dissected FIG. 1. The middle ear region in R. utricularia, drawn from artificially separated at their upper ends. (Scale, X12.)
gamentary attachment to an extended process of the columellar footplate. The form of this attachment varies regionally from a short, blunt ligament as seen in Fig. 3 to a long, thin band as seen in Fig. 4. The levator scapulae superior has a still more posterolateral attachment on the suprascapula, and runs to the lateral surface of the otic capsule as commonly described. This muscle in R. utricularia is only a little larger than the opercular muscle and is noticeably smaller than the columellar muscle. Earlier observers evidently did not recognize the distinct character of the columellar muscle and regarded it and the levator together as one bundle. It is of interest that Eiselt (2), in one of his drawings
Otic capsule
-
Coluniella
of "the operculocolumellar apparatus" of R. ridibunda (his figure 6, plate 2), clearly portrayed two muscles in addition to the opercular muscle, but had both attached to the otic capsule and designated both as "levator scapulae superior" though one of these in his illustration definitely makes contact with the columella. The fibers of the columellar and levator muscles are of similar cross section, usually of the order of 4-6 times the size of the opercular fibers. Though these two bundles run parallel and are closely adjacent over much of their courses, they can be followed over their separate paths both in direct examination under the microscope and in serial sections. They are identified by their different terminations, and in dissection they can be separated from one another with great ease with a fine needle. The lock mechanism Both the columellar footplate and the operculum are of complex form and take a variety of appearances when sectioned. In general, the cartilaginous pars interna of the columella expands greatly within the lateral chamber of the otic capsule (see Figs. 2 and 4) and often nearly fills this cavity. A deep notch is present in this element, as shown in Fig. 4, that usually appears between C
pe rculC'I Ira>
i (}peersuIt -v
OpercUlar
II SC
If.
OpercLOEar UIIWSC^f\
C :L e d Lr
C : Li m1elI a r lliC '.'i II"
ColUrmellar rL'.LJSCle FIG. 2. The middle ear region seen in a sagittal section of a specimen of R. catesbeiana at a level at which the opercular muscle is well represented. Only a portion of the columellar muscle is shown. The ligament partially separating the two muscles belongs to the columellar muscle and at a more ventral level connects to the colu-
mella. (Scale, X10.)
t
!
Columellar muscle
FIG. 3. The relationships between operculum and columella and their muscles as seen in a section cut in an oblique anterolateral plane in a specimen of R. pipiens. Note the distinct attachment of the columellar ligament to the extended process of the columella. (Scale, X17.)
Physiological Sciences:
Proc. Natl. Acad. Sci. USA 76 (1979)
Wever
3033
Otic cavity
FIG. 4. A sagittal section in the ear region of a specimen of R. catesbeiana showing the relationships between columella, operculum, and the columellar muscle. Only a few fibers of the opercular muscle may be seen in the opercular ligament; the bulk of this muscle lies dorsal to the level shown. (Scale, X10.)
the cartilaginous pars interna and the distal portion of the more-or-less osseous pars media or sometimes (as shown here) lies within the pars interna itself. Extending into this notch is an anteriorly extended process of the lateral end of the operculum. This process fits the more posterior contours of the notch rather closely, but usually does not extend all the way into the anterior depths of the notch. Its end is attached there by a bundle of fine strands that appear to be elastic fibers. The action of this mechanism is conceived as follows. A contraction of the columellar muscle pulls the footplate in a posterior direction and holds the nosepiece of the operculum firmly in the notch. Because the operculum is attached to the otic capsule at its medial end and can only swing about an axis at this end by reason of the flexibility of the cartilage, the contraction of the columellar muscle causes the two parts to be firmly locked together, and in-and-out movements of the columella are restrained. The ligamentary band from the columellar muscle running along the posterior surface of the operculum tends to push this element anteriorly while pulling the footplate posteriorly, increasing the security of the lock. Then, contrariwise, a relaxation of the columellar muscle and a contraction of the opercular muscle pulls the opercular nosepiece
partway out of the notch and frees the columella from its restraint. Sometimes there is a double notch between operculum and columella; in addition to the condition shown in Fig. 4, there is a posterior extension of a portion of the pars interna that fits into a depression in the operculum. Thirarrangement increases further the resistance encountered by the columella in its vibratory motion whenever the columellar muscle is activated. The action described is postulated on a basis of the mechanical arrangement and can account for the variations in sensitivity found in the responses of the frog's ear to sounds, but direct physiological evidence is still to be obtained. This research was supported by a grant from the National Institutes of Health. 1. Gaupp, E. (1896) A. Ecker's & R. Wiedersheim's Anatomie des Frosches (F. Vieweg & Sohn, Braunschweig, Germany), pp. 104-105. 2. Eiselt, J. (1941) Arch. Naturges 10, 179-219. 3. De Burlet, H. M. (1926) in Handbuch der vergleichenden Anatomie der Wirbeltiere, eds. Bolk, L., Goeppert, E., Kallius, E. & Lubosch, W. (Urban & Schwarzenberg, Berlin), Vol. 2, Part 2, pp. 1381-1432.
