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The Labyrinthine Sense Organs of the Frog

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  • Proc. Nat. Acad. Sci. USAVol. 70, No. 2, pp. 498-502, February 1973

    The Labyrinthine Sense Organs of the Frog(otic labyrinth/ear/amphibia)

    ERNEST GLEN WEVER

    Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540

    Contributed by Ernest Glen Wever, December 6, 1972

    ABSTRACT A study of the macula and crista organsof the frog's labyrinth with the use of an improved methodof histological preparation has shown these endings to bemore complex than heretofore believed. The structure ly-ing over the layer of sensory and supporting cells is not asingle "gelatinous" body as commonly described, but con-sists of two distinct layers with separate functions.In all these endings-macula sacculi, macula utriculi,

    macula lagenae, and the cristae of the three semicircularcanals-there is a special tectorial structure that lies overthe cellular surface and makes the connections to the cil-iary tufts of the hair cells. It has the general form of a re-ticulum, though in the saccule it is somewhat elaborated.A preliminary study of other vertebrates indicates that

    this tectorial reticulum is present in all the labyrinthineendings throughout the series from fishes to mammals.Consideration is given to the possible advantages of this

    special tectorial structure in the stimulation process.

    Three types of sensory endings are present in the otic laby-rinth. These are the papilla acustica (in advanced forms calledthe cochlea), the macula acustica, and the crista acustica.The papilla acustica is lacking in the fishes, and makes itsfirst appearance in the amphibians, and in most species of thisgroup there are two types, the papilla basilaris and the papillaamphibiorum; in all higher animals there is one type only.Three principal forms of the macula occur, the macula sacculi,macula utriculi, and macula lagenae, though the last-namedis lacking in the higher mammals and in a few other species.A macula neglecta is present in several forms, but is of smallsize and uncertain function, and will not be considered furtherhere. A crista is present uniformly in the ampulla of each ofthe three semicircular canals from fishes to mammals.Our understanding of the general structure of these organs

    arose out of the studies of the early anatomists, and perhapsreached its clearest formulations in the descriptions of Retziusin 1881 and 1884 (1). Extensive investigations performedsince, with the aid of electron microscopy, have added a wealthof fine details but yet have brought no important change inthe basic picture.These endings continue to be described essentially in the

    language of Retzius as consisting of two layers of tissue, onean array of hair cells held in a framework of supporting cellsand the other a covering layer usually characterized as gelat-inous and varying greatly in form in the three types of end-ings.The object of the present report is, first, to show that in all

    these endings the covering of the cellular elements consists oftwo distinct layers of tissue and not a single one, and then toconsider the particular functions of these separate structures.The observations are an offshoot of a study of the auditory

    papillae of the frog, a study that necessitated the develop-

    ment of improved methods for the histological treatment ofamphibian ears. These observations, described in detail else-where*, showed that the auditory papillae always include aspecial tectorial structure lying close over the ciliated ends ofthe hair cells, making connections with their ciliary tufts, andclearly involved in the stimulation process. This situation ledto the question whether some corresponding structures mightbe present in the nonauditory endings as well. These struc-tqres were looked for, and found to be present.

    In all four types of labyrinthine endings, in the utricularmacula, lagenar macula, saccular macula, and the cristae ofthe semicircular canals, there is a tectorial structure in theform of a fiber network, or for the saccular macula a form thatseems to be an elaboration of such a network. This structurealways lies above the surface membrane that represents theexposed ends of the hair cells and supporting cells, and hassuperimposed on it a structure that for the macular endingsis an otolithic mass and for the cristae is a further tectorialbody known as the cupula. The descriptions below referspecifically to Rana pipiens.

    The Utricular Reticulum. The tectorial structure lying overthe utricular hair cells varies somewhat in its different re-gions. In some places, especially toward the edges of the mac-ula, there is only a simple network, as shown in the photomi-crograph of Fig. 1 and in the drawing of Fig. 2.

    This network consists of an upper limiting membrane andan array of more or less vertical fibers that extend to thesensory surface below and sometimes at least attach to thissurface membrane. The limiting membrane is a loose networkwhose round, oval, and sometimes polygonal openings canbest be seen when the view is from one side. Fig. 3 shows thismembrane obliquely, and both the upper limiting network andthe vertical fibers can be seen. As will be noted, some of thesevertical fibers make connections with the tips of the ciliarytufts of the hair cells.

    In some regions, and especially in the middle of the macula,the structure is more complex. The vertical fibers are oftenconnected to one another by short and usually fine transversestrands, which sometimes branch and interconnect so that thewhole constitutes an open spongework of spaces in a three-dimensional lattice.

    In some places also the vertical fibers are expanded as nar-row ribbons or even as small, irregular sheets, and the spacesof the lattice then take on the appearance of shallow recessesor canals with imperfect walls.

    * Wever, E. G., "The ear and hearing in the frog, Rana pipiens,"to appear.

    498

  • The Labyrinthine Sense Organs of the Frog 499

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    FIG. 1. A photomicrograph of a portion of the utricular mac-ula of the frog, Rana pipiens, seen in cross section. For identifica-tion of the elements, see the next figure. Scale X 500.

    Careful examination at high magnification shows that mostof the ciliary tufts connect to the vertical fibers of the network,and it is likely that all of them either connect in this way orconnect more directly through their kinocilia to the strandsof the limiting membrane.Above the tectorial structure and resting on its limiting

    membrane is the otolithic mass, which in the utricle is com-paratively flat, reaching a height of only about 20 Mm. Thisotolithic structure consists of numerous crystals of calciumcarbonate in apparently random orientations in a matrix ofmaterial usually referred to as gelatinous. This material stainsdifferently from tectorial tissues with the procedures usedhere, and clearly is an entirely separate substance. Probably itis a thin gel in the living animal, but in fixed sections it appearsas a cloudy particulate matter in which the crystals seemfirmly embedded.

    It is important to note that the otolithic crystals are alwaysfound in the ground substance and never appear below thelimiting membrane of the tectorial structure.

    The Lagenar Reticulum. In the macula of the lagena thetectorial structure is closely similar to the one just described,but in some respects is a little further developed.

    In most regions the limiting membrane is a meshwork,but in others this membrane is better described as a perforatedsheet. In a limited area, in the middle of the macula, this sheethas only a few openings and thus has a rather solid appearance.Fig. 4 gives a view looking obliquely into the deep recess inwhich this ending is located, and shows a portion of the per-forated membrane with several ciliary tufts projecting throughthe openings.As seen in cross section, the lagenar reticulum has much the

    same form as this structure in the utricle. The vertical fibersthat extend between the limiting membrane and the sensorysurface are rather thick, and for the most part take curvedcourses. Many of the ciliary tufts attach to these fibers, othersconnect by fine threads (perhaps their kinocilia) to the limitingmembrane itself.

    In some regions there are cross fibers uniting the verticalstrands and making up a well-defined network extendingthrough the region close to the hair-cell layer. Also, to an

    FIG. 2. A drawing of part of the same specimen shown in thepreceding figure. Scale X 1000.

    extent greater than in the utricle, the vertical strands in someareas are expanded into ribbons or narrow sheets that encloserather well-defined compartments. These compartments seemalways to be open on the lower end, over the hair cells, andmany of the ciliary tufts extend into these openings.The otolithic mass is more extensive than in the utricle,

    but its composition and relations to the tectorial tissues areessentially the same.

    The Saccular Structure. In the saccule the tectorial layercan still be regarded as a reticulum, though a considerably

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    FIG. 3. A photomicrograph of a part of the utricular macula,from a frontal section that passed through the organ somewhatobliquely. Above is the otolithic layer, with two dark massesrepresenting crystals somewhat out of focus, and below are the haircells with their large nuclei. Between is the tectorial layer with itsnetwork of fibers, some of which connect to the ciliary tufts of thehair cells. Scale X 1000.

    Proc. Nat. Acad. Sci. USA 70 (1973)

  • Proc. Nat. Acad. Sci. USA 70 (1973)

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    I'w w9*__MFIG. 4. Photomicrograph of the lagenar macula of Rana pip-

    iens, in a view looking obliquely down o

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