Proc. Nati. Acad. Sci. USA
Vol. 73, No. 10, pp. 3744-3746, October 1976 Zoology
The caecilian ear: Further observations (hearing/cochlear potentials/Amphibia)
ERNEST GLEN WEVER* AND CARL GANSt *
Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540; and t Division of Biological Sciences, The University of Michigan,
Ann Arbor, Mich. 48109
Contributed by E. G. Wever, August 9, 1976
The Inner Ear. As observed for the other genera, there are eight sense organs in the otic capsule: three crista organs, one each in saccule, utricle, and lagena, and two others that may be designated as papillae: the papilla neglecta and papilla amphibiorum. The papilla neglecta in Ichthyophis may appropriately be called a crista neglecta, as it lacks the statolithic mass characteristic of macular organs. The papilla amphibiorum corresponds closely to this organ in frogs, but these animals lack a structure corresponding to the papilla basilaris that shares the auditory function in most frogs. The Papillar Structure. The cross section (Fig. 4) through the papillar region shows both the papilla amphibiorum and papilla neglecta in further detail. Each papilla consists of a shallow plate of cells occupying a depression in the limbic septum of the region. Their cellular structure is similar, involving a dense array of supporting cells along the limbic surface, and thin columns arising from these cells and running outward to embrace and support the larger, flask-shaped hair cells, the ciliated ends of which are free at the surface. Each papilla has a tectorial body of somewhat differing form. In the amphibian papilla the tectorial body is nearly homogeneous over its main extent, and an array of little recesses or caverns corresponds to the hair cell positions. The ciliary tufts of the hair cells extend into these recesses and attach along their side walls. The papilla neglecta has a tectorial body of blunt conical form with its main mass consisting of a fine reticulum. At its base it spreads out in numerous branching filaments that extend to make connection to the ciliary tufts of the hair cells. Functional considerations General. There is little doubt that the three ampullary organs and the three macular organs of this labyrinth serve equilibratory functions as these do in vertebrates generally. That the papilla amphibiorum serves for sound reception is inferred from its relation to a path of vibratory fluid flow in the presence of stimulating sounds. It is the only sense organ so situated. The Reentrant Fluid Circuit. As observed earlier, the caecilian ear lacks a round window, and mobilization of the cochlear fluid in the presence of sounds is achieved by a continuous fluid circuit as in a number of reptiles (amphisbaenians, snakes, turtles, Sphenodon, and a few lizards). Sounds acting on the side of the head and transmitted to the stapedial footplate can produce vibratory displacements of a fluid column extending from the footplate inward along a circuitous route through the medioventral portion of the otic capsule and then by way of the perilymphatic duct and sac and a path along the brain cavity dorsolaterally to the outer surface of the footplate. The amphibian papilla lies athwart the middle portion of this pathway (Fig. 3). The orifice of the hemispherical papillar enclosure faces the footplate. A thin membranous window in the ventromedial floor of the
ABSTRACT The structure of the ear is examined in two species of caecilians, Ichthyophis glutinosus and L orthoplicatus, and the sensitivity to aerial sounds is assessed in terms of the electrical potentials of the cochlea. The results are in general agreement with previous reports on other caecilian species.
An earlier report dealt with the structure of the caecilian ear and its cochlear potentials in response to sounds in two species, Geotrypetes seraphini and Dermophis mexicanus (1). Now to be reported are observations by similar methods on the two species Ichthyophis glutinosus (3 specimens) and I. orthoplicatus (1 specimen). See ref. 2 for status of these names. Cochlear potential observations Cochlear potentials were measured by inserting a needle electrode into a drilled hole that entered the perilymphatic space just peripheral to the crus commune of the labyrinth (1). Two other electrodes, one of which was grounded, were placed in inactive tissue in the vicinity, and the potentials produced by acoustic stimulation were conducted through a preamplifier to a wave analyzer serving as a selective voltmeter. Aerial tones were presented through a tube sealed to the skin at the side of the head, covering a region somewhat larger than the deeplying stapedial footplate. Results are shown in Fig. 1 for Ichthyophis glutinosus and in Fig. 2 for I. orthoplicatus. Indicated is the sound pressure in decibels relative to 1 dyne/cm2 required to produce a response of 0.1 AuV. The curve for I. glutinosus shows a moderately low level of sensitivity around 0 decibels in the low frequencies, with the maximum at 200 Hz and a relatively constant level of response up to 1000 Hz, after which there is a rapid decline. For I. orthoplicatvs the function has a different form in the low frequencies, with best sensitivity around -15 decibels at the low end of the tested range and again in the region 500-1500 Hz, and poorer sensitivity approaching 0 decibels between. Above 1500 Hz there is a rapid decline as in I. glutinosus. Anatomical observations General. The morphology of the ear in these species of Ichthyophis is much the same as reported earlier for Dermophis and Geotrypetes: the otic capsules are located on either side of the hindbrain in the lateral occipital region of the skull (see also Sarasin and Sarasin, ref. 3; and de Jaeger, ref. 4). The oval window is relatively large and contains a broad stapedial footplate with a headpiece that extends anterolaterally to a junction with the quadrate (Fig. 3). The footplate covers the lateral surface of the capsule, and is held in place by an annular ligament. Its headpiece, only partially indicated in the section shown in Fig. 3, is massive and presents a broad articulatory surface to the quadrate. The skin and muscle layers peripheral to these structures form the receptive surface for sound waves. 3744
Zoology: I
2
Proc. Natl. Acad. Sci. USA 73 (1976)
Wever and Gans 3
4
5
6 7 891
2
3
4
3745
5 6 7 891
+80
I
-4 anI
Lateral canal
'A
+4C0
-
_
Brain a -Perilymphatic cistern
a3 a}
Brain~~~~
0
(n
+20-
-20
_ --
100
---
--
Perilymphatic duct
1
1000 Frequency
10,000
FIG. 3. The ear region of Ichthyophis glutinosus in a longitudinal section, at a level cutting across the amphibian papilla. w indicates window; n, location of papilla neglecta. X25.
FIG. 1. A cochlear potential function for a specimen of Ichthyophis glutinosus.
Concluding remarks These results suggest a general similarity among the ears of these two species of Ichthyophis and two other species of caecilians. All forms lack a tympanic membrane and tympanic cavity and use the unaltered skin and muscle layers as a sound receptive surface. The middle ear contains a single, largely osseous stapes with footplate and headpiece. In the two species of Ichthyophis this headpiece is considerably more massive and has a firmer articulation with the quadrate than in the two caecilians studied previously. The auditory end-organ appears to consist of an amphibian papilla located in a reentrant fluid pathway. The form and location of this papilla vary somewhat among species, but the essential relation to the reentrant circuit is maintained; there is always an orifice accessible to vibratory pressures radiating from the stapedial footplate and a window leading into the perilymphatic duct affords pressure relief. This window has different locations: in Ichthyophis it is in the ventromedial wall of the papillar cavity, whereas in Geotrypetes seraphini it is in the ventral floor and in Dermophis mexicanus it is in the anterior wall, but always the tectorial body is interposed between orifice and window so that it is in the differential path. The mediocre performance of this ear in the present tests is no doubt due largely to the poor transduction of sound energy from an aerial medium to the head tissues. In water, which some
enclosure acoustically connects the papillar cavity with that of the perilymphatic duct. This duct runs posteriorly into the brain cavity, where it expands as the perilymphatic sac. A fluid-filled passage runs anteriorly and laterally along the medulla to lead to the lateral surface of the footplate, completing the fluid circuit. Membranes confining the perilymphatic and cranial fluids lie across this pathway, but impose no appreciable restraints to vibratory transmission. Accordingly, an inward deflection of the stapedial footplate can displace a quantity of fluid that passes around the circuit and is restored to the lateral stapedial surface. The tectorial body occupying the papillar cavity through which this vibratory discharge passes is set in oscillatory motion, and through its ciliary connections stimulates the hair cells lining the walls of the cavity. The adjacent crista neglecta lies outside this vibratory pathway (Fig. 4). It is no doubt exposed in some measure to the vibratory pressures, as are all the contents of the otic capsule, but not to the differential actions that are essential to stimulation. This end-organ most likely is not auditory in function; probably it is a receptor for head motion, as are the other crista organs.
Four ears of Ichthyophis glutinosus had 143, 144, 153, and 156 hair cells in the amphibian papilla. A specimen of I. orthoplicatus had 139 on one side and 181 on the other. These
values are lower than those found in Geotrypetes seraphini (219 and 241 for two ears). 3
4
5
6 7 89 1
2
Amphibian papilla
3
+60
+40-
+20-
0
Frequency
FIG. 2. Cochlear potential function for a specimen of Ichthyophis orthoplicatus.
3746
Zoology:
Wever and Gans
Proc. Natl. Acad. Sci. USA 73 (1976)
Tectoria
Lirnbic septum
Papilla amzphibrorum
Cranicl. wall
Perilymphatic duct
FIG. 4. Cross-sectional view of the papilla amphibiorum and papilla (or crista) neglecta in Ichthyophis orthoplicatus. X75.
species are said to enter on occasion as adults and more generally when young, or in mud, which all appear to inhabit during some seasons of the year, these ears should perform very effectively. We thank R. A. Nussbaum for comments and National Science Foundation Grant BMS 71 01380 and National Institutes of Health Grant NSO 3798-14 for support. The specimens result from the series of Sri Lankan trips of the second author, support for which has been acknowledged elsewhere.
1. Wever, E. G. (1975) "The caecilian ear," J. Exp. Zool. 191, 6372. 2. Nussbaum, R. A. & Gans, C. (1977), "On the Ichthyophis (Amphibia: Gymnophiona) of Sri Lanka," Spolia Zeylanica (in press). 3. Sarasin, P. & Sarasin, R. (1890) "Zur Entwicklungsgeschichte und Anatomie der ceylonesischen Blindwuhle Ichthyophis glutinosus," in Ergebnisse Naturuissenschaftlicher Forschungen auf Ceylon . . . (C. W. Kreidel, Wiesbaden), Vol. 2 (4), pp. 153-263. 4. de Jaeger, E. F. J. (1947) "Some points in the development of the stapes of Ichthyophis glutinosus," Anat. Anz. 96,203-210.
Vol. 73, No. 10, pp. 3744-3746, October 1976 Zoology
The caecilian ear: Further observations (hearing/cochlear potentials/Amphibia)
ERNEST GLEN WEVER* AND CARL GANSt *
Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540; and t Division of Biological Sciences, The University of Michigan,
Ann Arbor, Mich. 48109
Contributed by E. G. Wever, August 9, 1976
The Inner Ear. As observed for the other genera, there are eight sense organs in the otic capsule: three crista organs, one each in saccule, utricle, and lagena, and two others that may be designated as papillae: the papilla neglecta and papilla amphibiorum. The papilla neglecta in Ichthyophis may appropriately be called a crista neglecta, as it lacks the statolithic mass characteristic of macular organs. The papilla amphibiorum corresponds closely to this organ in frogs, but these animals lack a structure corresponding to the papilla basilaris that shares the auditory function in most frogs. The Papillar Structure. The cross section (Fig. 4) through the papillar region shows both the papilla amphibiorum and papilla neglecta in further detail. Each papilla consists of a shallow plate of cells occupying a depression in the limbic septum of the region. Their cellular structure is similar, involving a dense array of supporting cells along the limbic surface, and thin columns arising from these cells and running outward to embrace and support the larger, flask-shaped hair cells, the ciliated ends of which are free at the surface. Each papilla has a tectorial body of somewhat differing form. In the amphibian papilla the tectorial body is nearly homogeneous over its main extent, and an array of little recesses or caverns corresponds to the hair cell positions. The ciliary tufts of the hair cells extend into these recesses and attach along their side walls. The papilla neglecta has a tectorial body of blunt conical form with its main mass consisting of a fine reticulum. At its base it spreads out in numerous branching filaments that extend to make connection to the ciliary tufts of the hair cells. Functional considerations General. There is little doubt that the three ampullary organs and the three macular organs of this labyrinth serve equilibratory functions as these do in vertebrates generally. That the papilla amphibiorum serves for sound reception is inferred from its relation to a path of vibratory fluid flow in the presence of stimulating sounds. It is the only sense organ so situated. The Reentrant Fluid Circuit. As observed earlier, the caecilian ear lacks a round window, and mobilization of the cochlear fluid in the presence of sounds is achieved by a continuous fluid circuit as in a number of reptiles (amphisbaenians, snakes, turtles, Sphenodon, and a few lizards). Sounds acting on the side of the head and transmitted to the stapedial footplate can produce vibratory displacements of a fluid column extending from the footplate inward along a circuitous route through the medioventral portion of the otic capsule and then by way of the perilymphatic duct and sac and a path along the brain cavity dorsolaterally to the outer surface of the footplate. The amphibian papilla lies athwart the middle portion of this pathway (Fig. 3). The orifice of the hemispherical papillar enclosure faces the footplate. A thin membranous window in the ventromedial floor of the
ABSTRACT The structure of the ear is examined in two species of caecilians, Ichthyophis glutinosus and L orthoplicatus, and the sensitivity to aerial sounds is assessed in terms of the electrical potentials of the cochlea. The results are in general agreement with previous reports on other caecilian species.
An earlier report dealt with the structure of the caecilian ear and its cochlear potentials in response to sounds in two species, Geotrypetes seraphini and Dermophis mexicanus (1). Now to be reported are observations by similar methods on the two species Ichthyophis glutinosus (3 specimens) and I. orthoplicatus (1 specimen). See ref. 2 for status of these names. Cochlear potential observations Cochlear potentials were measured by inserting a needle electrode into a drilled hole that entered the perilymphatic space just peripheral to the crus commune of the labyrinth (1). Two other electrodes, one of which was grounded, were placed in inactive tissue in the vicinity, and the potentials produced by acoustic stimulation were conducted through a preamplifier to a wave analyzer serving as a selective voltmeter. Aerial tones were presented through a tube sealed to the skin at the side of the head, covering a region somewhat larger than the deeplying stapedial footplate. Results are shown in Fig. 1 for Ichthyophis glutinosus and in Fig. 2 for I. orthoplicatus. Indicated is the sound pressure in decibels relative to 1 dyne/cm2 required to produce a response of 0.1 AuV. The curve for I. glutinosus shows a moderately low level of sensitivity around 0 decibels in the low frequencies, with the maximum at 200 Hz and a relatively constant level of response up to 1000 Hz, after which there is a rapid decline. For I. orthoplicatvs the function has a different form in the low frequencies, with best sensitivity around -15 decibels at the low end of the tested range and again in the region 500-1500 Hz, and poorer sensitivity approaching 0 decibels between. Above 1500 Hz there is a rapid decline as in I. glutinosus. Anatomical observations General. The morphology of the ear in these species of Ichthyophis is much the same as reported earlier for Dermophis and Geotrypetes: the otic capsules are located on either side of the hindbrain in the lateral occipital region of the skull (see also Sarasin and Sarasin, ref. 3; and de Jaeger, ref. 4). The oval window is relatively large and contains a broad stapedial footplate with a headpiece that extends anterolaterally to a junction with the quadrate (Fig. 3). The footplate covers the lateral surface of the capsule, and is held in place by an annular ligament. Its headpiece, only partially indicated in the section shown in Fig. 3, is massive and presents a broad articulatory surface to the quadrate. The skin and muscle layers peripheral to these structures form the receptive surface for sound waves. 3744
Zoology: I
2
Proc. Natl. Acad. Sci. USA 73 (1976)
Wever and Gans 3
4
5
6 7 891
2
3
4
3745
5 6 7 891
+80
I
-4 anI
Lateral canal
'A
+4C0
-
_
Brain a -Perilymphatic cistern
a3 a}
Brain~~~~
0
(n
+20-
-20
_ --
100
---
--
Perilymphatic duct
1
1000 Frequency
10,000
FIG. 3. The ear region of Ichthyophis glutinosus in a longitudinal section, at a level cutting across the amphibian papilla. w indicates window; n, location of papilla neglecta. X25.
FIG. 1. A cochlear potential function for a specimen of Ichthyophis glutinosus.
Concluding remarks These results suggest a general similarity among the ears of these two species of Ichthyophis and two other species of caecilians. All forms lack a tympanic membrane and tympanic cavity and use the unaltered skin and muscle layers as a sound receptive surface. The middle ear contains a single, largely osseous stapes with footplate and headpiece. In the two species of Ichthyophis this headpiece is considerably more massive and has a firmer articulation with the quadrate than in the two caecilians studied previously. The auditory end-organ appears to consist of an amphibian papilla located in a reentrant fluid pathway. The form and location of this papilla vary somewhat among species, but the essential relation to the reentrant circuit is maintained; there is always an orifice accessible to vibratory pressures radiating from the stapedial footplate and a window leading into the perilymphatic duct affords pressure relief. This window has different locations: in Ichthyophis it is in the ventromedial wall of the papillar cavity, whereas in Geotrypetes seraphini it is in the ventral floor and in Dermophis mexicanus it is in the anterior wall, but always the tectorial body is interposed between orifice and window so that it is in the differential path. The mediocre performance of this ear in the present tests is no doubt due largely to the poor transduction of sound energy from an aerial medium to the head tissues. In water, which some
enclosure acoustically connects the papillar cavity with that of the perilymphatic duct. This duct runs posteriorly into the brain cavity, where it expands as the perilymphatic sac. A fluid-filled passage runs anteriorly and laterally along the medulla to lead to the lateral surface of the footplate, completing the fluid circuit. Membranes confining the perilymphatic and cranial fluids lie across this pathway, but impose no appreciable restraints to vibratory transmission. Accordingly, an inward deflection of the stapedial footplate can displace a quantity of fluid that passes around the circuit and is restored to the lateral stapedial surface. The tectorial body occupying the papillar cavity through which this vibratory discharge passes is set in oscillatory motion, and through its ciliary connections stimulates the hair cells lining the walls of the cavity. The adjacent crista neglecta lies outside this vibratory pathway (Fig. 4). It is no doubt exposed in some measure to the vibratory pressures, as are all the contents of the otic capsule, but not to the differential actions that are essential to stimulation. This end-organ most likely is not auditory in function; probably it is a receptor for head motion, as are the other crista organs.
Four ears of Ichthyophis glutinosus had 143, 144, 153, and 156 hair cells in the amphibian papilla. A specimen of I. orthoplicatus had 139 on one side and 181 on the other. These
values are lower than those found in Geotrypetes seraphini (219 and 241 for two ears). 3
4
5
6 7 89 1
2
Amphibian papilla
3
+60
+40-
+20-
0
Frequency
FIG. 2. Cochlear potential function for a specimen of Ichthyophis orthoplicatus.
3746
Zoology:
Wever and Gans
Proc. Natl. Acad. Sci. USA 73 (1976)
Tectoria
Lirnbic septum
Papilla amzphibrorum
Cranicl. wall
Perilymphatic duct
FIG. 4. Cross-sectional view of the papilla amphibiorum and papilla (or crista) neglecta in Ichthyophis orthoplicatus. X75.
species are said to enter on occasion as adults and more generally when young, or in mud, which all appear to inhabit during some seasons of the year, these ears should perform very effectively. We thank R. A. Nussbaum for comments and National Science Foundation Grant BMS 71 01380 and National Institutes of Health Grant NSO 3798-14 for support. The specimens result from the series of Sri Lankan trips of the second author, support for which has been acknowledged elsewhere.
1. Wever, E. G. (1975) "The caecilian ear," J. Exp. Zool. 191, 6372. 2. Nussbaum, R. A. & Gans, C. (1977), "On the Ichthyophis (Amphibia: Gymnophiona) of Sri Lanka," Spolia Zeylanica (in press). 3. Sarasin, P. & Sarasin, R. (1890) "Zur Entwicklungsgeschichte und Anatomie der ceylonesischen Blindwuhle Ichthyophis glutinosus," in Ergebnisse Naturuissenschaftlicher Forschungen auf Ceylon . . . (C. W. Kreidel, Wiesbaden), Vol. 2 (4), pp. 153-263. 4. de Jaeger, E. F. J. (1947) "Some points in the development of the stapes of Ichthyophis glutinosus," Anat. Anz. 96,203-210.
