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

ABSTRACT The structure of the ear is examined in two The Inner Ear. As observed for the other genera, there are species of caecilians, Ichthyophis glutinosus and L orthopli- eight sense organs in the otic capsule: three crista organs, one catus, and the sensitivity to aerial sounds is assessed in terms each in saccule, utricle, and lagena, and two others that may of the electrical potentials of the cochlea. The results are in general agreement with previous reports on other caecilian be designated as papillae: the papilla neglecta and papilla species. amphibiorum. The papilla neglecta in Ichthyophis may ap- propriately be called a crista neglecta, as it lacks the statolithic An earlier report dealt with the structure of the caecilian ear mass characteristic of macular organs. The papilla amphibio- and its cochlear potentials in response to sounds in two species, rum corresponds closely to this organ in frogs, but these animals Geotrypetes seraphini and Dermophis mexicanus (1). Now to lack a structure corresponding to the papilla basilaris that shares be reported are observations by similar methods on the two the auditory function in most frogs. species Ichthyophis glutinosus (3 specimens) and I. orthopli- The Papillar Structure. The cross section (Fig. 4) through catus (1 specimen). See ref. 2 for status of these names. the papillar region shows both the papilla amphibiorum and Cochlear potential observations papilla neglecta in further detail. Each papilla consists of a shallow plate of cells occupying a depression in the limbic Cochlear potentials were measured by inserting a needle septum of the region. Their cellular structure is similar, in- electrode into a drilled hole that entered the perilymphatic volving a dense array of supporting cells along the limbic sur- space just peripheral to the crus commune of the labyrinth (1). face, and thin columns arising from these cells and running Two other electrodes, one of which was grounded, were placed outward to embrace and support the larger, flask-shaped hair in inactive tissue in the vicinity, and the potentials produced cells, the ciliated ends of which are free at the surface. Each by acoustic stimulation were conducted through a preamplifier papilla has a tectorial body of somewhat differing form. In the to a wave analyzer serving as a selective voltmeter. Aerial tones amphibian papilla the tectorial body is nearly homogeneous were presented through a tube sealed to the skin at the side of over its main extent, and an array of little recesses or caverns the head, covering a region somewhat larger than the deep- corresponds to the hair cell positions. The ciliary tufts of the hair lying stapedial footplate. cells extend into these recesses and attach along their side Results are shown in Fig. 1 for Ichthyophis glutinosus and walls. in Fig. 2 for I. orthoplicatus. Indicated is the sound pressure The papilla neglecta has a tectorial body of blunt conical in decibels relative to 1 dyne/cm2 required to produce a re- form with its main mass consisting of a fine reticulum. At its sponse of 0.1 AuV. base it spreads out in numerous branching filaments that extend The curve for I. glutinosus shows a moderately low level of to make connection to the ciliary tufts of the hair cells. sensitivity around 0 decibels in the low frequencies, with the maximum at 200 Hz and a relatively constant level of response Functional considerations up to 1000 Hz, after which there is a rapid decline. For I. or- General. There is little doubt that the three ampullary organs thoplicatvs the function has a different form in the low and the three macular organs of this labyrinth serve equili- frequencies, with best sensitivity around -15 decibels at the bratory functions as these do in vertebrates generally. That the low end of the tested range and again in the region 500-1500 papilla amphibiorum serves for sound reception is inferred from Hz, and poorer sensitivity approaching 0 decibels between. its relation to a path of vibratory fluid flow in the presence of Above 1500 Hz there is a rapid decline as in I. glutinosus. stimulating sounds. It is the only sense organ so situated. Anatomical observations The Reentrant Fluid Circuit. As observed earlier, the cae- General. The morphology of the ear in these species of cilian ear lacks a round window, and mobilization of the co- Ichthyophis is much the same as reported earlier for Dermophis chlear fluid in the presence of sounds is achieved by a contin- and Geotrypetes: the otic capsules are located on either side of uous fluid circuit as in a number of reptiles (amphisbaenians, the hindbrain in the lateral occipital region of the skull (see also snakes, turtles, Sphenodon, and a few lizards). Sounds acting Sarasin and Sarasin, ref. 3; and de Jaeger, ref. 4). The oval on the side of the head and transmitted to the stapedial footplate window is relatively large and contains a broad stapedial can produce vibratory displacements of a fluid column ex- footplate with a headpiece that extends anterolaterally to a tending from the footplate inward along a circuitous route junction with the quadrate (Fig. 3). through the medioventral portion of the otic capsule and then The footplate covers the lateral surface of the capsule, and by way of the perilymphatic duct and sac and a path along the is held in place by an annular ligament. Its headpiece, only brain cavity dorsolaterally to the outer surface of the footplate. partially indicated in the section shown in Fig. 3, is massive and The amphibian papilla lies athwart the middle portion of this presents a broad articulatory surface to the quadrate. The skin pathway (Fig. 3). The orifice of the hemispherical papillar and muscle layers peripheral to these structures form the re- enclosure faces the footplate. ceptive surface for sound waves. A thin membranous window in the ventromedial floor of the 3744 Downloaded by guest on September 24, 2021 Zoology: Wever and Gans Proc. Natl. Acad. Sci. USA 73 (1976) 3745

I 2 3 4 5 6 7 891 2 3 4 5 6 7 891 +80

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'A +4C0 - _ a3 a} Brain a -Perilymphatic cistern

0 Brain~~~~

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-20 --_ 1 Perilymphatic duct 100 1000 10,000 Amphibian papilla Frequency FIG. 3. The ear region ofIchthyophis glutinosus in a longitudinal FIG. 1. A cochlear potential function for a specimen of Ichthy- section, at a level cutting across the amphibian papilla. w indicates ophis glutinosus. window; n, location of papilla neglecta. X25.

enclosure acoustically connects the papillar cavity with that of Concluding remarks the perilymphatic duct. This duct runs posteriorly into the brain These results suggest a general similarity among the ears of these cavity, where it expands as the perilymphatic sac. A fluid-filled two species of Ichthyophis and two other species of caecilians. passage runs anteriorly and laterally along the medulla to lead All forms lack a tympanic membrane and tympanic cavity and to the lateral surface of the footplate, completing the fluid use the unaltered skin and muscle layers as a sound receptive circuit. Membranes confining the perilymphatic and cranial surface. The middle ear contains a single, largely osseous stapes fluids lie across this pathway, but impose no appreciable re- with footplate and headpiece. In the two species of Ichthyophis straints to vibratory transmission. Accordingly, an inward de- this headpiece is considerably more massive and has a firmer flection of the stapedial footplate can displace a quantity of articulation with the quadrate than in the two caecilians studied fluid that passes around the circuit and is restored to the lateral previously. stapedial surface. The tectorial body occupying the papillar The auditory end-organ appears to consist of an amphibian cavity through which this vibratory discharge passes is set in papilla located in a reentrant fluid pathway. The form and oscillatory motion, and through its ciliary connections stimulates location of this papilla vary somewhat among species, but the the hair cells lining the walls of the cavity. essential relation to the reentrant circuit is maintained; there The adjacent crista neglecta lies outside this vibratory is always an orifice accessible to vibratory pressures radiating pathway (Fig. 4). It is no doubt exposed in some measure to the from the stapedial footplate and a window leading into the vibratory pressures, as are all the contents of the otic capsule, perilymphatic duct affords pressure relief. This window has but not to the differential actions that are essential to stimula- different locations: in Ichthyophis it is in the ventromedial wall tion. This end-organ most likely is not auditory in function; of the papillar cavity, whereas in Geotrypetes seraphini it is probably it is a receptor for head motion, as are the other crista in the ventral floor and in Dermophis mexicanus it is in the organs. anterior wall, but always the tectorial body is interposed be- Four ears of Ichthyophis glutinosus had 143, 144, 153, and tween orifice and window so that it is in the differential 156 hair cells in the amphibian papilla. A specimen of I. or- path. thoplicatus had 139 on one side and 181 on the other. These The mediocre performance of this ear in the present tests is values are lower than those found in Geotrypetes seraphini (219 no doubt due largely to the poor transduction of sound energy and 241 for two ears). from an aerial medium to the head tissues. In water, which some

3 4 5 6 7 89 1 2 3 +60

+40-

+20-

0

Frequency

FIG. 2. Cochlear potential function for a specimen of Ichthyophis orthoplicatus. Downloaded by guest on September 24, 2021 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 1. Wever, E. G. (1975) "The caecilian ear," J. Exp. Zool. 191, 63- when young, or in mud, which all appear to inhabit during 72. some seasons of the year, these ears should perform very ef- 2. Nussbaum, R. A. & Gans, C. (1977), "On the Ichthyophis (Am- fectively. phibia: Gymnophiona) of Sri Lanka," Spolia Zeylanica (in press). 3. Sarasin, P. & Sarasin, R. (1890) "Zur Entwicklungsgeschichte und We thank R. A. Nussbaum for comments and National Science Anatomie der ceylonesischen Blindwuhle Ichthyophis glutinosus," Foundation Grant BMS 71 01380 and National Institutes of Health in Ergebnisse Naturuissenschaftlicher Forschungen auf Ceylon Grant NSO 3798-14 for support. The specimens result from the series . . . (C. W. Kreidel, Wiesbaden), Vol. 2 (4), pp. 153-263. of Sri Lankan trips of the second author, support for which has been 4. de Jaeger, E. F. J. (1947) "Some points in the development of the acknowledged elsewhere. stapes of Ichthyophis glutinosus," Anat. Anz. 96,203-210. Downloaded by guest on September 24, 2021