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A Scanning Electron Microscopic Study of the Sacculus and Lagena in the Ears of Fifteen Species of Teleost Fishes

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A Scanning Electron Microscopic Study of the Sacculus and Lagena in the Ears of Fifteen Species of Teleost Fishes A Scanning Electron Microscopic Study of the Sacculus and Lagena in the Ears of Fifteen Species of Teleost Fishes ARTHUR N. POPPER Department of Zoology and Laboratory of Sensory Sciences, Unioersity of Hawaii, Honolulu, Hawaii 96822 and Kresge Hearing Research Institute, University of Michigan Medical Center, Ann Arbor, Michigan 48109 ABSTRACT The ulstrastructure of the saccular and lagenar maculae were studied in 15 species of teleost fishes, using the scanning electron microscope. Particular attention was paid to hair cell orientation patterns, composition of the ciliary bundles on the hair cells, hair cell distributions, and supporting cell types. The hair cells on both otolithic organs are divided into several groups with all of the hair cells in each group oriented in the same direction. The posterior region of the saccular macula in all species had dorsally oriented hair cells on the dorsal half of the macula and ventrally oriented hair cells on the ventral half. The cells on the anterior end of the macula were oriented anteriorly and poste- riorly, with the posterior group, in most species, being on the dorsal half of the anterior region of the macula. There was considerable inter-specific variation upon this basic pattern. Inter-specific variation on the lagenar macula was considerably less than on the saccular macula. The basic pattern in all of the species includes one dorsal cell group and one ventral cell group. There are four more-or-less discrete ciliary bundles, each varying in the rela- tive size of the kinocilia and stereocilia. Intermediary forms were also observed, making it difficult to differentiate ciliary bundles in some instances. It was ap- parent, however, that several of the ciliary bundles were found in particular macular regions. Interest in sound detection by teleost fishes capabilities of the ear (if any), and responses has increased markedly over the past several of the ear to sound source direction. decades (see reviews by Lowenstein, '71; Pop- The teleost ear (fig. 1) consists of three per and Fay, '73; Tavolga, '71) and we now semicircular canals and associated ampullary have a large body of data on detection mecha- regions, and three otolith-containing vesicles. nisms and capabilities, as well as on sound Two of these vesicles, the sacculus and lagena, processing at several levels of the auditory are associated with audition (von Frisch, '36) systems. One area that is now of particular in many species, although their specific con- interest is the role of the inner ear in sound tributions are still unknown (see Fay, '75; detection and processing (e.g., Enger, '63, '73; Furukawa and Ishii, '67). Enger et al., '73; Fay, '75; Fay and Popper, '74, Each otolith-containing vesicle has a senso- '75; Furukawa and Ishii, '67; Sand, '74). How- ry hair cell covered epithelium, or macula, in ever, the meaning of inner ear data, in terms close proximity to a single dense calcareous of the function of the ear, is still unclear be- otolith. The macula and otolith are separated cause of a lack of detailed knowledge of the by a thin otolithic membrane that may hold morphology and ultrastructure of the audito- the otolith in place on the macula and provide ry regions. These data are needed before a mechanical coupling between the otolith and detailed analysis can be made of responses of sensory hairs. The actual mechanisms for re- the inner ear to sound stimulation, analytic sponse to acoustic stimulation in the ear of J. MORPH., 153: 397-418. 397 398 ARTHUR N. POPPER Ahbreoiations aa, anterior ampulla k, kinocilium mu, utricular macula ap. posterior ampulla rn, microvilli pl, lagena ca, anterior canal ms. saccular macula s. sacculus cp, posterior canal st. stereocilia Fig. 1 Drawing (modified from Retzius. 1881, of a medial view of the right ear of Snlrno salur. fishes have not been directly studied, but it generally contains the typical 9 + 2 filament has been suggested that a sound field would pattern found in many metazoan flagella. cause the body of the fish (and the sensory Maximum hair cell depolarization occurs macula) and the considerably denser otolith when shearing is along the cilia towards the to move out of phase with one another, result- kinocilium, and the response is inhibited ing in bending of the cilia on the hair cells when stimulation is reversed 180". Stimula- (e.g., van Bergeijk, '67a; Wever, '69, '71). tion off this axis gives a response whose level The sensory hair cells consist of a cell body is a cosine function of the stimulus direction with a series of cilia on the apical surface. A relative to the axis of maximum response number of workers have provided evidence (Flock, '65, '71). that bending or shearing action on the cilia is Since the hair cells of the inner ear are responsible for the electrical response from functionally polarized, it is likely that this the hair cells (e.g., Bekesy, '60; Lowenstein could significantly affect auditory capabilities and Wersall, '59). Each ciliary (or hair) bun- and mechanisms. In fact, experiments have dle consists of many (30-50 in fishes) stereo- shown that the goldfish (Carassius auratus) cilia which are embedded in a thick cuticle sacculus has hair cells oriented in opposite di- that lies just under the apical cell membrane. rections, resulting in hair cell groups that re- A single, eccentrically placed kinocilium orig- spond to opposite phases (compression and inates inside the cell at the basal body and rarefaction) of a stimulating signal (Furu- penetrates the cell membrane. The kinocilium kawa and Ishii, '67; Piddington, '72). Recent SACCULUS AND LAGENA IN FISHES 399 work with perch (Perca fluviatilid and had- data are available. Furthermore, while we dock (Melanogrammus aeglefinus) has also have a limited idea regarding the functional demonstrated that different regions of the significance of bi-directionality in the saccu- saccular macula have their best responses to lus of the goldfish (Furukawa and Ishii, '671, it stimulation in different directions (Enger et is difficult to extrapolate from this to other al., '73; Sand, '741, again suggesting that in species. The present study is directed towards the inner ear there is a functional polariza- expanding our understanding of the ultra- tion which may be involved with detection of structure of the teleost sacculus and lagena sound source direction. through a scanning electron microscopic Data on hair cell orientation patterns in the (SEMI study of these organs in 15 species. inner ear of fishes show significant correla- While these data are not in any way repre- tions with the physiological data. Furukawa sentative of all (or even most) taxonomic and Ishii ('67), partially on the basis of the groups, they do give a fairly comprehensive biphasic response to sound stimulation in the indication of the variation in ultrastructure eighth nerve, hypothesized the presence of op- and enable us to suggest some general ideas positely polarized hair cell groups in the gold- on the auditory function of the teleost ear. fish sacculus. This hypothesis has been cor- roborated by Hama ('69) and Platt ('771, who MATERIALS AND METHODS have shown that most hair cells on the dorsal Data were obtained on the ultrastructure of half of the saccular macula in goldfish are the saccules and lagenae of 15 species of fish polarized dorsally (kinocilium on the dorsal representing 10 families. The species were side of the cells) while cells on the ventral selected on the basis of availability, although half of the macula are polarized ventrally. Bi- attempts were made to use species that directional orientation has been reported for showed taxonomic and ecological variability five species of catfish (Jenkins, '74), a group in and also to include a number of species for the same superorder (Ostariophysi) as the which sound detection and/or production data goldfish, and for the burbot (Lota vulgaris) by are available. Table 1 lists the species used as Wersall et al. ('65). well as data on number of animals, sizes, and, The data for the Ostariophysi and Lota where available, citations relating to acoustic closely resemble the bi-directional orientation behavior for these or related genera. pattern found in the saccules of tetrapods Animals were anesthetized with MS-222 (e.g., Lewis and Li, '75; Lindeman, '69; (Sandoz) until they were immobile and then Spoendlin, '65) and the elasmobranch Raja one of two procedures was followed. Animals clauata (Lowenstein et al., '64). However, from 5-20 cm in standard length were placed these data differ somewhat from recent data into a special dissection holder which permit- for a salmonid fish, the lake whitefish, Cor- ted respiration during dissection, thus en- egonus clupeaformis, (Popper, '761, the cod, abling a long dissection time. Specimens out- Gadus morhua, (Dale, '76), and two species of side of this range were decapitated, since they flatfish, Pleuronectes platessa and Limanda did not fit the available holder. In all cases limanda, (Jsrgensen, '76). While the posterior the cranium was opened dorsally, the brain re- saccule in Coregonus and the flatfish have dor- moved by dissection and aspiration, and the sal and ventral hair cell groups, as in other ears exposed. The sacculi in most species were species, the anterior-dorsal saccular quadrant then opened dorso-laterally with a sharp has posteriorly oriented cells and the anteri- blade, and chilled fixative (4%glutaraldehyde or-ventral quadrant has anteriorly oriented in S-collidine buffer for fresh water species; cells. The pattern in Gadus is similar except the same buffer with 4% sucrose for salt water that horizontally oriented cells are also found animals) was perfused into the ears and cra- on the posterior end of the saccular macula. nial cavity for four to eight minutes.
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