The Cochlea of the Dolphin, Tursiops Truncatus: General Morphology* (Organ of Corti/Ear/Light Microscopy) ERNEST GLEN WEVER, JAMES G

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The Cochlea of the Dolphin, Tursiops Truncatus: General Morphology* (Organ of Corti/Ear/Light Microscopy) ERNEST GLEN WEVER, JAMES G Proc. Nat. Acad. Sci. USA Vol. 68, No. 10, pp. 2381-2385, October 1971 The Cochlea of the Dolphin, Tursiops truncatus: General Morphology* (organ of Corti/ear/light microscopy) ERNEST GLEN WEVER, JAMES G. McCORMICKt, JERRY PALIN, AND SAM H. RIDGWAYT Department of Psychology, Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540 Contributed by Ernest Glen Wever, July 16, 1971 ABSTRACT The anatomy of the cochlea of the dolphin chloride. The ears were removed, further fixed by immersion Tursiops truncatus was studied in a number of specimens for 10 days, then held in 10% formol for final processing. after fixation by vital perfusion, celloidin embedding, and serial sectioning. The results reveal the general structural The dolphin ear is a formidable object for histology, as relations and cellular detail up to the limits of light Kolmer remarked earlier (3). We used several specimens and microscopy. A description is given of the variations of more than a year for the necessary adaptations of our usual structure along the course of the cochlea, in which there methods. In our final procedure, we decalcified the tissues are many departures from the typical mammalian form, especially in the compact quality of the tissues and the in 0.5% nitric acid in 10% formol, changed the solution 60 sturdiness of its elements. Apparently these features times over a period of 3 months, dehydrated the tissues in represent an adaptation of the cetacean ear to the recep- a series of alcohols ranging from 20 to 100%, in 10% steps, tion of high-frequency sounds. over a period of 1 month, embedded the tissues in celloidin in four steps from 4 to 16% over a period of 6 months, and Though many have studied the gross anatomy of the cetacean finally hardened them in chloroform and alcohol. of the cochlea little 80% ear (1), the detailed structure has received We determined the proper orientation for sectioning by attention. Boenninghaus (2) examined several specimens of preparing skulls with the ear bones in place, and in two the Phocaena communis, and observed the general form of preparations the petrous bone was carefully ground away to Kolmer studied a young membranous labyrinth. (3) specimen expose the cochlear turns. Sections were cut at 30 usually a few after and was able to Am, of Phocaena obtained hours death, in a plane parallel to the cochlear axis, either approximately make out of the cellular structures. He identified the many vertical to the head, as shown in Fig. 1, or at right angles to of the elements of the organ kinds epithelial cells, supporting this position. One specimen was sectioned in a plane perpen- of Corti, and the hair cells, and pointed out especially the the which dicular to the cochlear axis. great size of cells of Claudius, be characterized as All sections through the ear were stained and mounted. the largest epithelial cells known in mammals. Two other re- For some of the series, we used Pollak's trichrome stain and for ports are mentioned in the references§ (4¶1). others a combination of hematoxylin, azocarmine, and orange METHOD G. Our study was performed on specimens of the bottlenosed dolphin, Tursiops truncatus Montagu, that had been used in an electrophysiological investigation of sound conduction (5). At the end of the tests on these ears, the anesthetized animals were perfused for histological examination. The blood was flushed out through a cannula in the dorsal aorta with about 40 liters of physiological saline, and then the tissues were fixed with 120 liters or more of a mixture of potassium dichromate, sodium sulfate, formaldehyde, and (sometimes) mercuric * This is the first of a series of articles on the cochlea of the dolphin, Tursiops truncatus. t Present address, Section of Otolaryngology, Bowman-Gray School of Medicine, Winston-Salem, N.C. $ Naval Undersea Research and Development Center, San Diego, Calif. § Bloome, K., The delphinid auditory apparatus, Parts I and II. Unpublished; seen in manuscript. An electron microscope study of tissues from freshly killed dolphins. Special attention is given to the microvilli on many of the sensory cells. ¶ In Russian, translated by Joint Publications Research Service. The description of cochlear structures is brief and FIG. 1. A posterior view of a skull of Tursiops truncatus, show- indicates close similarities to terrestrial mammals. ing the vertical planes for right and left cochleas. 2381 Downloaded by guest on September 29, 2021 2382 Physiology: Wever et al. Proc. Nat. Acad. Sci. USA 68 (1971) Of 25 ears treated in the preliminary and final procedures, The large cochlear nerve is seen as it sends its bundles into good to excellent results were obtained in 7, and in 6 others the ganglionic masses in the different turns. The ganglia are the series were useful for such purposes as observations of the only partially enclosed in the bone of the modiolus in basal and width of the basilar membrane and the distribution of gan- lower apical regions, and in the upper apical region the glion cells. ganglion lies almost free in the scala tympani. The first step in the study of these ears was the graphic re- This picture indicates also the varying size of the cochlear construction of the cochlear spiral by Guild's method (6). structures from lower basal to upper apical regions. We see in The junctions between the inner and outer pillar cells were this progression a decrease in the cross-sectional area of the located for every cochlear turn cut tangentially, and these scala tympani, an increase in the area of the scala vestibuli, points were laid out on a graph along a chosen axis. Semicircles the greatly diminishing mass of the external spiral ligament, were drawn from centers on the axis to connect the appropriate a considerable increase in the width of the basilar membrane, points, yielding a good approximation to a spiral except for the and a moderate increase in the size of the tectorial membrane. two end portions. The end points were located and measure- ments were made between them and cochlear turns already Cochlear structure outlined, from which the extensions were drawn in. The result The features just mentioned, along with others, are better is an orthogonal projection to scale of the cochlear spiral, as seen in enlarged views of the different regions. Five such views represented for a particular ear in Fig. 2. Section numbers are given by the drawings and photomicrographs of Figs. 4-8, are shown on the left. which include two positions in the lower basal and one each in This ear contains a little over two cochlear turns, and the the other three half-turns. The locations along the cochlea of length of the basilar membrane, found by stepping off the all five figures are indicated by the numbered circles of Fig. 2. distances from the basal end as shown, is 38.5 mm. The con- (a) In the basal region there is no clear distinction between centricity of the constructed spiral indicates the accuracy of external sulcus cells and Claudius cells. These tall columnar orienting the block of tissue in sectioning. cells extend as a continuous row from the edge of the basilar membrane along the shallow sulcus to the thickest portion RESULTS of the spiral ligament. In the apical region, a distinction might All the suitable specimens were thoroughly studied, and all be made: the Claudius cells may be taken as those over the enter into our conceptions of the anatomical relations. For basilar membrane and the external sulcus cells as the ones simplicity of presentation, however, we mainly picture a single turning upward along the spiral ligament. specimen, the one whose spiral is given in Fig. 2. From the basal-end upward these cells undergo a progres- sive change in size, from a maximum height in the basal General orientation region around 145 /im to about 7 /Am in the upper apical A mid-modiolar section of the cochlea is shown at low power region. At the same time the epithelial strip greatly changes its in Fig. 3, in which the cochlear spiral is cut through at four form. places. Reference to Fig. 2 at the level of Section 158 will show Kolmer described these large cells in Phocaena as showing a that this number of cuts must occur, and will show also that series of infoldings along their sides, a feature that he con- these cuts are nearly transverse, i.e., are nearly perpendicular sidered usual in mammals. No such feature is seen in our to the course of the basilar membrane. better specimens. Something similar appears in our poorer As we follow the four cochlear regions of Fig. 3 from lower- specimens, which we consider to be an artifact. left upward and to the right, we encounter in order the lower (b) Boettcher cells are found in most mammals only in the basal, lower apical, upper apical, and upper basal half-turns. basal part of the cochlea as a compact group of low-lying The same order is seen in the spiral diagram in going from cells on the outer edge of the basilar membrane, overlaid by left to right at the level of Section 158. the Claudius cells. These cells in Tursiops are few at the basal .W If I 11 N /I I I .. Imvvl.,. D .0I.. a,C C/ FIG. 2. A graphic reconstruction of the cochlear spiral of the FIG. 3. Photomicrograph of a mid-modiolar section of the right ear of a specimen of truncatus. cochlea of a specimen from truncatus. (X 7) Downloaded by guest on September 29, 2021 Proc.
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