Development of lateral line organs in leptocephali of the freshwater eel Anguilla japonica (Teleostei,Anguilliformes)

A study of the ontogeny of the lateral line system in leptocephali of the Japanese eel Anguilla japonica reveals the existence of three morphologically different types of lateral line organs. Type I is a novel sensory organ with hair cells bearing a single kinocilium, lacking stereocilia, distributed mainly on the head of larvae, and morphologically different from typical superficial neuromasts of the lateral line system. Its developmental sequence suggests that it may be a presumptive canal neuromast. Type II is an ordinary superficial neuromast, common in other teleost larvae, which includes presumptive canal neuromasts that first appear on the trunk and accessory superficial neuromasts that later appear on the head and trunk. Type III is a very unusual neuromast located just behind the orbit, close to the otic vesicle, with radially oriented hair cells, suggesting that these serve as multiple axes of sensitivity for mechanical stimuli. The behavior of larval eels suggests that the radially oriented neuromasts may act as the sole mechanosensory organ until the ordinary superficial neuromasts develop. The finding that larval eels possess a well-developed mechanosensory system suggests the possibility that they are also capable of perceiving weak environmental mechanical stimuli, like other teleost larvae.     

VISION AND SENSORY PHYSIOLOGY The lateral line systems of three deep-sea fish

The distribution and ultrastructure of the lateral line systems in three taxonomically dispersed deep-sea fish are described: Poromitra capito, Melanonus zugmayeri and Phrynichthys wedli. They are meso- to bathpelagic and are thought to feed on small crustaceans and fish. All possess highly developed lateral line systems, a feature associated with life in the deep sea. Poromitra capito and M. zugmayeri exhibit widened head canals which are connected to the outside by large pores and which contain around 60 large neuromasts. Each neuromast consists of a cupula, shield-shaped mantle and a sensory plate containing hundreds to thousands of hair cells. Direction of sensitivity is in the long axis of the canal (perpendicular to the long axis of the mantle). Depending on their position on the sensory plate, the hair cells have different morphologies. They fall into three basic classes which, from comparison with past work, may be tuned to different frequencies. Alternatively, the various hair cell morphologies could be interpreted as being members of a developmental or growth sequence. Phrynichthys wedli has no canal organs, these being replaced secondarily by many superficial neuromasts placed on prominent papillae in rows which cover much of the 'head' and body. Direction of sensitivity is along the axis of the neuromast row. An extreme proliferation of superficial neuromasts are also found on the heads of P. capito and M. zugmayeri and these are of a type not described before. They consist of stitches, raised on papillae in M. zugmayeri and several mm long in P. capito , in which continuous lines of hair cells, two to three cells wide, are embedded. Direction of sensitivity is perpendicular to the long axis of the stitch. Based on the structure and direction of sensitivity, possible functional implications of all the neuromast types described are compared and discussed.     

Sensory structures at the surface of fish skin. II. Lateralis System

Scanning electron microscopy shows the form of the cupulae of free neuromasts in two species of teleost fish, and gives information about the organization of the free neuromasts in teleosts and lampreys. In lampreys some neuromasts were found to lack the surrounding moat and the flanking hillocks characteristic of the lateral line organs previously described in these fish. In all cases, the sensory cells had the kinocilium aligned with respect to the stereocilia on the longer axis of the neuromast surface, thus enabling the direction of effective stimulation of the free neuromasts to be deduced from their morphological arrangement.     

Development of free and canal neuromasts and their directions of maximum sensitivity in the larvae of ayu,Plecoglossus altivelis

Morphological changes in free neuromasts are reported from larvae of the Ayu,Plecoglossus altivelis. In newly-hatched larvae, free neuromasts were already recognizable in both the head and trunk. During larval growth, the number of free neuromasts increased, and the number of its sensory cells 2 days after hatching was constant. In the trunk, two types of free neuromasts, one with maximum sensitivity in the antero-posterior direction and the other with maximum sensitivity in the dorso-ventral direction, were observed. The former type predominated. In the head, free neuromasts were located around the eye and nose, their directions of maximum sensitivity forming lines tangential to concentric circles about the eye and nose. Distinct changes in free neuromasts occurred during the formation of the canal organ. The canal organ was first observed in the head region 64 days after hatching and in the trunk region 100 days after hatching. Concomitant with the formation of the canal organ, the profile of the cupulae of the free neuromasts changed from a flat bar to semispherical. Sensory cells in the canal neuromasts did not differ morphologically from those in the free neuromasts. It is considered that there is a close relationship between the sensitivity of the neuromast and the shape of the cupula, i.e., that the free neuromasts are adapted to slow water flow, as in lakes and the sea, while the neuromasts in the canal organ are adapted to rapid water flow.     

Surface and subsurface structures of neuromasts in tadpoles of the crab-eating frog, Rana cancrivora

Neuromast structure in Rana cancrivora larvae was observed by scanning and transmission electron microscopy. Neuromast units, each being composed of two or three neuromasts, are arranged in several well-defined lines in the head, body, and tail regions. The structure of neuromasts in these three regions is basically identical. The neuromast is composed of sensory, sustentacular, and mantle cells. The top of each neuromast has a hillocklike appearance, and is surrounded by four to six epidermal cells with tight intercellular junctions. Long kinocilia and many stereocilia occur in the apex of the neuromasts and are surrounded by numerous microvilli. Numerous granules are present on the apical portions of the mantle and the sustentacular cells. Four or five trapeziform mantle cells are connected closely with each other to form the shell of the neuromast. Large intercellular spaces occur between the mantle cells and the cells of the inner epidermal layers, and between the cells of the inner epidermal layer. Thus, at the apical parts of the neuromast intercellular junctions are tight and the intercellular spaces are more dilated in more basal areas. Morphologically the neuromasts of R. cancrivora larvae resemble those of generalized pond anurans, based on the grouping of Lannoo (Journal of Morphology 191:115-129, 1987a), although larvae of this species inhabit brackish water.     

Neuromast formation in the prehatching embryos of the Japanese flounder (Paralichthys olivaceus)

The present paper clarifies the initial development of the lateral line organs in the embryonic Japanese flounder, Paralichthys olivaceus. The first appearances of lateral line primordia, and the proliferation, distribution and morphological development of the free neuromasts, including nerve ending formation: establishment of hair cell innervations via the formation of synapses, were examined by light microscopy, scanning and transmission electron microscopy. The first pair of neuromast primordia appeared in the otic region ≈ 30 h prior to hatching and subsequently differentiated into free neuromasts, otic neuromasts, after ≈ 8 h. At hatching, a pair of free neuromasts and three pairs of neuromast primordia were present on the head, and three pairs of neuromast primordia were present on the trunk. The hair cell polarity of the otic neuromast until just prior to hatching was radial, but not bi‐directional. The typical afferent and efferent nerve endings in the otic neuromasts had formed by the time of hatching, suggesting that the otic neuromasts are functional prior to hatching. The three neuromast primordia located on each side of the trunk were derived from a long, narrow ectodermal cell cluster and erupted through the epidermis after hatching.     

Pit organs in axolotls: a second class of lateral line neuromasts

The lateral line system of axolotls (Ambystoma mexicanum) consists of mechanoreceptive neuromasts and electroreceptive ampullary organs. All neuromasts in salamanders are located superficially and are organized into lines that are homologous to canal neuromasts in fishes. Ampullary organs are confined to the head and generally are located adjacent to the lines of superficial neuromasts. Axolotls, however, also possess a third class of receptors; these form restricted patches on the head and are possibly homologous to the superficial pit organs in fishes. In order to test this hypothesis the morphology of the suspected pit organs was examined with scanning electron microscopy, and a number of their physiological properties were determined. Pit organs are approximately half the size of neuromasts and have fewer hair cells, although these hair cells do possess kinocilia and stereocilia like those of neuromasts. Pit organs also possess cupulae and exhibit a pattern of innervation identical to that of neuromasts. Pit organs and neuromasts also exhibit similar rates of spontaneous activity, are excited by weak water currents but not weak electric stimuli, and are not inhibited by magnesium ions. Pit organs appear to have slightly lower rates of spontaneous discharge than neuromasts, however, and have slightly lower displacement thresholds to low frequency wave stimuli. These data support the contention that the pit organs of axolotls constitute a second class of neuromasts homologous to the pit organs of fishes.     

Topography and mechanics of the cupula in the fish lateral line. I. Variation of cupular structure and composition in three dimensions.

The cupula of the supraorbital neuromast in the lateral line canal of the clown knifefish contains vertical columns. In the central region of the cupula overlying the macula, these columns are densely packed, are relatively constant in size, and run from the base of the cupula to the surface of the cupula which is exposed to canal fluid. There are two types of columns, dark and light, which form elliptical compartments in planes of section that cut across the columns; the cupula therefore has the appearance of mosaic tile in such sections. The dark compartments contain tubules that extend from the base of the cupula at the junction with the macula to the top of the cupula. Each tubule is associated with the kinocilium of a single hair cell. The lateral parts of the cupula, not overlying the macula, also contain compartments, but these compartments differ in size and structure from those in the central region. In addition to the compartments, the central region of the cupula also contains spherical aggregates of droplets. These small aggregates, termed mora, are found principally in a layer within the central region of the cupula, but are also found outside this layer. Because of their light-reflecting properties, the mora can be used for noninvasive optical measurements in vivo of the motion of the cupula.     

Fine structure of the ordinary lateral line organ

Summary The lateral line organ of the spotted shark is characterized by its semi-cylindrical shape. Each organ (neuromast) is so closely apposed to the next that the individual neuromasts are almost continuous. The neuromast is composed of receptor cells, supporting cells and mantle cells. The receptor cells bear one kinocilium and up to 40 stereocilia. Bi-directional arrangement of the receptor cells as occurs in teleosts was demonstrated. Afferent and efferent nerve endings were found at the base of the receptor cells. The supporting cells extend from the basal lamina to the free surface. Long microvilli and a cilium-like ciliary rod project from the top of each supporting cell. The cell contains relatively few elements of the Golgi apparatus and little rough endoplasmic reticulum, but mitochondria and filaments are abundant. The mantle cell limits the lateral margin of the neuromast. It is distinguished from the supporting cell because of its long crescent-shaped nucleus and scarce, short microvilli. Myelinated nerve fibres are found in the subepithelial connective tissue but not in the epithelium.The fine structure of the shark lateral line organ suggests that this organ is in an intermediated step of evolution between that of lamprey and teleost.     

Regeneration in zebrafish lateral line neuromasts: expression of the neural progenitor cell marker sox2 and proliferation-dependent and-independent mechanisms of hair cell renewal

Mechanosensory hair cells are essential for audition in vertebrates, and in many species, have the capacity for regeneration when damaged. Regeneration is robust in the fish lateral line system as new hair cells can reappear after damage induced by waterborne aminoglycoside antibiotics, platinum-based drugs, and heavy metals. Here, we characterize the loss and reappearance of lateral line hair cells induced in zebrafish larvae treated with copper sulfate using diverse molecular markers. Transgenic fish that express green fluorescent protein in different cell types in the lateral line system have allowed us to follow the regeneration of hair cells after different damage protocols. We show that conditions that damage only differentiated hair cells lead to reappearance of new hair cells within 24 h from nondividing precursors, whereas harsher conditions are followed by a longer recovery period that is accompanied by extensive cell division. In order to characterize the cell population that gives rise to new hair cells, we describe the expression of a neural stem cell marker in neuromasts. The zebrafish sox2 gene is strongly expressed in neuromast progenitor cells, including those of the migrating lateral line primordium, the accessory cells that underlie the hair cells in neuromasts, and in interneuromastic cells that give rise to new neuromasts. Moreover, we find that most of the cells that proliferate within the neuromast during regeneration express this marker. Thus, our results describe the dynamics of hair cell regeneration in zebrafish and suggest the existence of at least two mechanisms for recovery of these cells in neuromasts.     

Neuromast topography in anuran amphibians

Generalized anuran tadpoles across families exhibit a similar neuromast morphology on their heads, as follows: (1) all neuromast lines known for anurans are present; (2) within these lines total neuromast number ranges from about 250 to 320; (3) neuromasts form linear stitches composed of two to three, but sometimes up to five, neuromasts; (4) neuromast linear dimensions are ? 10 μm; and (5) neuromasts contain ? 15 hair cells. Compared with generalized forms, stream, arboreal, carnivorous, and desert-pond forms have fewer neuromasts but they contain more hair cells. They do not, however, form stitches. Obligate midwater suspension-feeding forms, including Xenopus (Pipidae), Rhinophrynus (Rhinophyrnidae), and Phrynomerus (Microhylidae), form stitches that contain > six, but potentially up to 18 or more, loosely aggregated neuromasts. Xenopus and Rhinophrynus have large neuromasts (up to 40 μm across). Chiasmocleis (Microhylidae) tadpoles form stiches that are linearly arranged with up to ten neuromasts. Whereas urodeles can have more than one neuromast row per line and may form both linear and transverse stitches, anurans have only one row of neuromasts per line and form only transverse stitches. Neuromasts in anurans tend to be smaller and more circular than in urodeles and positioned flush with the epidermal surface. A greater percentage of anurans form stitches, and anurans have greater intrafamilial variation in stitch formation than do urodeles.     

Structures transmitting stimulatory force to the sensory hairs of vestibular ampullae of fishes and frog

Summary Serial sections of the vestibular ampullae of two species of fish and one species of frog were investigated by electron microscopy. The kinocilium is the only connection between the sensory cells and the auxiliary structure (cupula). The cupula possesses canals that traverse its entire height. Each canal contains a single kinocilium in its proximal part; distally, it is filled with material that stains with colloidal silver. The matrix of the cupula consists of filaments running perpendicular to the canals. These filaments do not stain with colloidal silver. The kinocilium is connected to the wall of the canal via structures that differ in the studied species of fish and frog. The filamentous links between the kinocilium and the longest stereovilli of the sensory hair bundle are similar in all the investigated species. The stereovilli are interconnected by basal and shaft links, and by horizontal and oblique tip connectors, similar to those described by other authors for macula organs and the organ of Corti, although differences in structural details, especially of the horizontal tip and the shaft connectors, are present. Some of these are species specific and some are related to the position of the sensory cell in the epithelium and/or specific to the organ (ampulla or macula organ). Some attachment sites of the links are associated with osmiophilic submembranous material. These differences in the structure, distribution and attachment sites of the links are possibly of functional importance.     

Ultrastructure of the lateral-line sense organs of the ratfish,Chimaera monstrosa

Summary The ultrastructure of the lateral-line neuromasts in the ratfish, Chimaera monstrosa is described. The neuromasts rest at the bottom of open grooves and consist of sensory, supporting, basal and mantle cells. Each sensory cell is equipped with sensory hairs consisting of a single kinocilium and several stereocilia. There are several types of sensory hair arrangement, and cells with a particular arrangement form patches within the neuromast. There are two types of afferent synapse. The most common afferent synapse has a presynaptic body and is typically associated with an extensive system of anastomosing tubules on the presynaptic side. When the tubules are absent, vesicles surround the presynaptic body. These synapses are often associated into synaptic fields, containing up to 35 synaptic sites. The second type of afferent synapse does not have a presynaptic body and is not associated with the tubular system. The afferent synapses of the second type do not form synaptic fields and are uncommon. The efferent synapses are either associated with a postsynaptic sac or more commonly with a strongly osmiophilic postsynaptic membrane. The accessory cells are similar to those in the acoustico-lateralis organs of other aquatic vertebrates. A possibility of movement of the presynaptic bodies and of involvement of the tubular system in the turnover of the transmitter is discussed. A comparison of the hair tuft types in the neuromasts of Ch. monstrosa with those in the labyrinth of the goldfish and of the frog is attempted.     

Neuromast morphology and lateral line trunk canal ontogeny in two species of cichlids: an SEM study

A study of neuromast ontogeny and lateral line canal formation in Oreochromis aureus and Cichlasoma nigrofasciatum reveals the existence of two classes of neuromasts: those that arise just before hatching (presumptive canal neuromasts, dorsal superficial neuromasts, gap neuromasts, and caudal fin neuromasts) and pairs of neuromasts that arise on each lateral line scale lateral to each canal segment at the same time as canal formation. In the anterior trunk canal segment, each presumptive canal neuromast is accompanied by a dorsoventrally oriented superficial neuromast forming an orthogonal neuromast pair. It is suggested that each of these dorsoventrally oriented superficial neuromasts is homologous to the transverse superficial neuromast row described by Münz (Zoomorphology 93:73-86, '79) in other cichlids. It is further suggested that the longitudinal lines described by Münz (Zoomorphology 93:73-86, '79) are derived from the pair of superficial neuromasts that arise during canal formation. Distinct changes in neuromast topography are documented. Neuromast formation, scale formation, and lateral line canal formation are three distinct and sequential processes. The distribution of neuromasts is correlated with myomere configuration; there is always one presumptive canal neuromast on each myomere. A single scale forms beneath each presumptive canal neuromast. Canal segment formation is initiated with the enclosure of each presumptive canal neuromast by an epithelial bridge which later ossifies. The distinction of these three processes raises questions as to the causal relationships among them.     

Mechanosensory system of the lateral line in the subantarctic Patagonian blenny Eleginops maclovinus

This study describes the cephalic and trunk lateral line systems in Patagonian blenny Eleginops maclovinus juveniles, providing morphological details for pores, canals and neuromasts. Eleginops maclovinus juveniles possess a complete laterodorsal lateral line that extends from the upper apex of the gill opening along the trunk as far as the caudal fin. The lateral line was ramified through pores and canals. The following pores were recorded: four supraorbital pores, with two along the eye border and two on the snout; seven infraorbital pores, with three on the lacrimal bone and four being infraorbital; five postorbital pores, with three along the preopercular border (upper preoperculum branch) and two on the bone curvature (inferior preoperculum branch); and four mandibular pores aligned along the jaw. Furthermore, five narrow-simple and interconnected canals were found (i.e. preopercular, mandibular, supraorbital and infraorbital canals). Histologically, the dorsal lateral line presented thin neuromasts (350 μm) with short hair cells. By contrast, the cranial region presented long, thick neuromasts. Infraorbital and mandibular neuromasts had a major axis length of 260 μm and respective average diameters of 200 and 185 μm. Sensory system variations would be due to a greater concentration of neuromasts in the cranial region, allowing for a greater perception of changes in water pressure. Scarce morphological information is available for the lateral sensory system in Eleginopsidae, particularly compared to Channichthyidae, Bovichthydae, Artedidraconidae and Bathydraconidae. Therefore, the presented results form a fundamental foundation of knowledge for the lateral-line system in juvenile E. maclovinus and provide a basis for future related research in this taxon as well as within the Notothenioidei suborder.     

The lateral line system and its innervation in Champsodon snyderi (Champsodontidae): distribution of approximately 1000 neuromasts

The lateral line system and its innervation were studied in Champsodon snyderi (Champsodontidae). The lateral line system was composed of 43 canal and 935 superficial neuromasts, the former being arranged in 8 lines (7 on the head, 1 on the body). Tubular lateral line scales, clearly differing from the heart-shaped spinoid scales on the remaining parts of the head and body, were arranged dorsolaterally along the body, enclosing 19 canal neuromasts. Superficial neuromasts on the body were vertically aligned along 3 distinct body sections (comprising 19 dorsal, 26 lateral, and 20 ventrally positioned vertical lines), the lateral section being separated from the adjacent sections by single dorsolateral and ventrolateral horizontal lines of superficial neuromasts, respectively. All the canal neuromasts in the lateral line scales were included in the dorsal vertical lines. Accessory lateral rami, innervating most of the neuromasts on the body, were derived from the lateral ramus in a one-to-one relationship with the vertebrae.     

Morphology and development of the multiple lateral line canals on the trunk in two species of Hexagrammos (Scorpaeniformes,Hexagrammidae)

The morphology and development of the multiple lateral line canals (canals 1–5 in dorsal to ventral sequence) on the trunk of two representative hexagrammids, Hexagrammos decagrammus and H. stelleri, were studied using histological and cleared and stained material. The morphology of the lateral line scales of which the lateral line canals are composed and the distribution of canal neuromasts within them were described quantitatively. We hypothesized that 1) one neuromast is contained in each lateral line scale and all five canals contain neuromasts, 2) all five canals develop similarly, and 3) the multiple trunk canals are an adaptation for the alteration of lateral line function. Lateral line scale morphology was found to be similar among the five canals in Hexagrammos decagrammus and H. stelleri. However, canal 3 is significantly wider than the other four canals. It is the only one of the five canals connected to the canals on the head, and more significantly, it is the only one of the five canals that contains neuromasts. The lateral line scales that comprise all five lateral line canals show the same pattern of development whether or not they contain neuromasts. The five canals develop asynchronously, and each of the canals develops either rostro-caudally or caudo-rostrally. Canal 3 is the homologue of a single trunk canal in other teleosts; canals 1, 2, 4, and 5 are apomorphic features of the two species of Hexagrammos. Canals 1, 2, 4, and 5 cannot be functional components of the lateral line system because they do not contain neuromasts and thus cannot be adaptations for the alteration of lateral line function. The occurrence of lateral line canals lacking neuromasts demands a direct assessment of neuromast distributions in the lateral line canals among fishes. Finally, our data suggest that the putative role of neuromasts in the morphogenesis of lateral line canals and the nature of neuromast-bone relationships need to be critically reevaluated. J. Morphol. 233:195–214, 1997. © 1997 Wiley-Liss, Inc.     

The development of neuromasts in Cirrhina mrigala Ham. Buch. (Cyprinidae) and Ophicephalus (Channa) punctatus Bloch (Channidae)

The development of neuromasts was studied in two species of teleosts, Cirrhina mrigala Ham. Buch. and Ophicephalus punctatus Bloch, and the findings are presented and discussed. It has been discovered, in the course of this investigation, that a neuromast arises by a process of invagination — a fact hitherto not reported. The occurrence of the dorsal lateral line and the accessory lateral line of the trunk, in addition to the main lateral line, has also been reported for the first time for teleosts, although known for other bony fishes.     

Organization of the superficial neuromast system in goldfish, Carassius auratus

Distribution, morphology, and orientation of superficial neuromasts and polarization of the hair cells within superficial neuromasts of the goldfish (Carassius auratus) were examined using fluorescence labeling and scanning electron microscopy. On each body side, goldfish have 1,800-2,000 superficial neuromasts distributed across the head, trunk and tail fin. Each superficial neuromast had about 14-32 hair cells that were arranged in the sensory epithelium with the axis of best sensitivity aligned perpendicular to the long axis of the neuromast. Hair cell polarization was rostro-caudal in most superficial neuromasts on trunk scales (with the exception of those on the lateral line scales), or on the tail fin. On lateral line scales, the most frequent hair cell polarization was dorso-ventral in 45% and rostro-caudal in 20% of the superficial neuromasts. On individual trunk scales, superficial neuromasts were organized in rows which in most scales showed similar orientations with angle deviations smaller than 45 degrees . In about 16% of all trunk scales, groups of superficial neuromasts in the dorsal and ventral half of the scale were oriented orthogonal to each other. On the head, most superficial neuromasts were arranged in rows or groups of similar orientation with angle deviations smaller than 45 degrees . Neighboring groups of superficial neuromasts could differ with respect to their orientation. The most frequent hair cell polarization was dorso-ventral in front of the eyes and on the ventral mandible and rostro-caudal below the eye and on the operculum.     

Development of the lateral line system in the sea bass

Using light and electron microscopy, a study of the development of the lateral line system of the sea bass Dicentrarchus labrax , from embryo to adult, revealed that the first free neuromasts appeared on the head shortly before hatching and multiplied during the larval stage. They were aligned on the head and trunk in a pattern which corresponded to the location of future canals. The transition to the juvenile stage marked the start of important anatomical changes during which head and trunk canals were formed successively. Neuromasts, with a cupula and consisting of standard sensory cells and supporting cells, were characterized by bidirectional polarity. The exact location of the first neuromast formed in the embryo was identified and its differentiation monitored from primordium to eruption. This neuromast was distinguishable from the others by its radial polarity. Correlations were made between the development of the lateral line system and the behaviour of the sea bass.