Vibrometric studies of the middle ear of the bullfrog Rana catesbeiana II. The operculum
Department of Physiological Science, UCLA, 405 Hilgard Avenue, Los Angeles, CA 90095, USA
* Author for correspondence at present address: Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK (e-mail: mjm68{at}hermes.cam.ac.uk)
Accepted 15 July 2002
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Summary |
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Key words: middle ear, bullfrog, Rana catesbeiana, laser Doppler vibrometry, operculum, stapes, hearing
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Introduction |
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The function of the operculum has intrigued biologists for many years.
Hypotheses have included a kinaesthetic role
(Eiselt, 1941;
Baker, 1969
), a means of
modulating the impedance of the middle ear apparatus
(Lombard and Straughan, 1974
)
and a protective mechanism to restrain the movement of the footplate (Wever,
1979
,
1985
). In recent years, a
refined version of the older idea that the operculum is used in the detection
of groundborne vibrations by means of its muscular attachment to the pectoral
girdle (Kingsbury and Reed,
1909
) has gained prominence (Hetherington,
1985
,
1987a
,
1988
;
Hetherington et al., 1986
).
According to this hypothesis, low-frequency movements of the head relative to
the scapula are translated by an opercularis muscle in sustained contraction
into movements of the operculum relative to the skull (Hetherington,
1985
,
1987a
,
1988
). It is proposed that the
resulting pressure wave within the inner ear stimulates low-frequency,
vibration-sensitive receptors such as those in the saccular or lagenar maculae
(see Hetherington, 1985
,
1988
;
Hetherington et al., 1986
). As
part of this hypothesis, it is argued that the tympanic system and the
opercularis system are functionally independent
(Hetherington et al., 1986
;
Jaslow et al., 1988
;
Hetherington, 1992
).
In the present study, laser Doppler interferometry was used to record vibrations of both the operculum and stapes of the bullfrog in response to airborne sound, to examine the hypothesis that the stapes footplate and operculum are functionally independent. This is apparently the first time that direct measurements of opercular movement have been reported.
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Materials and methods |
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Since the methodology for the laser measurements is described in detail in
the companion paper (Mason and Narins,
2002), only a brief account is presented here. The surgery used to
expose the left stapes footplate and operculum from a dorsal approach allowed
access to these structures without breaching the middle ear cavity and without
damaging the opercularis muscle. The borders of the triangular area of the
operculum visible following this surgery are delineated by the articulation
with the stapes footplate rostrally, with the opercularis muscle ventrally and
caudally and with the otic capsule dorsally. Up to five reflective glass beads
(Polytec) were placed within this exposed region of the operculum, according
to the experiment. Beads were also placed on the stapes footplate, parotic
crest and tympanic membrane, as described by Mason and Narins
(2002
). The velocity of the
parotic crest, part of the otic region of the skull of the frog, was
considered to represent the velocity of the otic capsule and was used as a
control for the vibrations of stapes and operculum
(Mason and Narins, 2002
).
Small sponge blocks were positioned under the pectoral girdle and snout of
the anaesthetised frog to prop it in a sitting position. The frog was then
placed on a vibration-isolated table (Backer-Loring Micro-g) within a
double-walled sound-attenuating chamber (IAC 1202-A). There, it was exposed to
free-field pure tones from 180 to 3 kHz, calibrated to be 90 dB SPL at the
left tympanic membrane. The speaker producing the tones was resting on a
separate table. A laser interferometer (Polytec OFV-303 sensor head connected
to an OFV-3001 controller) was used to measure the vibration velocities of the
reflective beads, which were assumed to be equal to the velocities of the
structures upon which they were placed. The measurements recorded from the
tympanic membrane were obtained with the laser head tilted downwards at
approximately 25° to the horizontal. The velocity component measured at
this angle is typically within 2 dB of the true velocity of the tympanic
membrane (Mason and Narins,
2002). The vertical components of the velocities of the other
structures were measured by deflecting the laser beam through a prism mounted
in the barrel of a microscope (Zeiss OP-1) positioned above the frog. A
custom-designed program (Acoustic Analyzer 0.20ß: A. Purgue, 1999),
running on an Apple Macintosh iMac computer, was used to generate and adjust
the output sent to the speaker, to record the amplitude of the laser
vibrometer output and to measure the phase of the returning vibrometer signal
relative to the signal returning from the speaker. The sampling frequency was
44.1 kHz. Comparisons of the tympanic membrane responses obtained at the
beginning and at the end of the experiments were made as controls to ensure
that the response of the tympanic membrane remained approximately constant.
Most runs were repeated three times and averaged; reported velocity amplitudes
are peak values. Data from one male frog were rejected since the tympanic
membrane was clearly drying.
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Results |
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The similarities between the stapes footplate and operculum velocity
responses suggest that the structures are coupled. However, movements of the
operculum could also be caused by sound impinging on the exposed opercular
surface directly or via vibrations of the suprascapular cartilage,
conveyed to the operculum by means of the opercularis muscle
(Hetherington, 1988). To
examine these possibilities, the same frog as represented in
Fig. 2 was removed from the
sound-attenuating chamber, and the extrastapes was excised using iris scissors
inserted through the wide Eustachian tube. The frog was repositioned, and the
responses of the operculum and stapes were then remeasured
(Fig. 3). As expected, the
velocity amplitude of the stapes footplate, uncoupled from the tympanic
membrane, now matches the `background' response of the parotic crest
(Fig. 3A). The response of the
operculum also falls to match that of the parotic crest. The footplate no
longer shows a consistent phase relationship with the tympanic membrane, but
the footplate and operculum still vibrate in phase
(Fig. 3B). This experiment was
performed on seven frogs. The responses of stapes footplate and operculum
always dropped dramatically as a result of the excision of the extrastapes. In
one animal, the responses of both structures remained clearly above the
parotic crest response between 600 and 750 Hz, a frequency range at which
tympanic membrane vibration was near-maximal. This could have been due to a
residual mucosal connection or blood clot between the tympanic membrane and
pars media, offering a means of coupling.
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The measured operculum (or footplate) response is a combination of the
opercular (or footplate) response relative to the otic capsule added to the
`background' vibration of the otic capsule itself. Because the relative
response is presumably the effective input to the inner ear, the parotic crest
response, taken to represent otic capsule vibration, was subtracted from the
responses of both operculum and stapes footplate (for more details, see
Mason and Narins, 2002). The
operculum and footplate responses presented in Figs
4 and
5 have been so adjusted.
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The rotatory axes of the stapes and operculum
Fig. 4 illustrates the
results of an experiment in which two beads were placed on the stapes
footplate and two on the operculum, in both cases arranged with one bead
medial and one lateral. The more medial bead on the stapes footplate
(Fig. 4A, red trace) has a
higher velocity amplitude than the more lateral bead (pink trace), consistent
with a footplate rotatory axis lateral to the footplate. However, the converse
is true of the operculum: the more lateral bead in this case
(Fig. 4A, orange trace) has a
higher velocity amplitude than the more medial bead (dark brown trace),
consistent with an opercular rotatory axis medial to the operculum. At
frequencies of above 2 kHz, the responses of both structures fall into the
noise. The phase differences between the two footplate beads and between the
two operculum beads remain very close to zero across a wide frequency range
(Fig. 4B), and the relative
amplitudes remain constant, indicating that these structures were not bending
between the points of measurement.
Measurements were also made from different positions arranged rostrocaudally on the operculum: a typical experiment is shown in Fig. 5, in which responses from rostral, middle and caudal opercular beads are represented as orange, red and dark brown traces, respectively. The velocity amplitude of the operculum is similar in all three measurement positions. However, the relative amplitudes at the three measurement positions change slightly with frequency, and there are phase differences between the velocities recorded from the three positions (Fig. 5B). This suggests that the movement of the operculum is not as simple as that of a stiff plate rotating about a fixed, linear axis.
Experiments in which more than one bead was placed on the stapes were performed on five animals, with consistent results. Experiments in which more than one bead was placed on the operculum were performed on 16 frogs. In these cases, results from different animals were more variable, probably as a result of different bead positions, but showed some consistent trends: lateral positions on the operculum have a higher amplitude of vibration than medial positions; and positions near the stapes footplate vibrate in phase with the footplate and tend to have a slightly higher velocity amplitude than more caudal positions.
The opercular rotatory axis was taken to pass along the medial edge of the
operculum. The angle between a line perpendicular to the axis and passing
through the reflective bead on the operculum and the horizontal plane was
estimated to be 20° in both sexes. The small amount of curvature of the
operculum results in a slightly different angle for each bead, but this was
considered negligible. The corresponding angle between the stapes footplate
bead, the footplate rotatory axis and the horizontal was taken to average
57° in males and 48° in females
(Mason and Narins, 2002).
Since only the vertical component of vibration of the stapes and operculum was
measured in this study, the measured velocity amplitudes must be divided by
the consines of these angles to estimate the true velocity at each point of
measurement. This angular adjustment was taken into account in Figs
4 and
5.
Anatomical observations
In anatomical dissections, positive pressure applied to the outside of the
tympanic membrane can be seen to result in downward movement of the shaft of
the stapes. The footplate articulates with the otic capsule by means of a
ridge of the pars media (Fig.
1B), and the footplate rotates about this articulation as the
shaft moves ventrally. The resulting lever arrangement means that the
footplate moves outwards as the tympanic membrane moves inwards. As the
footplate moves outwards, the operculum can also be seen to move outwards,
rotating about its dorsomedial border (see
Fig. 6), but with a smaller
amplitude than the footplate.
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Coupling between the footplate and operculum in the bullfrog is the result
of several anatomical features. A robust flange of the cartilaginous pars
interna extends underneath the rostral third of the operculum
(Fig. 1B; see also
figure 1 of
Lombard and Straughan, 1974).
The operculum is often described as fitting into a notch in the stapes
footplate (Wever, 1979
,
1985
;
Hetherington et al., 1986
;
Hetherington, 1987b
). This
probably refers to the space between the flange and the caudal process of the
pars media, which would appear as a notch in serial sections. A ligamentous
band extends from the rostroventral border of the operculum between the pars
interna and pars media of the stapes. Elastic tissue also extends between the
pars interna and operculum at their articulation. The oval window is covered
over laterally by a thick, fibrous membrane, which adheres to the internal
surfaces of both the pars interna and operculum. These various ligamentous
connections are strong enough that the footplate and operculum may readily be
removed from the oval window still in articulation with each other.
The caudal process of the pars media of the stapes
(Fig. 1) represents the point
of attachment of a tough, ligamentous sheet that runs along the ventral rim of
the oval window lateral to the operculum. This sheet forms an aponeurosis for
the insertion of the m. levator scapulae superior, part of which is considered
to be a discrete columellar muscle (Wever,
1979,
1985
). The bony protuberance,
being on the rotatory axis, would appear to represent the least efficient
insertion point for a muscle functioning to influence the vibrations of the
stapes. The intervention of the aponeurosis would also appear to transmit much
of the tension applied by the muscle to the rim of the oval window rather than
to the footplate. The columellar muscle described by Wever
(1979
,
1985
) is not considered to
exist as a discrete functional entity in most frogs
(Hetherington and Lombard,
1983
; Hetherington et al.,
1986
; Hetherington,
1987b
), including the bullfrog
(Hetherington and Lombard,
1983
), and this view is shared by the current authors.
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Discussion |
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Experimental data suggest that the operculum is tightly coupled to the
footplate rostrally, although the operculum may be forced to bend a little
more caudally to accommodate footplate movement. The coupling between the
stapes and operculum is contrary to the interpretation of Hetherington et al.
(1986) and Jaslow et al.
(1988
), who state that the
difference in hinge position allows these structures to move independently.
Wever (1973
) argues that, if
the operculum were free to move in the oval window in response to acoustic
pressures within the lateral chamber of the inner ear (caused by stapes
footplate movement), this would represent an acoustic bypass, impairing
transmission of sound to the inner ear proper. He felt that the presence of
such an apparently maladaptive bypass is unlikely. The bypass hypothesis
demands that the operculum move out of phase with the footplate, which is not
the case. The in-phase movement of the rostral operculum and footplate is
expected to minimise this shunting effect, and it also implies that the
operculum will contribute to the total volume velocity at the oval window.
For each frog, the highest measured opercular velocity amplitude, always near the stapes footplate, was subtracted from the highest measured footplate amplitude. When velocity component angle was taken into account, opercular amplitudes were found to be, on average, 11.6 dB below those of the stapes footplate at frequencies below 2 kHz (21 frogs). No sex differences were apparent. The distance from this opercular measurement position to the opercular axis was typically approximately half the distance from the footplate measurement position to the footplate axis. This suggests that the angular velocity of the rostral operculum is, on average, 5.6 dB below that of the stapes footplate and that the coupling between the otic elements therefore operates as a lever.
To estimate the contribution of the operculum to the volume velocity at the oval window, scale diagrams of the stapes and operculum in articulation were prepared for five frogs. In each case, the position of the rotatory axis of the footplate was estimated, and the diagram was divided into 40-60 thin sections, each parallel to this axis. Assuming that the footplate rotates about this fixed axis as a stiff plate, the volume displacement of one of the thin sections will be proportional to the area of that section multiplied by its distance from the axis of rotation. The total volume displacement is approximated by the sum of the volume displacements of the sections. The volume displacement of the operculum was calculated in a similar way, except that only the area of the operculum not overlapped by the footplate flange was included. The lever effect between the footplate and operculum was taken into account by multiplying opercular volume velocity by 0.52 (-5.6 dB). Using this methodology, the operculum was calculated to contribute, on average, 19% (range 13-26%) of the total volume velocity at the oval window (volume velocity is proportional to volume displacement). Bearing in mind that the operculum seems to bend rather than to move as a rigid plate, its actual contribution will be somewhat smaller than this.
If the role of the operculum is merely to contribute a small amount to the
volume velocity at the inner ear, then what would be the adaptive advantage of
two elements separated by an articulation, which would inevitably introduce
frictional losses into the system, over simply having a stapes footplate of
greater area? The relative orientations of the opercularis muscle and
opercular hinge are such that the muscle can exert maximum leverage on the
operculum (Hetherington et al.,
1986). This demands a dorsomedial axis of rotation, rather than
ventrolateral as for the footplate, which suggests that the explanation for
the complicated system might involve the opercularis muscle. Several
hypotheses regarding the function of the opercularis system are reconsidered
here in the light of the new evidence from the present study.
The operculum and airborne sound transmission
Lombard and Straughan
(1974) found that severing or
denervating the opercularis muscle of certain hylid and leptodactylid frogs
decreased midbrain neural responses to airborne sound by up to 20-30 dB at
frequencies below 1000 Hz. These authors suggested that contraction of the m.
opercularis would lock the stapes and operculum together, increasing the mass
and stiffness of the middle ear apparatus and decreasing the area ratio
between the tympanic membrane and oval window. Wever
(1979
,
1985
) proposed that
contraction of the muscle actually decouples the stapes and operculum: the
opposite of Lombard and Straughan's interpretation. The results of the present
study show that the stapes and operculum of the bullfrog are coupled when the
frog is anaesthetised and the m. opercularis is presumably under no more than
passive tension, suggesting that Wever's hypothesis is more likely to be
correct. The middle ear seems to be important in both terrestrial and
underwater hearing in bullfrogs
(Hetherington and Lombard,
1982
), and the opercularis muscle may be in a state of sustained
contraction when the frog is out of water
(Hetherington and Lombard,
1983
). A mechanism to change the impedance-matching properties of
the middle ear between aquatic and terrestrial situations might well be
advantageous (Lombard et al.,
1981
) and demands further investigation.
`Extratympanic' transmission of airborne sound to the inner ear is the term
given to transmission by routes other than via the tympanic membrane
(Wilczynski et al., 1987).
Extratympanic transmission is more effective than tympanic transmission at
frequencies below 300 Hz in Rana pipiens and contributes
significantly to overall sound transmission at frequencies up to 1.0-1.2 kHz
(Wilczynski et al., 1987
). The
operculum has been implicated as a possible mechanism for extratympanic
transmission by means of its muscular connection to a vibrating suprascapula
or through its inertia alone (Hetherington,
1985
,
1987a
,
1988
,
1992
;
Jaslow et al., 1988
).
Wilczynski et al. (1987
)
anaesthetised or immobilised their frogs, and even positioned them on their
backs, in their experiments in which the effectiveness of extratympanic
transmission was demonstrated, suggesting that extratympanic transmission does
not depend on a tensed opercularis muscle. Indeed, microphonic response
amplitude to low-frequency airborne sound decreases by only a few decibels on
removal of the muscle in the bullfrog
(Paton, 1971
, cited in
Hetherington, 1989
;
Hetherington, 1989
); a far
smaller effect than that observed by Lombard and Straughan
(1974
) in their hylid and
leptodactylid specimens. In the present study, the response of the operculum
dropped considerably and was very close to the background skull response when
the extrastapes was severed, even at low frequencies. These findings argue
against an important role for the opercularis system in extratympanic airborne
sound transmission in Rana species, at least within the frequency
range considered here.
The operculum and seismic sensitivity
The hypothesis that the opercularis system is used in the detection of very
low-frequency seismic vibrations was not directly addressed in this study.
However, the notion that the footplate and operculum move independently within
the oval window (Hetherington et al.,
1986; Hetherington,
1988
,
1992
) needs to be revised. The
foramen leading from the lateral chamber to the inner ear proper in the
bullfrog is small (mean area 0.577 mm2, N=56 left ears;
this study) and is located directly underneath the operculum. This leaves no
obvious opportunity for stapes and operculum vibrations to be channelled along
different pathways to separate end-organs. Different inputs to the footplate
and operculum will also interfere with each other as a result of their
coupling. It is difficult to see how the frog would be able to identify the
modality of the resulting vibrations passed to the inner ear. However, if the
opercularis system works only to transmit seismic vibrations of very low
frequency, whereas the tympanic system transmits higher-frequency airborne
sound, it could be that the lowest frequencies reaching the inner ear of the
frog are always interpreted as being of seismic origin.
The opercularis system as a protective mechanism
Wever (1979,
1985
) believed that the
operculum is decoupled from the stapes footplate when the opercularis muscle
is contracted and the columellar muscle relaxed, the footplate then being free
to move in response to airborne sound. When the opercularis muscle is relaxed
and the columellar muscle contracted, Wever argued that the stapes footplate
and operculum would become locked together, thus reducing stapes footplate
vibration and acting as a protective mechanism, for instance when the frog was
calling. Wever (1985
) states
that, when tension was applied to each of these muscles in turn, the
electrical responses of the inner ear to airborne sound were altered in the
way predicted by his hypothesis, although the results of sectioning or
anaesthetising the muscles were more variable. The columellar muscle is not
present in the bullfrog (Hetherington and
Lombard, 1983
; this study), and the opercularis muscle of anurans
is primarily a tonic muscle, adapted for slow, sustained contraction rather
than for a fast, reflex response (Becker
and Lombard, 1977
;
Hetherington, 1987a
).
Contraction of the opercularis muscle does not seem to affect the response of
the tympanic membrane (Hetherington,
1994
). A protective role for the opercularis muscle analogous to
the stapedius reflex in mammals has therefore been considered unlikely
(Hetherington, 1987a
,
1994
).
To force air into its lungs, a frog (which lacks diaphragm and ribs)
increases the pressure in its buccal cavity and opens its glottis
(Gans et al., 1969;
de Jongh and Gans, 1969
). In
bullfrogs, contractions of the opercularis muscle are associated with this
force-pump phase of ventilation, both when on land and when floating in water
with just the nostrils above the surface
(Hetherington and Lombard,
1983
). Contractions are not associated with the more regular
buccal cycles that exchange air within the buccal cavity only. Ventilation
rate, and associated opercularis contraction, may decrease from once per
second to as little as once every 10 s in a relaxed frog and may even be
halted if the frog is startled
(Hetherington and Lombard,
1983
). However, it is argued that the association between
opercularis contraction and breathing could maintain the muscle in a state of
constant tension (Hetherington and
Lombard, 1983
; Hetherington,
1987a
) and may represent an `evolutionarily convenient' way of
coupling this sustained tension to (mostly) terrestrial situations in which
the feet are in contact with the substratum
(Hetherington and Lombard,
1983
).
The buccal cavity of the frog is in free communication with the middle ear
cavity by means of the wide and permanently patent Eustachian tubes. The
pressure in the middle ear cavity therefore rises with the high buccal
pressure during ventilation, and the tympanic membranes bulge outwards
(Hetherington and Lombard,
1983; Jørgensen et al.,
1991
; Narins,
1992
; Narins et al.,
2001
). In male bullfrogs, part of the vocalisation is broadcast
from the tympanic membranes, and pressure in the buccal cavity also rises
during these events (Purgue,
1997
). This pressure increase again results in bulging of the
tympanic membranes: membrane displacements of approximately 0.2 mm have been
measured, similar to the mean displacements associated with breathing (A.
Purgue, unpublished observations in Purgue
and Narins, 2000a
). Since the stapes footplate moves 180° out
of phase with the tympanic membrane at low frequencies
(Jørgensen and Kanneworff,
1998
; Mason and Narins,
2002
; this study), the footplate will tend to be forced into the
inner ear when the tympanic membrane bulges outwards (Purgue and Narins,
2000a
,b
)
with an amplitude orders of magnitude greater than during airborne audition.
Bulging may stiffen the membrane and thus reduce its response
(Jaslow et al., 1988
;
Narins, 1992
). The massive
central patch of the male bullfrog tympanic membrane has a reduced vibratory
response at higher frequencies due to its inertia, and this is seen as a means
of decoupling the tympanic membrane vibration from the extrastapes during
vocalisation (Purgue, 1997
).
These protective mechanisms may help to reduce the vibration transferred to
the stapes, but they do not address the quasi-static (very low frequency)
displacement of the stapes caused by bulging of the tympanic membranes (onto
which the higher-frequency vocalisation vibration may be superimposed).
High-amplitude pressure changes within the inner ear, as caused by
quasi-static displacement of middle ear ossicles, are believed to be
potentially damaging (Wever,
1979
; Purgue and Narins,
2000a
,b
).
Adaptations to resist quasi-static pressure changes in the mammalian middle
ear from displacing the ossicles too far may include the compliant pars
flaccida of the tympanic membrane, flexible articulations between the
ossicles, the middle ear muscles and certain tethering ligaments
(Stenfors et al., 1979
;
Cancura, 1980
;
Marquet, 1981
;
Hüttenbrink, 1988
;
Dirckx et al., 1998
). In frogs,
flexibility both between the tympanic membrane and extrastapes and between the
extrastapes and pars media might help to reduce the displacement of the
footplate during breathing and vocalisation
(Mason and Narins, 2002
). In
addition, a fluid bypass pathway within the inner ear of amphibians is
expected to divert high-amplitude, low-frequency pressure waves away from the
sensory papillae (Smith, 1968
;
Purgue and Narins,
2000a
,b
).
We propose here that the opercularis system might mediate another
protective mechanism in the bullfrog, and that the link between opercularis
contraction and breathing (Hetherington
and Lombard, 1983) may be a direct rather than an indirect one. If
operculum and footplate remain coupled, tension in the opercularis muscle
could help to resist the stapes footplate from being forced into the inner ear
during breathing and vocalisation. Alternatively, if the elements are
decoupled during opercularis contraction, the increase in fluid pressure
induced by the stapes being forced into the lateral chamber will be reduced by
the operculum being both pulled outwards by the muscle and pushed outwards by
the fluid pressure itself. This shunting effect, representing Wever's
(1973
) `acoustic by-pass',
would serve to reduce the net displacement of fluid from the lateral chamber
into the inner ear proper. In dissections, pulling on the opercularis muscle
moves both the operculum and stapes footplate outwards (M. J. Mason and P. M.
Narins, personal observation), as predicted by the first hypothesis. Both
hypotheses demand a slow contraction of the opercularis muscle concomitant
with the increase in middle ear pressure, a function for which the
physiological properties of the muscle
(Becker and Lombard, 1977
;
Hetherington, 1987a
) seem
appropriate.
The operculum in other amphibians
Some amphibians, including urodeles and certain frogs such as
Bombina species, lack both a tympanic membrane and a middle ear
cavity but retain an opercularis system (Hetherington,
1987b,
1992
;
Jaslow et al., 1988
; M. J.
Mason and P. M. Narins, personal observation). The opercularis system in these
animals clearly cannot have the same protective function proposed here for
bullfrogs. In the salamander Ambystoma tigrinum, severing the
opercularis muscle caused a small reduction in auditory responses to airborne
sound at frequencies up to 3 kHz, suggesting that the opercularis system has a
role in sound reception in this species
(Hetherington, 1989
). However,
on the basis of experiments in which tension was put on the muscle, Wever
(1985
) argued that the
opercularis system has a protective function whereby muscular contraction
reduces responses to airborne sound. The experimental evidence therefore seems
inconclusive.
When the operculum of salamanders is moved inwards, perilymphatic fluid is
pushed through the perilymphatic foramen from the otic capsule to the cranial
cavity (Smith, 1968;
Ross and Smith, 1982
). Flexing
the head downwards relative to the spine results in fluid movements in the
opposite direction (Smith,
1968
). Evidence suggests that acoustic vibrations may also pass
between the ears and cranial cavity
(Wever, 1978
). In frogs,
pressure waves conducted from the vertebral canal to the inner ear have been
implicated as potentially mediating extratympanic airborne hearing
(Narins et al., 1988
). Since
the head moves relative to the body when a bullfrog is exposed to ground
vibrations (Hetherington,
1988
), this could represent an alternative means of seismic
detection. The opercularis system might conceivably have a protective role in
reducing large pressure changes in the inner ear fluids induced by relative
movement of the skull and spine during ambulatory or ventilatory movements in
amphibians with or without tympanic ears.
We contend that the role or roles of the opercularis system are far from clear and are not necessarily the same in all amphibians. Direct measurements of opercular and footplate motion with the opercularis muscle in different states of contraction, and in response to seismic vibration as well as airborne sound, would be a useful direction for future study.
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Acknowledgments |
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Baker, M. C. (1969). The effect of severing the opercularis muscle on body orientation of the leopard frog, Rana pipiens.Copeia 1969,613 -616.
Becker, R. P. and Lombard, R. E. (1977). Structural correlates of function in the `opercularis' muscle of amphibians. Cell Tissue Res. 175,499 -522.[Medline]
Bolt, J. R. and Lombard, R. E. (1985). Evolution of the amphibian tympanic ear and the origin of frogs. Biol. J. Linn. Soc. 24,83 -99.
Cancura, W. (1980). On the statics of malleus and incus and on the function of the malleusincus joint. Acta Oto-Laryngol. 89,342 -344.[Medline]
de Jongh, H. J. and Gans, C. (1969). On the mechanism of respiration in the bullfrog, Rana catesbeiana: a reassessment. J. Morphol. 127,259 -290.
Dirckx, J. J. J., Decraemer, W. F., Unge, von M. and Larsson, C. (1998). Volume displacement of the gerbil eardrum pars flaccida as a function of middle ear pressure. Hear. Res. 118,35 -46.[Medline]
Eiselt, J. (1941). Der Musculus opercularis und die mittlere Ohrsphäre der anuren Amphibien. Arch. Naturgesch. 10,179 -230.
Gans, C., de Jongh, H. J. and Farber, J. (1969). Bullfrog (Rana catesbeiana) ventilation: how does the frog breathe? Science 163,1223 -1225.[Medline]
Hetherington, T. E. (1985). Role of the opercularis muscle in seismic sensitivity in the bullfrog Rana catesbeiana. J. Exp. Zool. 235, 27-43.[Medline]
Hetherington, T. E. (1987a). Physiological features of the opercularis muscle and their effects on vibration sensitivity in the bullfrog Rana catesbeiana. J. Exp. Biol. 131,189 -204.[Abstract]
Hetherington, T. E. (1987b). Timing of development of the middle ear of Anura (Amphibia). Zoomorphology 106,289 -300.
Hetherington, T. E. (1988). Biomechanics of vibration reception in the bullfrog, Rana catesbeiana. J. Comp. Physiol. A 163,43 -52.[Medline]
Hetherington, T. E. (1989). Effect of the amphibian opercularis muscle on auditory responses. Prog. Zool. 35,356 -359.
Hetherington, T. E. (1992). The effects of body size on the evolution of the amphibian middle ear. In The Evolutionary Biology of Hearing (ed. D.B. Webster, R.R. Fay and A.N. Popper), pp. 421-437. New York: Springer-Verlag.
Hetherington, T. E. (1994). The middle ear muscle of frogs does not modulate tympanic responses to sound. J. Acoust. Soc. Am. 95,2122 -2125.[Medline]
Hetherington, T. E., Jaslow, A. P. and Lombard, R. E. (1986). Comparative morphology of the amphibian opercularis system. I. General design features and functional interpretation. J. Morphol. 190,43 -61.[Medline]
Hetherington, T. E. and Lombard, R. E. (1982). Biophysics of underwater hearing in anuran amphibians. J. Exp. Biol. 98,49 -66.[Abstract]
Hetherington, T. E. and Lombard, R. E. (1983). Electromyography of the opercularis muscle of Rana catesbeiana: an amphibian tonic muscle. J. Morphol. 175, 17-26.[Medline]
Hüttenbrink, K. B. (1988). The mechanics of the middle-ear at static air pressures: the role of the ossicular joints, the function of the middle-ear muscles and the behaviour of stapedial prostheses. Acta Oto-Laryngol. Suppl. 451,1 -35.
Jaslow, A. P., Hetherington, T. E. and Lombard, R. E. (1988). Structure and function of the amphibian middle ear. In The Evolution of the Amphibian Auditory System (ed. B. Fritzsch, M.J. Ryan, W. Wilczynski, T.E. Hetherington and W. Walkowiak), pp.69 -91. New York: John Wiley & Sons.
Jørgensen, M. B. and Kanneworff, M. (1998). Middle ear transmission in the grass frog, Rana temporaria. J. Comp. Physiol. A 182, 59-64.[Medline]
Jørgensen, M. B., Schmitz, B. and Christensen-Dalsgaard, J. (1991). Biophysics of directional hearing in the frog Eleutherodactylus coqui. J. Comp. Physiol. A 168,223 -232.
Kingsbury, B. F. and Reed, H. D. (1909). The columella auris in Amphibia. J. Morphol. 20,549 -627.
Lombard, R. E., Fay, R. R. and Werner, Y. L. (1981). Underwater hearing in the frog, Rana catesbeiana.J. Exp. Biol. 91,57 -71.
Lombard, R. E. and Straughan, I. R. (1974). Functional aspects of anuran middle ear structures. J. Exp. Biol. 61,71 -93.[Medline]
Marquet, J. (1981). The incudo-malleal joint. J. Laryngol. Otol. 95,543 -565.[Medline]
Mason, M. J. and Narins, P. M. (2002).
Vibrometric studies of the middle ear of the bullfrog Rana
catesbeiana. I. The extrastapes. J. Exp. Biol.
205,3153
-3165.
Narins, P. M. (1992). Reduction of tympanic membrane displacement during vocalization of the arboreal frog, Eleutherodactylus coqui. J. Acoust. Soc. Am. 91,3551 -3557.[Medline]
Narins, P. M., Ehret, G. and Tautz, J. (1988). Accessory pathway for sound transfer in a neotropical frog. Proc. Natl. Acad. Sci. U.S.A. 85,1508 -1512.[Abstract]
Narins, P. M., Lewis, E. R., Purgue, A. P., Bishop, P. J.,
Minter, L. R. and Lawson, D. P. (2001). Functional
consequences of a novel middle ear adaptation in the central African frog
Petropedetes parkeri (Ranidae). J. Exp. Biol.
204,1223
-1232.
Paton, J. A. (1971). Microphonic potentials in the inner ear of the bullfrog. Master's dissertation, Cornell University.
Purgue, A. P. (1997). Tympanic sound radiation in the bullfrog Rana catesbeiana. J. Comp. Physiol. A 181,438 -445.[Medline]
Purgue, A. P. and Narins, P. M. (2000a). Mechanics of the inner ear of the bullfrog (Rana catesbeiana): the contact membranes and the periotic canal. J. Comp. Physiol. A 186,481 -488.[Medline]
Purgue, A. P. and Narins, P. M. (2000b). A model for energy flow in the inner ear of the bullfrog (Rana catesbeiana). J. Comp. Physiol. A 186,489 -495.[Medline]
Ross, R. J. and Smith, J. J. B. (1982). Responses of the salamander inner ear to vibrations of the middle ear. Can. J. Zool. 60,220 -226.
Smith, J. J. B. (1968). Hearing in terrestrial urodeles: a vibration-sensitive mechanism in the ear. J. Exp. Biol. 48,191 -205.[Medline]
Stenfors, L.-E., Salén, B. and Winblad, B. (1979). The role of the pars flaccida in the mechanics of the middle ear. Acta Oto-Laryngol. 88,395 -400.[Medline]
Wever, E. G. (1973). The ear and hearing in the frog, Rana pipiens. J. Morphol. 141,461 -478.[Medline]
Wever, E. G. (1978). Sound transmission in the salamander ear. Proc. Natl. Acad. Sci. USA 75,529 -530.[Abstract]
Wever, E. G. (1979). Middle ear muscles of the frog. Proc. Natl. Acad. Sci. USA 76,3031 -3033.[Abstract]
Wever, E. G. (1985). The Amphibian Ear. Princeton: Princeton University Press.
Wilczynski, W., Resler, C. and Capranica, R. R. (1987). Tympanic and extratympanic sound transmission in the leopard frog. J. Comp. Physiol. A 161,659 -669.[Medline]
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