Development of the lateral line system in Xenopus

Abstract

The lateral line system of fishes and amphibians consists of numerous epidermal mechano-receptors which are distributed over the whole body surface. As in other amphibians, the lateral line system of Xenopus develops from epidermal placodes situated on the head region of the embryo. The dorsolateralis placodes form a rostro-caudal series of epidermal thickenings centered around the otic placode. In this series, placodes remaining within the epidermis and forming lateral line primordia alternate with lateral line ganglion forming placodes. Each lateral line primordium elongates and migrates within the epidermis along a well-defined pathway, leaving behind a row of small cell groups, the primary lateral line organs. As the ganglion which supplies a given row of organs and the corresponding lateral line primordium originate in spatial contiguity, and as the axons of the lateral line nerve grow out together with the migrating primordium, the lateral line neurones remain in contact with their target cells throughout development. After segregation of a primary organ from a migrating primordium, cell differentiation occurs. Receptor cells establish afferent and efferent synaptic contacts with axons from the lateral line nerve. Apically, a bundle of stereocilia and a single, microtubule-containing kinocilium protrude from the surface of a receptor cell into a jelly-like cupula, which extends into the surrounding fluid. Displacement of the cupula and the concomitant bending of the cilia stimulates the receptor cells. The cilia of a receptor cell are asymmetrically arranged, and this structural polarity is related to the directional sensitivity of the cells. Two types of receptor cells, with opposite orientations, are intermingled within each organ, giving the whole organ a bidirectional sensitivity. The number of lateral line organs is increased by the process of accessory organ formation, where primary organs grow and divide to produce secondary organs. In this way, existing rows of organs are extended. Moreover, single primary organs are transformed into elongate plaques of closely apposed organs. The lateral line system has reached its greatest extent at late larval stages. During metamorphosis, the number of organ plaques is reduced in some lines, and one line even disappears completely. Two large, myelinated afferent fibers innervate a whole organ plaque. They branch repeatedly to supply every organ of the plaque, and each fiber is thought to innervate only receptor cells of the same polarity. In addition to these afferent fibers, a few unmyelinated efferent fibers and, in the adult, 0–3 small myelinated efferent fibers supply each organ plaque. The development of the supraorbital (SO) system of lateral line organs has been studied in detail. The SO primordium elongates along the dorsal margin of the eye to form a streak of cells in the inner layer of the epidermis. Both an increase in cell number, and a rearrangement of cells in the plane of the epidermis contribute to this elongation. The elongate SO primordium becomes fragmented, from proximal to distal, into a series of small cell groups, the primary lateral line organs. The initial size of these organs is not adjusted to the overall size of the primordium. From experimentally diminished SO primordia, truncated SO systems develop which contain fewer organs than normal. Due to the small cell numbers involved, the initial growth of the SO system can be quantitated by directly counting cells. Two growth phases can be discerned. Between the beginning of primordial elongation and the completion of primary organ development, cell number increases linearly with time. The second growth phase is associated with accessory organ formation. Different primary organs grow at very different rates, and their final size may range from 6 to 64 cells. The frequency distribution of these final organ sizes is not smooth, but exhibits a regular series of distinct peaks. Nine peaks are observed, with the first peak at an organ size of 8 cells/organ, with a distance of 7 cells/organ between neighbouring peaks, and with the relative size of the peaks approximating a binominal distribution. This surprising regularity in the frequency distribution can be explained by the interference of the process of organ segregation with a specific cell division programme of the SO system involving a predetermined number of asymmetric stem cell divisions. The presence of such a rigid cell division programme in a vertebrate is unexpected.