The Lateralis Organs and their Innervation inXenopus laevis

0 (From the Department of Zoology and Comparative Physiology, University of Birmingham) SUMMARY The innervation and general morphology of the lateralis organs of Xenopus laevis are described. Each group of organs is innervated by two large and two or fewer small fibres. Each of the large fibres gives off a branch to each of the lateralis organs in the group, but the branching of the small fibres is less regular. Each lateralis organ is therefore innervated by two large and up to two small fibres. The large fibres branch extensively at the base of the organ, the small fibres less so, and the nerve endings lie basal to or between the sensory cells. No terminal swellings could be seen. The endings of a particular fibre are not restricted to any one region of the organ. No special function could be assigned to the dual arrangement of the innervation. The original accounts of the structure of the lateralis organs were adequate. The recently suggested division of the supporting cells into three types is not justified. It is probable that a cupula exists on the lateralis organs but it could not be observed. It is suggested that the supporting cells secrete the cupula. - With one plate (fig. 4) separate from the roots of V, VII, and VIII (although its ganglion fuses with that of V and VII); most of the fibres separate out again distally and continue as the tractus supraorbitalis to the organs of the head and snout; a few run ventrally in the mixed ramus mentalis VII. The second, or posterior lateralis nerve, runs from a nucleus immediately posterior to that of the anterior nerve, forms a mixed ganglion with the vagus, then separates out again and runs to the skin alongside the main cutaneous blood-vessels. The details of the innervation near and in the lateralis organs have not hitherto been investigated. A trematode infection of the skin of Xenopus, which was restricted to the locality of the lateralis organs, was described by Elkan and Murray (1952). Those properties of the lateralis organs which have not been directly studied in Xenopus may be deduced from the properties of the homologous lateralis organs in other amphibians and fish. The embryology and experimental regeneration of the lateralis system are the main subjects of a review by Wright (1951) and the structure and function of the whole acousticolateralis system are surveyed by Dijkgraaf (1952). Details of the innervation of the lateralis organs have been studied in urodeles, but the results are contradictory. Retzius (1892) and Larsell (1929) both described the nerve-fibres as ending extracellularly between the sensory cells at the level of their nuclei; terminal swellings were found. On the other hand, Charipper (1928) and Chezar (1930) held that the endings were intracellular, with the fibres entering the bases of the sensory cells and ending in a cup-shaped network about the base of the nucleus. My investigation has been carried out in order to provide the anatomical background for an electrophysiological study of the function of the lateralis organs in Xenopus laevis (Daudin) (which will be published elsewhere). Certain of the electrical results are of interest in connexion with the innervation and will be referred to in the discussion. The arrangement and structure of the lateralis organs The lateralis organs are grouped together in small ridges or plaques which are arranged over the skin in rows, each row corresponding to a lateral 'line' in fish. The distribution of the plaques and the nomenclature of the rows adopted in this account are shown in fig. 1. In each plaque there are from three to twelve lateralis organs, arranged along its length alternately with tactile organs (Calabresi, 1924) (figs. 2 and 4, A). Each lateralis (or neuromast) organ consists of a rounded group of cells embedded in the epidermis, open to the external medium at the surface and separated from the basement membrane of the epidermis by a tenuous layer of epidermal cells (figs. 3 and 4, B). The opening at the surface is oval (with its long axis transverse to the long axis of the plaque) and is usually sunk slightly, and the base of the organ and therefore the basement membrane of the epidermis may extend down into the stratum spongiosum of the dermis. The dimensions of a typical organ are 70 /n from base to apex, 70 p. in the direction of the length of the plaque, and 100 /x across the plaque. Each lateralis organ contains two types of cell, sensory and supporting. The sensory cells, which are secondary sense cells, are pear-shaped and lie in the centre of the organ with the so-called sensory hairs at their apices; the elongated supporting cells occupy the rest of the organ on each side of and basal to the sensory cells, with their nuclei forming a layer round the base of the organ. FIG. I. The arrangement of the lateralis plaques in Xenopus laevis. Dorsal and ventral views of a typical adult female. METHODS Pieces of skin of recently pithed Xenopus were prevented from rolling up by laying them on card, and were then fixed. Nerve axons in serial paraffin sections were stained by Holmes's (1947) method after fixation in a 4% solution of formaldehyde in a saturated solution of mercuric chloride. Since this method did not prove very satisfactory in demonstrating the extreme tips of the fibres even when the buffer solution was of pH 8 7 or 9-0 (suggested by Holmespersonal communication), a modification of Bielchowski's method and a methylene blue method were attempted, but the initial results were not promising and the methods were not followed up. Other special techniques employed will be mentioned in their context. The innervation of the lateralis plaques Maurer (1895) stated that each plaque was supplied by its own small branch of the local lateralis nerve. This innervation has now been studied in greater detail. A typical plaque is innervated by two myelinated fibres of diameter 8-15 p.. Each of these fibres divides, and gives a branch to each of the lateralis organs of the plaque, with the result that each organ is supplied by two fibres. The arrangement of this branching is very regular and may even present a Lateralis Organs and their stratum two lateralis cutaneous compactum nerve fibres nerve FIG. 2. A lateralis plaque, showing the arrangement of the lateralis and tactile organs and their nerves (diagrammatic longitudinal section). FIG. 3. A single lateralis organ, showing its situation in the epidermis and the relationships of the sensory and supporting cells (diagrammatic). 'tramline' appearance (figs. 2 and 4, A). This two-fibre system has been traced in serial sections of individual plaques from the circumorbital and maxillary rows, from the anterior and posterior regions of the middle lateral row, and from the median ventral row. As well as by the two large fibres, the plaque may be innervated by a variable number of small, myelinated fibres of diameter 1-5 /*. In those plaques which were most intensively s (...truncated)