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Notes on the comparative mechanics of hearing. I. A shock-proof ear
73
Hearing Research, 13 (1984) 73-76 Elsevier
HRR 00449
Notes on the comparative mechanics of hearing. I. A shock-proof ear L.U.E. Kohlbffel Institut
fiir Physiologic und Biokybernetik, Universitiit Erlangen - Niirnberg, Universitiitsstr. I7, 8520 Erlangen, F. KG. (Received 11 July 1983; accepted 21 November
1983)
In woodpeckers, the cochlear windows show functional specialization. The small membrane of the round window is attached to a special bony plate of the columella. This arrangement of coupled windows probably increases power dissipation at the fenestral boundaries woodpecker,
and so dampens impulsive mechanical ear protection,
disturbances.
bone conduction
Introduction The ear is sensitive to small amounts of mechanical energy. How does it cope with the energy released suddenly in mechanical shock? In woodpeckers [l-5,10,11,13,14] one might expect to find special features for ear protection. In pecking, collision exchange with the substrate could cause bone-conducted mechanical transients in the auditory range. Rapid skull deceleration on impact and impact-induced bone vibration could lead to excessive ossicular excursions and shock wave formation in cochlear fluids. This report describes the functional specialization at the cochlear windows observed in woodpeckers. Methods The otic region and the inner ear of many birds were dissected to discover common and variant features in avian gross cochlear morphology: goose, northern mallard, partridge; common quail, domestic turkey, guinea fowl, domestic cock, pheasant, domestic pigeon, tawny owl, blackbird, coal-titmouse, nuthatch, wood-wren; Piciformes: toucan - Ramphastus taco (2, x), green woodpecker - Picus viridis (3, x), grey-headed woodpecker - Picus cunw (1, x), black,woodpecker Dryocopus martius (2, x), great spotted woodpecker - Dendrocopus major (3 nestlings, 3 adult birds). 0378-5955/84/$03.00
0 1984 Elsevier Science Publishers B.V.
(In parentheses are given the number of specimens; an x indicates that dried specimens obtained from zoological collections were examined). Preparations were fixed and stored in 10% formalin solution. Dissection was done under the stereomicroscope. Drawings are by the author. Results and Discussion In woodpeckers, specialization is in the recessus stapedialis at the cochlear windows *. The stapedial recess is narrow and its opening towards the middle ear cavity is just wide enough for the handle of the columella to pass through (Fig. la). The oval window has the usual area, but the round window has less than half the usual area. The specially narrow round window roofs over the anterior and posterior part of the oval window. The trabeculated, light-weight columella has two footplates. The usual ovoid vestibular plate fits the oval window and faces Scala vestibuli (cisterna scalae vestibuli). The special trapezoidal tympanic plate faces the recessus scalae tympani (Fig. lb). The pattern of trabeculation of the columella shows
l
The orientation of the ear in the skull is similar to other birds. Eardrum, extracohtmella, middle ear muscle, cochlear aquaeduct, hehcotrema, ductus brevis, basilar and tectorial membrane do not show specializations in woodpeckers as seen under the stereomicroscope.
a ,
lmm
b
,
lmm
,
Fig. 1. Stapedial recess in the black woodpecker - Dryocopur martins (left ear, round window membrane removed). (a) Outer view of the narrow recess which closely surrounds the handle of columella (extracolumella removed). (b) View from the opened recessus scalae tympani into the stapedial recess through the round window. The tympanic plate of the columella faces the narrow round window. C, columella; TP, tympanic plate of columella; IFP, interfenestral process; RST, recessus scalae tympani; an, anterior; me, medial; do, dorsal.
intra- and interspecies variation. But the dual-plate columella (Fig. 2) and the narrow round window are osteological features common to all four species examined, in spite of the differences in hacking habits between the black and great spotted woodpecker (‘Baum-, Hackspechte’) and the green and grey-headed woodpecker (‘Bodenspechte’) *. The perilymphatic space at the round window is sealed by the tympanic face of the columella and the membrane of the round window (membrana tympani secundaria). The membrane connects to the perimeter of the tympanic plate. As seen in preparations of the great spotted woodpecker, the membrane is small and it has a steep thickness gradient: close to the tympanic plate it is thin, and towards the roof of the recessus scalae tympani it is very thick (Fig. 3). Morphogenetically the characteristic features of the stapedial recess form early
Fig. 2. The piciform columella has two footplates: the usual ovoid vestibular plate and the special trapezoidal tympanic plate. (a) Black woodpecker - Dryocopw murrius (right columella), (b) great spotted woodpecker - Dendrocopur major (right), (c) green woodpecker - Picus oiridis (right), (d) greyheaded woodpecker - Picus canus (left). VP, vestibular plate; TP, tympanic plate of columella.
* The picture of the columella of the green woodpecker by Krause ([9], Taf. 2, No. 17) is misleading. It does not show the tympanic plate and portrays the handle of the columella as too massive.
**In parrots [6,12] and the nuthatch (S&a europaa, own observations) the round window membrane also has a steep thickness gradient. In the toucan the round window membrane is attached to a bony ridge of the columella [g].
in development. The typical features are found complete in young nestlings with the labyrinthine bone still thin and soft (ca. 14 days after hatching) * *. The attachment of the round window membrane to the tympanic plate impairs the vibration of the columella. Force is required to stretch the membrane, and the force is the greater the smaller and thicker the membrane and the longer the border line with the tympanic plate. Owing to the
a
dO&A
RWM /
.
YP
Fig. 3. The membrane of the round window is attached at the circumference of the tympanic plate of the columella (great spotted woodpecker - Dendrocopus major, left ear). (a) Window configuration seen from outside (stapedial recess opened; extracolumella partly shown). (b) Round window membrane in section (inner ear opened, extracolumella removed). RWM, round window membrane; AL, annular ligament; VP and TP, vestibular and tympanic plate of columella; CSV, cistema scalae vestibuh; RST, recessus scalae tympani; an, anterior; me, medial; do, dorsal.
thickness gradient, membrane strain is concentrated in the thin part close to the columella. Here the membrane is soft as noticed by testing with a static point-load (hair-probe). Little elastic force is transmitted to the tympanic plate since membrane deformation does not noticeably displace columella, extracolumella and eardrum. Thus the elastic restoring forces of the middle ear transmission system appear little changed by window coupling. It is likely, however, that the frictional force at the window is increased due to viscous shear stress. The smaller and narrower the membrane and the steeper its thickness gradient the steeper are the velocity gradients in the membrane and the greater are the viscous shear stresses during vibration. So the coupling probably increases frictional resistance and power dissipation at the co&ear
windows - the vestibular and tympanic faces of the columella footplate have about equal areas in contact with perilymph. If the mode of ossicular motion was a rotational vibration with the interfenestral process as axis of rotation, the cochlear fluid would be driven in a fully re-entrant mode. (Re-entrant fluid circuits have been described in several reptilian ears [l&16].) However, as in other birds, the columella in woodpecker is constrained by the suspension system of the extracolumella to move in a translational mode whose axis coincides with the handle of the columella and is normal to the plane of the oval window. (At least so it is seen when the eardrum is statically displaced.) Thus the fluid circuit is only partially re-entrant: the volume displacement of the round window membrane I’,, is smaller than the volume displacement of the oval window Vow since V,, = Va, + Van, with V,, as the re-entrant fluid volume. The functional significance of the coupled flow fields at the windows is unclear. Flow coupling through partial re-entrance may reduce the resultant transient force acting on the sound conducting system in the condition of mechanical shock. References 1 Ass, M.J. (1958): Akustische Orientierung nahrungssuchender Spechte. J. Omithol. 99, 367-377. 2 Becher, F. (1953): Untersuchungen an Spechten zur Frage der funktionellen Anpassungen an die mechanische Belastung. 2. Naturforsch. 8b, 192-203. 3 Berlepsch, H., Freiherr von (1929): Der gesamte Vogelschutz. Neumann, Neudamm. 4 Blume, D. (1958): Bemerkungen zu ‘Akustische Orientierung nahrungssuchender Spechte’ von J.M. Ass. J. Omithol. 99, 317. 5 Blume, D. (1970): Echte Spechte. In: Grzymeks Tierleben. Vol. 9, Vogel 3, pp. 88-114. Kindler, Zurich. 6 Denker, A. (1907): Das Gehororgan und die Sprechwerkzeuge der Papageien. Bergmann, Leipzig. I Hantge, E. (1966): Zum Nahrungserwerb des Dreizehenspechtes. Vogelwelt 87, 21-22. 8 Kohlloffel, L.U.E. (1984): Notes on the comparative mechanics of hearing. II. On cochlear shunts in birds. Hearing Res. 13, 77-81. 9 Krause, G. (1901): Die Columella der Vogel. Friedlander, Berlin. 10 Ramp, W.K. (1965): The auditory range of the hairy woodpecker. Condor 67, 183-185. 11 Rtiger, A. (1972): Funktionell-anatomische Untersuchungen an Spechten. Z. Wiss. Zool. 184, 63-163. 12 Schwartzkopff, J. and Winter, P. (1960): Zur Anatomie der
Vogel-Cochlea unter natiidichen Bedingungen. Biot. Zbl. 79, 607-625. 13 Sielmann, H. (1978): Das Jahr mit den Spechten. Ullstein, Berlin. 14 Spring, L.W. (1965): Climbing and pecking adaptations in
some North American woodpeckers. Condor 67,457-488. 15 Wever, E.G. (1969): Cochlear stimulation and Lempert’s mobilization theory. Arch. Otolaryngol. 90, 720-725. 16 Wever, E.G. (1978): The Reptile Ear. Its Structure and Function. Princeton University Press, Princeton, NJ.
Hearing Research, 13 (1984) 73-76 Elsevier
HRR 00449
Notes on the comparative mechanics of hearing. I. A shock-proof ear L.U.E. Kohlbffel Institut
fiir Physiologic und Biokybernetik, Universitiit Erlangen - Niirnberg, Universitiitsstr. I7, 8520 Erlangen, F. KG. (Received 11 July 1983; accepted 21 November
1983)
In woodpeckers, the cochlear windows show functional specialization. The small membrane of the round window is attached to a special bony plate of the columella. This arrangement of coupled windows probably increases power dissipation at the fenestral boundaries woodpecker,
and so dampens impulsive mechanical ear protection,
disturbances.
bone conduction
Introduction The ear is sensitive to small amounts of mechanical energy. How does it cope with the energy released suddenly in mechanical shock? In woodpeckers [l-5,10,11,13,14] one might expect to find special features for ear protection. In pecking, collision exchange with the substrate could cause bone-conducted mechanical transients in the auditory range. Rapid skull deceleration on impact and impact-induced bone vibration could lead to excessive ossicular excursions and shock wave formation in cochlear fluids. This report describes the functional specialization at the cochlear windows observed in woodpeckers. Methods The otic region and the inner ear of many birds were dissected to discover common and variant features in avian gross cochlear morphology: goose, northern mallard, partridge; common quail, domestic turkey, guinea fowl, domestic cock, pheasant, domestic pigeon, tawny owl, blackbird, coal-titmouse, nuthatch, wood-wren; Piciformes: toucan - Ramphastus taco (2, x), green woodpecker - Picus viridis (3, x), grey-headed woodpecker - Picus cunw (1, x), black,woodpecker Dryocopus martius (2, x), great spotted woodpecker - Dendrocopus major (3 nestlings, 3 adult birds). 0378-5955/84/$03.00
0 1984 Elsevier Science Publishers B.V.
(In parentheses are given the number of specimens; an x indicates that dried specimens obtained from zoological collections were examined). Preparations were fixed and stored in 10% formalin solution. Dissection was done under the stereomicroscope. Drawings are by the author. Results and Discussion In woodpeckers, specialization is in the recessus stapedialis at the cochlear windows *. The stapedial recess is narrow and its opening towards the middle ear cavity is just wide enough for the handle of the columella to pass through (Fig. la). The oval window has the usual area, but the round window has less than half the usual area. The specially narrow round window roofs over the anterior and posterior part of the oval window. The trabeculated, light-weight columella has two footplates. The usual ovoid vestibular plate fits the oval window and faces Scala vestibuli (cisterna scalae vestibuli). The special trapezoidal tympanic plate faces the recessus scalae tympani (Fig. lb). The pattern of trabeculation of the columella shows
l
The orientation of the ear in the skull is similar to other birds. Eardrum, extracohtmella, middle ear muscle, cochlear aquaeduct, hehcotrema, ductus brevis, basilar and tectorial membrane do not show specializations in woodpeckers as seen under the stereomicroscope.
a ,
lmm
b
,
lmm
,
Fig. 1. Stapedial recess in the black woodpecker - Dryocopur martins (left ear, round window membrane removed). (a) Outer view of the narrow recess which closely surrounds the handle of columella (extracolumella removed). (b) View from the opened recessus scalae tympani into the stapedial recess through the round window. The tympanic plate of the columella faces the narrow round window. C, columella; TP, tympanic plate of columella; IFP, interfenestral process; RST, recessus scalae tympani; an, anterior; me, medial; do, dorsal.
intra- and interspecies variation. But the dual-plate columella (Fig. 2) and the narrow round window are osteological features common to all four species examined, in spite of the differences in hacking habits between the black and great spotted woodpecker (‘Baum-, Hackspechte’) and the green and grey-headed woodpecker (‘Bodenspechte’) *. The perilymphatic space at the round window is sealed by the tympanic face of the columella and the membrane of the round window (membrana tympani secundaria). The membrane connects to the perimeter of the tympanic plate. As seen in preparations of the great spotted woodpecker, the membrane is small and it has a steep thickness gradient: close to the tympanic plate it is thin, and towards the roof of the recessus scalae tympani it is very thick (Fig. 3). Morphogenetically the characteristic features of the stapedial recess form early
Fig. 2. The piciform columella has two footplates: the usual ovoid vestibular plate and the special trapezoidal tympanic plate. (a) Black woodpecker - Dryocopw murrius (right columella), (b) great spotted woodpecker - Dendrocopur major (right), (c) green woodpecker - Picus oiridis (right), (d) greyheaded woodpecker - Picus canus (left). VP, vestibular plate; TP, tympanic plate of columella.
* The picture of the columella of the green woodpecker by Krause ([9], Taf. 2, No. 17) is misleading. It does not show the tympanic plate and portrays the handle of the columella as too massive.
**In parrots [6,12] and the nuthatch (S&a europaa, own observations) the round window membrane also has a steep thickness gradient. In the toucan the round window membrane is attached to a bony ridge of the columella [g].
in development. The typical features are found complete in young nestlings with the labyrinthine bone still thin and soft (ca. 14 days after hatching) * *. The attachment of the round window membrane to the tympanic plate impairs the vibration of the columella. Force is required to stretch the membrane, and the force is the greater the smaller and thicker the membrane and the longer the border line with the tympanic plate. Owing to the
a
dO&A
RWM /
.
YP
Fig. 3. The membrane of the round window is attached at the circumference of the tympanic plate of the columella (great spotted woodpecker - Dendrocopus major, left ear). (a) Window configuration seen from outside (stapedial recess opened; extracolumella partly shown). (b) Round window membrane in section (inner ear opened, extracolumella removed). RWM, round window membrane; AL, annular ligament; VP and TP, vestibular and tympanic plate of columella; CSV, cistema scalae vestibuh; RST, recessus scalae tympani; an, anterior; me, medial; do, dorsal.
thickness gradient, membrane strain is concentrated in the thin part close to the columella. Here the membrane is soft as noticed by testing with a static point-load (hair-probe). Little elastic force is transmitted to the tympanic plate since membrane deformation does not noticeably displace columella, extracolumella and eardrum. Thus the elastic restoring forces of the middle ear transmission system appear little changed by window coupling. It is likely, however, that the frictional force at the window is increased due to viscous shear stress. The smaller and narrower the membrane and the steeper its thickness gradient the steeper are the velocity gradients in the membrane and the greater are the viscous shear stresses during vibration. So the coupling probably increases frictional resistance and power dissipation at the co&ear
windows - the vestibular and tympanic faces of the columella footplate have about equal areas in contact with perilymph. If the mode of ossicular motion was a rotational vibration with the interfenestral process as axis of rotation, the cochlear fluid would be driven in a fully re-entrant mode. (Re-entrant fluid circuits have been described in several reptilian ears [l&16].) However, as in other birds, the columella in woodpecker is constrained by the suspension system of the extracolumella to move in a translational mode whose axis coincides with the handle of the columella and is normal to the plane of the oval window. (At least so it is seen when the eardrum is statically displaced.) Thus the fluid circuit is only partially re-entrant: the volume displacement of the round window membrane I’,, is smaller than the volume displacement of the oval window Vow since V,, = Va, + Van, with V,, as the re-entrant fluid volume. The functional significance of the coupled flow fields at the windows is unclear. Flow coupling through partial re-entrance may reduce the resultant transient force acting on the sound conducting system in the condition of mechanical shock. References 1 Ass, M.J. (1958): Akustische Orientierung nahrungssuchender Spechte. J. Omithol. 99, 367-377. 2 Becher, F. (1953): Untersuchungen an Spechten zur Frage der funktionellen Anpassungen an die mechanische Belastung. 2. Naturforsch. 8b, 192-203. 3 Berlepsch, H., Freiherr von (1929): Der gesamte Vogelschutz. Neumann, Neudamm. 4 Blume, D. (1958): Bemerkungen zu ‘Akustische Orientierung nahrungssuchender Spechte’ von J.M. Ass. J. Omithol. 99, 317. 5 Blume, D. (1970): Echte Spechte. In: Grzymeks Tierleben. Vol. 9, Vogel 3, pp. 88-114. Kindler, Zurich. 6 Denker, A. (1907): Das Gehororgan und die Sprechwerkzeuge der Papageien. Bergmann, Leipzig. I Hantge, E. (1966): Zum Nahrungserwerb des Dreizehenspechtes. Vogelwelt 87, 21-22. 8 Kohlloffel, L.U.E. (1984): Notes on the comparative mechanics of hearing. II. On cochlear shunts in birds. Hearing Res. 13, 77-81. 9 Krause, G. (1901): Die Columella der Vogel. Friedlander, Berlin. 10 Ramp, W.K. (1965): The auditory range of the hairy woodpecker. Condor 67, 183-185. 11 Rtiger, A. (1972): Funktionell-anatomische Untersuchungen an Spechten. Z. Wiss. Zool. 184, 63-163. 12 Schwartzkopff, J. and Winter, P. (1960): Zur Anatomie der
Vogel-Cochlea unter natiidichen Bedingungen. Biot. Zbl. 79, 607-625. 13 Sielmann, H. (1978): Das Jahr mit den Spechten. Ullstein, Berlin. 14 Spring, L.W. (1965): Climbing and pecking adaptations in
some North American woodpeckers. Condor 67,457-488. 15 Wever, E.G. (1969): Cochlear stimulation and Lempert’s mobilization theory. Arch. Otolaryngol. 90, 720-725. 16 Wever, E.G. (1978): The Reptile Ear. Its Structure and Function. Princeton University Press, Princeton, NJ.