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The Tectorial Membrane of the Rat' The Tectorial Membrane of the Rat’ MURIEL D. ROSS Department of Anatomy, The University of Michigan, Ann Arbor, Michigan 48104 ABSTRACT Histochemical, x-ray analytical and scanning and transmission electron microscopical procedures have been utilized to determine the chemical nature, physical appearance and attachments of the tectorial membrane in nor- mal rats and to correlate these results with biochemical data on protein-carbo- hydrate complexes. Additionally, pertinent histochemical and ultrastructural findings in chemically sympathectomized rats are considered. The results indi- cate that the tectorial membrane is a viscous, complex, colloid of glycoprotein( s) possessing some oriented molecules and an ionic composition different from either endolymph or perilymph. It is attached to the reticular laminar surface of the organ of Corti and to the tips of the outer hair cells; it is attached to and encloses the hairs of the inner hair cells. A fluid compartment may exist within the limbs of the “W’formed by the hairs on each outer hair cell surface. Present biochemical concepts of viscous glycoproteins suggest that they are polyelectro- lytes interacting physically to form complex networks. They possess character- istics making them important in fluid and ion transport. Furthermore, the macro- molecular configuration assumed by such polyelectrolytes is unstable and subject to change from stress or shifts in pH or ions. Thus, the attachments of the tec- torial membrane to the hair cells may play an important role in the transduction process at the molecular level. The present investigation is an out- of the tectorial membrane remain matters growth of a prior study of the effects of of dispute. As will be made evident in the chemical sympathectomy upon the struc- Review of the Literature which follows, tures of the inner ear. None of the findings one can find support for almost any inter- of this prior study were more interesting pretation of the structure of the tectorial than those concerning the internal struc- membrane or its degree of attachment to ture and the attachments of the tectorial the organ of Corti. Although the tectorial membrane. In chemically sympathectom- membrane is generally accepted to be rich ized rats, the filamentous organization of in acid mucopolysaccharide, this point is the membrane was often remarkably evi- also a matter of some contention. dent ultrastructurally, and the membrane It was decided, therefore, to undertake showed a proclivity for remaining attached histochemical and scanning electron micro- to the tips of the hairs of the outer hair scopical research which might provide new cells. These results raised questions con- information on certain of the controversial cerning the chemical nature and attach- aspects of the tectorial membrane (chemi- ments of the tectorial membrane in un- cal nature, structure, and attachments) in treated rats, and whether or not these rats with developed auditory systems (rats properties had been altered by chemical beyond 14 days of age). It was hoped that sympathec tomy. new insights into the functions of the A search of the literature showed that membrane would result from elucidation the answers to the questions posed were of these particular points. not to be found there for, although the It became apparent, however, that a membrane has been extensively studied clearer understanding of the functional from the time of Corti (1851) to the significance of the tectorial membrane de- present, the origin, attachments, chemical pended not only upon such chemical or nature, physical appearance and functions 1 Supported by grant NB-07306 USPHS. AM. J. ANAT., 139: 449482. 449 450 MURIEL D. ROSS structural evidence as could be obtained thickness from one species to another, by the methods chosen, but also upon cor- (40 A, guinea pig, Engstrom and Wersa, relation of this data with that obtained by '58; 100 A, rat, Iurato, '60; variable, cat, biochemists working in the field of pro- Spoendlin, '57). However, Spoendlin ('57) tein-carbohydrate complexes. Biochemical pointed out that the filaments could be knowledge of such complexes has advanced artifactitious and Engstrom and Wersa rapidly in recent years and has reached a ('58) indicated that, because of their size, . point where its application to structures they cannot be the same as those observed such as the inner ear membranes could be with the light microscope. The last-named most enlightening, not only with respect to authors suggested that the tectorial mem- understanding tectorial membrane func- brane might be jelly-like with micellar tions in the normal auditory organ, but structures interspersed in some substance also in perceiving possible mechanisms which dissolves away in preparation of underlying some degenerative diseases of the tissue. the inner ear. The integration of histo- Scanning electron microscopy has gen- chemical, ultrastructural and biochemical erally revealed the tectorial membraue to data is, then, a further important aim of be smooth on much of its under side but this report. to be grossly fibrillar on its upper side and in the interior (Kosaka et al., '71; Lim, Review of the Literature '72). In his diagram, Urn ('72) showed From the earliest descriptions of its mi- the smooth regions as separate sheets, cor- croscopic appearance, the tectorial mem- responding to Hensen's stripe and to brane has been considered to be a fibrillar Hardesty's membrane. structure (Boettcher, 1859; Kolliker, 1854, All of the early investigators thought 1861; Waldeyer, 1873; Henle, 1880; Ret- that the membrane was attached to the zius, 1884). Many observers have con- epithelial cells of the entire organ develop- sidered the membrane to be comprised of mentally, but differed in their opinion of fibrils embedded in a gelatinous or amor- its degree of attachment in the adult. Thus, phous matrix (Retzius, 1884; Kolmer, '07; many have stated that the membrane was Hardesty, '08, '15; Keith, '18; Wislocki free, or "floated" over the organ of Corti and Ladman, '55; Iurato, '60; Lim, '72); in the adult (Kolliker, 1861; Helmholtz, to be stratified, or composed of lamellae in 1863; Waldeyer, 1873; Retzius, 1884; toto or in part (Henle, 1880; Held, '02, '09; Rickenbacher, '01; Hardesty, '08; Held, Shambaugh, '07; Prentiss, '13); or to be a '09; Kolmer, '07, '27). Waldeyer com- reticulum (Coyne and Cannieu, 1895; mented, however, that he occasionally Prentiss, '13). Still others have thought found the hairs of the outer hair cells im- that the fibrils were either products of co- bedded in the membrane and, after hard- agulation of endolymph (Czinner and ening in alcohol, sometimes found the Hammerschlag, 1897) or were continua- lamina reticularis carried away with the tions of the hairs of the hair cells (Ayers, membrane as it contracted. Boettcher 1891; Borghesan, '49; '52; Mygind, '52). (1859) indicated that the membrane did Recently, Borghesan ('71) suggested that not float free but was connected to the sur- the hairs are deeply embedded in the mem- face of the organ of Corti, an opinion brane, and that they are artifactitiously shared by Coyne and Cannieu (1895), elongated as the shrinkage forces pull the Kishi ('07), Shambaugh ('07) and Prentiss membrane away from the hairs. ('13). Prentiss was emphatic in stating Research carried out by phase contrast that he meant that the attachments were or with polarized light has suggested that to the entire surface of the organ of Corti, the tectorial membrane is a filamentous as occurred in the fetal state. Corti (1851), structure, with the filaments coursing at Boettcher (1859) and Lowenberg (1864) 30"-40" angles in an apical direction (A. considered the tectorial membrane to ex- Hilding, '52; Iurato, '60). Transmission tend beyond the organ of Corti, even to electron microscopy demonstrates that the the spiral ligament; Henle (1880) found membrane appears to be comprised of it attached just beyond the last row of hair slender filaments which vary somewhat in cells. Keith ('18) mentioned an attachment TECTORIAL MEMBRANE OF THE RAT 45 1 of the tectorial membrane to inner support- vergent results. Biochemical studies have ing cells as well as a peripheral connection indicated that the fibrils of the tectorial to outermost Deiters cells. Among more membrane are not comprised of collagen recent investigators, Wittmack ('36) main. (Bairati and Iurato, '57; Iurato, '60; and tained that the tectorial membrane at- Naftalin et al., '64) and are not related to tached to the hairs of both inner and outer keratin (Belanger, '56a). Naftalin et al. hair cells; such connections were also ('64) found the tectorial membrane to be found by von BCkCsy ('60) and Hawkins a gel which binds calcium and magnesium, and Johnsson ('68). According to Witt- with calcium the more firmly bound, and mack ('36), other attachments existed to to contain potassium in higher concentra- border cells and to Hensen cells. These tion than in extracellular fluid but lower results were supported by A. Hilding ('52), than in endolymph. They and others (Ayers, who also observed attachments to outer, 1891; Shambaugh, '07; Wittmack, '36) but not inner, hair cells. The peripheral noted the great sensitivity of the tectorial attachment of the tectorial membrane to membrane to the state of hydration. In- the reticular lamina (von BekCsy, '60), vestigators have found the tectorial mem- or to Hensen cells (Tonndorf et al., '62), has been described as firm, effectively brane to be PAS-positive (Wislocki and Lad- forming a seal between the organ of Corti man, '55; Belanger, '56a; Friberg and and the endolymph. Ringertz, '56; Igarashi and Alford, '69; Scanning electron microscopists have Vinnekov and Titova, '64). Results with found attachments of the tectorial mem- toluidine blue are in dispute. Wislocki and brane to various parts of the organ of Corti. Ladman ('55) and Friberg and Ringertz Kosaka et al. ('71) reported indentations ('56) found the membrane to lack meta- of the tips of the hairs of outer hair cells chromasia, but BClanger ('53, '54, '56a,b), in the tectorial membrane; Lim ('72) Plotz and Perlman ('55) and Tonndorf et found connections of the membrane to the al.
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