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.     

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.     

The fine structure of the lateral-line organs of larval Ichthyophis (Amphibia: Gymnophiona)

Light and electron microscopic observations of the lateral-line organs of larval Ichthyophis kohtaoensis confirmed earlier reports of the occurrence of two different types of lateral-line organs. One type, the ampullary organ, possesses 15–26 egg-shaped sensory cells. Each sensory cell extends a single kinocilium surrounded by a few microvilli into the ampullary lumen. This is in contrast to the ampullary organs of urodele amphibians that contain only microvilli. The second type of organ, the ordinary neuromast, has 15–24 pear-shaped sensory cells arranged in two to three rows. Each sensory cell shows a kinocilium that is asymmetrically placed with respect to both a basal plate and approximately 60 stereovilli. The sensory cells of ampullary organs are always separated by supporting cells; those of neuromasts are occasionally in contact with one another. Numerous (neuromasts) or few (ampullary organs) mantle cells separate the organs from the epidermal cells. Only afferent synapses are found in the ampullary organs whereas vesicle-filled fibers together with afferent nerve terminals are found in neuromasts. Both organs contain similarly sized presynaptic spheres adjacent to the afferent fibers. It is suggested that the neuromasts have a mechanoreceptive function, whereas the ampullary organs have an electroreceptive one.     

The development of lateral line placodes: Taking a broader view

The lateral line system of anamniote vertebrates enables the detection of local water movement and weak bioelectric fields. Ancestrally, it comprises neuromasts – small sense organs containing mechanosensory hair cells – distributed in characteristic lines over the head and trunk, flanked on the head by fields of electroreceptive ampullary organs, innervated by afferent neurons projecting respectively to the medial and dorsal octavolateral nuclei in the hindbrain. Given the independent loss of the electrosensory system in multiple lineages, the development and evolution of the mechanosensory and electrosensory components of the lateral line must be dissociable. Nevertheless, the entire system arises from a series of cranial lateral line placodes, which exhibit two modes of sensory organ formation: elongation to form sensory ridges that fragment (with neuromasts differentiating in the center of the ridge, and ampullary organs on the flanks), or migration as collectives of cells, depositing sense organs in their wake. Intensive study of the migrating posterior lateral line placode in zebrafish has yielded a wealth of information concerning the molecular control of migration and neuromast formation in this migrating placode, in this cypriniform teleost species. However, our mechanistic understanding of neuromast and ampullary organ formation by elongating lateral line placodes, and even of other zebrafish lateral line placodes, is sparse or non-existent. Here, we attempt to highlight the diversity of lateral line development and the limits of the current research focus on the zebrafish posterior lateral line placode. We hope this will stimulate a broader approach to this fascinating sensory system.     

Directional cell migration establishes the axes of planar polarity in the posterior lateral-line organ of the zebrafish

The proper orientation of mechanosensory hair cells along the lateral-line organ of a fish or amphibian is essential for the animal's ability to sense directional water movements. Within the sensory epithelium, hair cells are polarized in a stereotyped manner, but the mechanisms that control their alignment relative to the body axes are unknown. We have found, however, that neuromasts can be oriented either parallel or perpendicular to the anteroposterior body axis. By characterizing the strauss mutant zebrafish line and by tracking labeled cells, we have demonstrated that neuromasts of these two orientations originate from, respectively, the first and second primordia. Furthermore, altering the migratory pathway of a primordium reorients a neuromast's axis of planar polarity. We propose that the global orientation of hair cells relative to the body axes is established through an interaction between directional movement by primordial cells and the timing of neuromast maturation.     

西伯利亚鲟仔鱼侧线系统的发育

鲟鱼属软骨硬鳞鱼,在电感受器的进化中占据着极为重要的地位。该文以光镜和扫描电镜手段研究了西伯利亚鲟侧线系统早期发育,包括侧线基板发育及感觉嵴的形成、侧线感受器的发育和侧线管道的形成。1日龄,听囊前后外胚层增厚区域出现6对侧线基板;除后侧线基板细胞向躯干侧面迁移外,其他侧线基板均形成感觉嵴结构;每一侧线基板中均有神经丘原基形成。7日龄,壶腹器官在吻部腹面两侧出现,壶腹器官的发育比神经丘晚一周左右。9日龄,神经丘下的表皮略有凹陷,侧线管道开始形成。29日龄,在吻部腹面两侧可见少数个别的壶腹器官表皮细胞覆盖壶腹器官中央区域留下3～4个小的开口;壶腹管内可见大量的微绒毛存在,在其他鲟形目鱼类、软骨鱼类中也存在类似的结构。57日龄,躯干侧线管道已完全埋于侧骨板中;壶腹器官主要分布在吻部腹面,3～4个聚集在一起,呈"梅花状",分布紧密,并且该部分皮肤表面凹陷,形成花朵状凹穴;侧线系统发育完善。     

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.     

Evolution of posterior lateral line development in fish and amphibians

The lateral line is a sensory system present in fish and amphibians. It is composed of discrete sense organs, the neuromasts, arranged on the head and body in species-specific patterns. The neuromasts are deposited by migrating primordia that originate from pre- and postotic placodes and follow defined pathways on the head and body. Here we examine the formation of the posterior lateral line (PLL), which extends rostrocaudally on the trunk and tail. In amphibians, the PLL neuromasts are deposited as a single wave from the head to the tip of the tail. In the zebrafish, however, the first wave of neuromast deposition forms but a rudimentary PLL, and several additional waves are needed to form the adult pattern. We show that the amphibian mode is also present in the sturgeon and therefore probably represents the primitive mode, whereas the zebrafish mode is highly conserved in several teleost species. A third mode is found in a subgroup of teleosts, the protacanthopterygians, and may represent a synapomorphy of this group. Altogether, the mode of formation of the embryonic PLL appears to have undergone remarkably few changes during the long history of anamniote evolution, even though large differences can be observed in the lateral line morphology of adult fishes.     

Early breeding protects anuran eggs from Saprolegnia infection

Here, we studied the ecological significance of Saprolegnia infections (‘saprolegniasis’) on the survival and development of two populations of the endemic Patagonian anuran Pleurodema thaul (Anura, Leiuperidae). We found that four different Saprolegnia species infected eggs and embryos of P. thaul, indicating that the infection by these ‘zoosporic fungi’ was different in each anuran population and among different cohorts. Late anuran cohorts generally showed a higher incidence of infection than early cohorts, but we observed no clear overall pattern between populations. In addition, in laboratory experiments, we determined that some of the Saprolegnia species induce early hatching, and that hatching timing was variable between populations. In summary, we found that early breeding (by underlying priority effects) could improve the survival of the earliest cohorts of P. thaul by allowing them to survive the stress imposed by epidemic events of Saprolegnia.     

Dermal morphogenesis controls lateral line patterning during postembryonic development of teleost fish

The lateral line system displays highly divergent patterns in adult teleost fish. The mechanisms underlying this variability are poorly understood. Here, we demonstrate that the lateral line mechanoreceptor, the neuromast, gives rise to a series of accessory neuromasts by a serial budding process during postembryonic development in zebrafish. We also show that accessory neuromast formation is highly correlated to the development of underlying dermal structures such as bones and scales. Abnormalities in opercular bone morphogenesis, in endothelin 1-knockdown embryos, are accompanied by stereotypic errors in neuromast budding and positioning, further demonstrating the tight correlation between the patterning of neuromasts and of the underlying dermal bones. In medaka, where scales form between peridermis and opercular bones, the lateral line displays a scale-specific pattern which is never observed in zebrafish. These results strongly suggest a control of postembryonic neuromast patterns by underlying dermal structures. This dermal control may explain some aspects of the evolution of lateral line patterns.     

The influence of viscous hydrodynamics on the fish lateral-line system

Fish exhibit many behaviors that involve sensing water flows with their lateral-line system. In many situations, viscosity affects how the flow interacts with the body of the fish and the neuromasts of the lateral line. Here we discuss how viscosity influences the stimulus to the fish lateral-line system. The movement of a fish's body creates flows that can interfere with the detection of external signals, but these flows can also serve as a source of information about nearby obstacles and the fish's own hydrodynamic performance. The viscous boundary layer on the surface of the skin alters external signals by attenuating the low-frequency components of stimuli. The stimulus to each neuromast depends on the interaction of the fluid surrounding the neuromast and the structural properties of that neuromast, including the number of mechanosensory hair cells it contains. A consideration of the influences of viscosity on flow, at both the whole-body and receptor levels, offers the promise of a more comprehensive understanding of the signals involved in behaviors mediated by the lateral-line system.     

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.     

Comparative Study of the Lateral-line System of the Three-spined Stickleback (Gasterosteus aculeatus) and the Nine-spined Stickleback (Pungitius pungitius)

Abstract The morphology of the lateral-line system of the nine-spined stickleback (Pungitius pungitius) and the three-spined stickleback (Gasterosteus aculeatus) has been studied. In the nine-spined stickleback, a preopercular, infraorbital, supraorbital, postotic and peduncular canal can be identified on both sides of the body. Replacement lines are found as a continuation of the preopercular and infraorbital canal. In addition, lines of free neuromasts are found on the mandible and trunk. An accessory line is present above and below the peduncular canal. The presence of both canals and accessory lines on the peduncle suggests that the peduncle in this species has important sensory functions. No canals are found in the three-spined stickleback. Instead, replacement lines corresponding to the canals can be identified on the head. Accordingly, the lateral-line system of the three-spined and the nine-spined stickleback has a different structure. The lateral-line system of both species shows signs of specialization but the three-spined stickleback has a more specialized lateral-line system than the nine-spined stickleback.     

Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates

The lateral line system of fishes and amphibians comprises two ancient sensory systems: mechanoreception and electroreception. Electroreception is found in all major vertebrate groups (i.e. jawless fishes, cartilaginous fishes, and bony fishes); however, it was lost in several groups including anuran amphibians (frogs) and amniotes (reptiles, birds, and mammals), as well as in the lineage leading to the neopterygian clade of bony fishes (bowfins, gars, and teleosts). Electroreception is mediated by modified “hair cells,” which are collected in ampullary organs that flank lines of mechanosensory hair cell containing neuromasts. In the axolotl (a urodele amphibian), grafting and ablation studies have shown a lateral line placode origin for both mechanosensory neuromasts and electrosensory ampullary organs (and the neurons that innervate them). However, little is known at the molecular level about the development of the amphibian lateral line system in general and electrosensory ampullary organs in particular. Previously, we identified Eya4 as a marker for lateral line (and otic) placodes, neuromasts, and ampullary organs in a shark (a cartilaginous fish) and a paddlefish (a basal ray‐finned fish). Here, we show that Eya4 is similarly expressed during otic and lateral line placode development in the axolotl (a representative of the lobe‐finned fish clade). Furthermore, Eya4 expression is specifically restricted to hair cells in both neuromasts and ampullary organs, as identified by coexpression with the calcium‐buffering protein Parvalbumin3. As well as identifying new molecular markers for amphibian mechanosensory and electrosensory hair cells, these data demonstrate that Eya4 is a conserved marker for lateral line placodes and their derivatives in all jawed vertebrates.     

Cell migration in the postembryonic development of the fish lateral line

We examine at the cellular level the postembryonic development of the posterior lateral line in the zebrafish. We show that the first wave of secondary neuromasts is laid down by a migrating primordium, primII. This primordium originates from a cephalic region much like the primordium that formed the primary line during embryogenesis. PrimII contributes to both the lateral and the dorsal branches of the posterior lateral line. Once they are deposited by the primordium, the differentiating neuromasts induce the specialisation of overlying epidermal cells into a pore-forming annulus, and the entire structure begins to migrate ventrally across the epithelium. Thus the final two-dimensional pattern depends on the combination of two orthogonal processes: anteroposterior waves of neuromast formation and dorsoventral migration of individual neuromasts. Finally, we examine how general these migratory processes can be by describing two fish species with very different adult patterns, Astyanax fasciatus (Mexican blind cavefish) and Oryzias latipes (medaka). We show that their primary patterns are nearly identical to that observed in zebrafish embryos, and that their postembryonic growth relies on the same combination of migratory processes that we documented in the case of the zebrafish.     

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.     

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.     

Lateral-Line System of Siren intermedia Le Conte (Amphibia: Sirenidae), During Aquatic Activity and Aestivation

Siren intermedia is peculiar in that the lateral-line system is retained throughout life, even though the animal is forced into terrestrial situations during aestivation. The lateral-line system is constructed of neuromasts arranged in pit fields instead of pit lines as in most amphibians. The neuromasts are unusual, because the sense cells are arranged in a single row through the long axis of the organ and a few of the sustentacular cells contain “orange granules.” During aestivation, the neuromasts are either shielded by a secreted cocoon, or occluded by proliferated skin epithelium. Those organs occluded by epithelium undergo dedifferentiation which continues through postaestivation. Loss of the lateral-line system by amphibians was apparently late in amphibian evolution. Gradual loss of the system suggests that retention and/or protection of the lateral-line system proved maladaptive and physiologically too expensive. Thus the system was abandoned by most amphibian taxa at metamorphosis.     

The pattern of lateral-line afferents in urodeles

Summary The organization of posterior and anterior afferents of the lateralline system was studied in several species of urodeles by means of transganglionic transport of horseradish peroxidase. The afferents of each lateral-line nerve form distinct fascicles in the medullary alar plate. Each of the two branches of the anterior lateral-line nerve is organized in two long and one short fascicles. The posterior lateral-line afferents form only two long fascicles. Each ordinary neuromast is supplied by only two afferents, which run in the two ventral medullary fiber bundles. It is suggested that afferents to hair cells displaying one type of polarity form together one bundle, but those contacting hair cells polarized in the opposite way form the second ventral bundle of one lateral-line branch. Thus, the lateral-line afferents may be organized in a directotopic fashion.The short dorsal fascicle formed only by the anterior lateral-line afferents receives fibers exclusively from small pit organs. Each pit organ is supplied by only one afferent. Anatomically, these pit organs resemble in many respects the electroreceptive ampullary organs of certain fish.Neurons labeled retrogradely via the anterior lateral-line nerve afferents have been attributed to the nervus trigeminus or facialis. In addition to the posterior lateral-line afferents, only few centrifugally projecting neurons were labeled. These neurons are discussed as efferents to the posterior lateral-line neuromasts.