Proc. Natl. Acad. Sci. USA
Vol. 75, No. 1, pp. 529-530, January 1978 Physiological Sciences
Sound transmission in the salamander ear (hearing/cochlear potentials/amphibia)
ERNEST GLEN WEVER Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540
Contributed by E. G. Wever, October 17, 1977
ABSTRACT The mode of stimulation of the ear by sounds is considered in Amphibia, in which it differs among the three Recent orders. Of special interest is the order Caudata, in which this stimulation takes a unique form: sounds applied to the oval window of one ear produce a path of vibratory motion that passes through the brain cavity to the oval win ow on the opposite side. In this course the vibratory movements traverse both right and left amphibian papillae, and both basilar papillae also in species that contain these endorgans. Thus, in the salamander therearing is invariably binaural.
In vertebrates the auditory hair cells are immersed in fluid and are sensitive to displacements; in all vertebrates above the fishes, sound stimuli involve these cells only by mobilizing the inner ear fluids. This fluid mobilization ordinarily is achieved in one of two ways. In birds and mammals and in a number of reptiles one wall of the inner ear capsule contains a round window, an opening covered by a thin membrane beyond which lies an air cavity. This window provides a place of pressure relief when vibratory sound pressures are exerted from the outside, usually by way of an external ear opening and a middle ear apparatus applied to the oval window of the cochlea. The fluid then is set in oscillation between oval and round windows: an inward displacement at the oval window is accompanied by an outward displacement of equal volume at the round window. A second method of fluid mobilization is utilized in many of the reptiles, including turtles, snakes, amphisbaenians, Sphenodon, and a few species of lizards, which lack a round window. These use a reentrant fluid circuit: a pathway leads inward from the footplate of the oval window and takes a roundabout course to the outer surface of this same footplate, and the fluid surges back and forth along this pathway. These two modes of fluid mobilization are both effective for their purpose, though the reentrant fluid circuit, because of the increased mass of fluid that must be set in motion, serves best for low tones and restricts the ear's sensitivity to high tones. A consideration of this problem of fluid mobilization in the three orders of living amphibians reveals three types of solution: the two just described for other vertebrates and one that is entirely new. The Anura (frogs and toads) possess a round window and use the first solution mentioned. The Gymnophiona (caecilians) use a reentrant fluid circuit (1, 2). The Caudata (salamanders), however, resort to a peculiar expedient: literally a sound must "go in one ear and out the other." The evidence that this is the case will now be presented.
RESULTS The Otocranial Enclosure in the Salamanders Presents Only Two Significant Openings, One on Either Side of the Head. These are properly regarded as oval windows, and each
is covered by a membrane in which is embedded a firm structure whose composition varies with species and often varies with the animal's stage of development. In its simplest form, which is all that need be considered here, this structure is a disk of cartilage, known as the operculum. As shown in Fig. 1 for the newt, Taricha granulosa, the otocranial enclosure is of firm material, of bone and cartilage, except in two areas at the sides of the head. This figure presents a particular cross section, but any other section in the otic region will show the same condition: pressures exerted at one operculum can produce fluid displacements within the otocranium only by traversing a complex path across the head to the contralateral operculum, as indicated by the arrows. This path leads through three different fluids separated by thin membranes; from right to left the path traverses first the perilymph of the perilymphatic cistern, then passes into the saccular cavity, which contains endolymph, thus reaching the amphibian papilla that lies in a recess that is a diverticulum of the sacculus. From the amphibian papilla a membranous window leads to the perilymphatic duct that passes through the bony partition between otic and cranial cavities and reaches the perilymphatic sac within the cranium. Thereafter, the pathway traverses the arachnoid membrane to the cerebrospinal fluid and extends across the midline, chiefly passing beneath the brain, and thereafter continues through the same structures in reverse order until the opposite operculum is reached. It will be noted
that the sensory cells of both right and left amphibian papillae lie in the path of the vibratory movements. In many species of salamanders a second endorgan, the basilar papilla, is encountered on each side also. This papilla is not shown in Fig. 1 as it lies at a different level, and indeed it appears to be vestigial in this species. This papilla, when present, has the same relations to the pathway across the head as the amphibian papilla. Stimulation at One Operculum Produces Responses in Both Ears. These responses were recorded by inserting fine needle electrodes on both sides through holes drilled in the otic capsules so as to enter the dorsal portion of the perilymphatic cistern. Cochlear potentials were then produced by sounds applied with a vibrating needle in contact with the right operculum. Results of one of these experiments are presented in Fig. 2. Typically, as shown, the ipsilateral responses are greater than the contralateral ones. This difference is explained if it is supposed, as seems likely, that there are leakages of acoustic energy along the fluid circuit: not all the vibratory motion that passes over the right amphibian papilla is able to reach the left one.
Immobilization and Loading of the Operculum on One Side Produces a Profound Alteration of Responses as Recorded from the Other Side. If the stimulus is applied to the right operculum, and the recording electrode is in the right perilymphatic cistern, a blocking of the left operculum with a lump of bone wax or a mass of modeling clay has a marked
The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. 529
Proc. Natl. Acad. Sci. US.A 75 (1978)
Physiological Sciences: Wever
530
Amphibian papilla
Otocranial capsule
1
2
3
2
4 5 6 7891
3
4 5 6789'1
-D 5
a +20
40 ~
E
Brain ccavity
effect on the responses, greatly reducing them for some tones and often augmenting them for others. As Fig. 3 shows, the reduction is greatest for those tones to which the ear normally is most sensitive, and smaller changes, which are sometimes increases, occur for lower and higher tones. The blocking of the operculum in the manner described evidently adds both mass and stiffness to the vibrating fluid column and alters the resonances of the system in complicated ways. Bilateral Stimulation while Recording from Either Ear Produces Additive Effects Depending on Phase Relations. A vibratory stimulus was applied to the right operculum and the intensity was adjusted to produce some arbitrary level of cochlear potentials as recorded from an electrode on the right side, then the same procedure was carried out independently for stimulation of the left operculum. An application of both stimuli simultaneously then produced an increased response (a response V2 times the previous one) at a certain phase relation between right and left stimuli. A cancellation of the response was obtained at a phase relation 1800 from the first one, and intermediate values of response were found for phase relations between these two. 3 4 5 6 7891 2 T [ J
1
-~+40
Contralateral ear'
~+20 +20 -~ C-
g
|
3 4 56 7891
2 1
A
I% \
|> |
psi lateral ear
cn
100
1000 Frequency
10,000
FIG. 2. Sensitivity functions for a specimen of the salamander Ambystoma tigrinum. Sensory potentials are shown in response to aerial sounds presented to the right side of the head as recorded from right and left ears. The curves indicate the sound pressure, in decibels relative to 1 dyne/cm2, required to produce a standard response of 0.1
IAV.
l-
-1
~
~
I
>
FIG. 1. Cross section of the head of Taricha granulosa through the ear region. (x4.3.)
+60
-
-0
F 40
| -60 _ -
61
100
X|
X
rX
V ~~~~~~Contralaterl operculum-
Normal
J2.6I LL L..I..I .. 1000 Frequency
IIw 10,000
FIG. 3. The effects of blocking the left operculum on sensory potentials produced in a specimen of Ambystoma maculatum by vibratory stimuli applied to the right operculum. Recording was from an electrode in the right otic capsule.
DISCUSSION It is evident that in the salamander a sound applied to one ear passes across the head and involves both right and left auditory sense organs. This peculiar performance presents a number of problems. The most serious problem is how the salamander is able to hear at all under ordinary conditions: with its relatively small head the two sides should be almost equally stimulated when the animal is in a uniform sound field, and complete cancellation would be expected. Perhaps the salamander is mainly sensitive to incident sounds or to sudden changes in sustained sounds, and largely fails to hear steady tones. The localization of sounds in space may be expected to be impaired in these animals. Cues that depend upon binaural differences of intensity, which are utilized in most animals in determining the direction of a sound source, will be much reduced or lacking. Binaural differences of phase and in the time of incidence of sounds should still be present in these animals and may be effective. Unfortunately, we have little information about the behavioral reactions of salamanders to acoustic stimuli and little knowledge about the importance of sounds in their adaptations. This research was supported by grants from the National Institutes of Health and the National Science Foundation. 1. Wever, E. G. (1975) "The caecilian ear," J. Exp. Zool. 191, 6372. 2. Wever, E. G. & Gans, C. (1976) "The caecilian ear: Further observations," Proc. Natl. Acad. Sci. USA 73,3747-3746.
Vol. 75, No. 1, pp. 529-530, January 1978 Physiological Sciences
Sound transmission in the salamander ear (hearing/cochlear potentials/amphibia)
ERNEST GLEN WEVER Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540
Contributed by E. G. Wever, October 17, 1977
ABSTRACT The mode of stimulation of the ear by sounds is considered in Amphibia, in which it differs among the three Recent orders. Of special interest is the order Caudata, in which this stimulation takes a unique form: sounds applied to the oval window of one ear produce a path of vibratory motion that passes through the brain cavity to the oval win ow on the opposite side. In this course the vibratory movements traverse both right and left amphibian papillae, and both basilar papillae also in species that contain these endorgans. Thus, in the salamander therearing is invariably binaural.
In vertebrates the auditory hair cells are immersed in fluid and are sensitive to displacements; in all vertebrates above the fishes, sound stimuli involve these cells only by mobilizing the inner ear fluids. This fluid mobilization ordinarily is achieved in one of two ways. In birds and mammals and in a number of reptiles one wall of the inner ear capsule contains a round window, an opening covered by a thin membrane beyond which lies an air cavity. This window provides a place of pressure relief when vibratory sound pressures are exerted from the outside, usually by way of an external ear opening and a middle ear apparatus applied to the oval window of the cochlea. The fluid then is set in oscillation between oval and round windows: an inward displacement at the oval window is accompanied by an outward displacement of equal volume at the round window. A second method of fluid mobilization is utilized in many of the reptiles, including turtles, snakes, amphisbaenians, Sphenodon, and a few species of lizards, which lack a round window. These use a reentrant fluid circuit: a pathway leads inward from the footplate of the oval window and takes a roundabout course to the outer surface of this same footplate, and the fluid surges back and forth along this pathway. These two modes of fluid mobilization are both effective for their purpose, though the reentrant fluid circuit, because of the increased mass of fluid that must be set in motion, serves best for low tones and restricts the ear's sensitivity to high tones. A consideration of this problem of fluid mobilization in the three orders of living amphibians reveals three types of solution: the two just described for other vertebrates and one that is entirely new. The Anura (frogs and toads) possess a round window and use the first solution mentioned. The Gymnophiona (caecilians) use a reentrant fluid circuit (1, 2). The Caudata (salamanders), however, resort to a peculiar expedient: literally a sound must "go in one ear and out the other." The evidence that this is the case will now be presented.
RESULTS The Otocranial Enclosure in the Salamanders Presents Only Two Significant Openings, One on Either Side of the Head. These are properly regarded as oval windows, and each
is covered by a membrane in which is embedded a firm structure whose composition varies with species and often varies with the animal's stage of development. In its simplest form, which is all that need be considered here, this structure is a disk of cartilage, known as the operculum. As shown in Fig. 1 for the newt, Taricha granulosa, the otocranial enclosure is of firm material, of bone and cartilage, except in two areas at the sides of the head. This figure presents a particular cross section, but any other section in the otic region will show the same condition: pressures exerted at one operculum can produce fluid displacements within the otocranium only by traversing a complex path across the head to the contralateral operculum, as indicated by the arrows. This path leads through three different fluids separated by thin membranes; from right to left the path traverses first the perilymph of the perilymphatic cistern, then passes into the saccular cavity, which contains endolymph, thus reaching the amphibian papilla that lies in a recess that is a diverticulum of the sacculus. From the amphibian papilla a membranous window leads to the perilymphatic duct that passes through the bony partition between otic and cranial cavities and reaches the perilymphatic sac within the cranium. Thereafter, the pathway traverses the arachnoid membrane to the cerebrospinal fluid and extends across the midline, chiefly passing beneath the brain, and thereafter continues through the same structures in reverse order until the opposite operculum is reached. It will be noted
that the sensory cells of both right and left amphibian papillae lie in the path of the vibratory movements. In many species of salamanders a second endorgan, the basilar papilla, is encountered on each side also. This papilla is not shown in Fig. 1 as it lies at a different level, and indeed it appears to be vestigial in this species. This papilla, when present, has the same relations to the pathway across the head as the amphibian papilla. Stimulation at One Operculum Produces Responses in Both Ears. These responses were recorded by inserting fine needle electrodes on both sides through holes drilled in the otic capsules so as to enter the dorsal portion of the perilymphatic cistern. Cochlear potentials were then produced by sounds applied with a vibrating needle in contact with the right operculum. Results of one of these experiments are presented in Fig. 2. Typically, as shown, the ipsilateral responses are greater than the contralateral ones. This difference is explained if it is supposed, as seems likely, that there are leakages of acoustic energy along the fluid circuit: not all the vibratory motion that passes over the right amphibian papilla is able to reach the left one.
Immobilization and Loading of the Operculum on One Side Produces a Profound Alteration of Responses as Recorded from the Other Side. If the stimulus is applied to the right operculum, and the recording electrode is in the right perilymphatic cistern, a blocking of the left operculum with a lump of bone wax or a mass of modeling clay has a marked
The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. 529
Proc. Natl. Acad. Sci. US.A 75 (1978)
Physiological Sciences: Wever
530
Amphibian papilla
Otocranial capsule
1
2
3
2
4 5 6 7891
3
4 5 6789'1
-D 5
a +20
40 ~
E
Brain ccavity
effect on the responses, greatly reducing them for some tones and often augmenting them for others. As Fig. 3 shows, the reduction is greatest for those tones to which the ear normally is most sensitive, and smaller changes, which are sometimes increases, occur for lower and higher tones. The blocking of the operculum in the manner described evidently adds both mass and stiffness to the vibrating fluid column and alters the resonances of the system in complicated ways. Bilateral Stimulation while Recording from Either Ear Produces Additive Effects Depending on Phase Relations. A vibratory stimulus was applied to the right operculum and the intensity was adjusted to produce some arbitrary level of cochlear potentials as recorded from an electrode on the right side, then the same procedure was carried out independently for stimulation of the left operculum. An application of both stimuli simultaneously then produced an increased response (a response V2 times the previous one) at a certain phase relation between right and left stimuli. A cancellation of the response was obtained at a phase relation 1800 from the first one, and intermediate values of response were found for phase relations between these two. 3 4 5 6 7891 2 T [ J
1
-~+40
Contralateral ear'
~+20 +20 -~ C-
g
|
3 4 56 7891
2 1
A
I% \
|> |
psi lateral ear
cn
100
1000 Frequency
10,000
FIG. 2. Sensitivity functions for a specimen of the salamander Ambystoma tigrinum. Sensory potentials are shown in response to aerial sounds presented to the right side of the head as recorded from right and left ears. The curves indicate the sound pressure, in decibels relative to 1 dyne/cm2, required to produce a standard response of 0.1
IAV.
l-
-1
~
~
I
>
FIG. 1. Cross section of the head of Taricha granulosa through the ear region. (x4.3.)
+60
-
-0
F 40
| -60 _ -
61
100
X|
X
rX
V ~~~~~~Contralaterl operculum-
Normal
J2.6I LL L..I..I .. 1000 Frequency
IIw 10,000
FIG. 3. The effects of blocking the left operculum on sensory potentials produced in a specimen of Ambystoma maculatum by vibratory stimuli applied to the right operculum. Recording was from an electrode in the right otic capsule.
DISCUSSION It is evident that in the salamander a sound applied to one ear passes across the head and involves both right and left auditory sense organs. This peculiar performance presents a number of problems. The most serious problem is how the salamander is able to hear at all under ordinary conditions: with its relatively small head the two sides should be almost equally stimulated when the animal is in a uniform sound field, and complete cancellation would be expected. Perhaps the salamander is mainly sensitive to incident sounds or to sudden changes in sustained sounds, and largely fails to hear steady tones. The localization of sounds in space may be expected to be impaired in these animals. Cues that depend upon binaural differences of intensity, which are utilized in most animals in determining the direction of a sound source, will be much reduced or lacking. Binaural differences of phase and in the time of incidence of sounds should still be present in these animals and may be effective. Unfortunately, we have little information about the behavioral reactions of salamanders to acoustic stimuli and little knowledge about the importance of sounds in their adaptations. This research was supported by grants from the National Institutes of Health and the National Science Foundation. 1. Wever, E. G. (1975) "The caecilian ear," J. Exp. Zool. 191, 6372. 2. Wever, E. G. & Gans, C. (1976) "The caecilian ear: Further observations," Proc. Natl. Acad. Sci. USA 73,3747-3746.
