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.     

The lateral line system in larvalIchthyophis (Amphibia: Gymnophiona)

Summary The lateral line systems of larval caecilians of the genusIchthyophis possess two types of elements, free neuromasts and ampullary organs. Free mechanoreceptive neuromasts are typical of those found in other vertebrates, and are arranged in series roughly homologous to neuromast groups in many other fishes and amphibians. In contrast to other amphibians,Ichthyophis larvae possess only one paired, dorsal body series of neuromasts. Regional specialization of neuromasts is evident inIchthyophis. Premaxillary and anterior head neuromasts are the largest in size and total cell number. Overall, size and total cell numbers are correlated with depth of epidermis. Neuromasts on the anterior sides of the head occur in slight grooves and have apical tips situated farther below the level of the epidermis and with greater apical indentation. These features probably provide increased protection against abrasion. Apparently abnormal neuromasts are frequently found among the neuromast series. Such neuromasts contain fewer cells that lack normal apical extension, producing a sunken effect similar to that of the ampullary organ elements. The ampullary organs ofIchthyophis are morphologically similar to those found in various freshwater fishes and known to function as electroreceptors. These organs are not observed in the lateral line systems of members of other amphibian orders (Urodela and Anura), and we suggest that they function as electroreceptors. The sunken neuromasts of theIchthyophis lateral line system may parallel the possible evolutionary development of pit organs from normal neuromasts.     

The pit organs of elasmobranchs: a review

Elasmobranchs have hundreds of tiny sensory organs, called pit organs, scattered over the skin surface. The pit organs were noted in many early studies of the lateral line, but their exact nature has long remained a mystery. Although pit organs were known to be innervated by the lateral line nerves, and light micrographs suggested that they were free neuromasts, speculation that they may be external taste buds or chemoreceptors has persisted until recently. Electron micrographs have now revealed that the pit organs are indeed free neuromasts. Their functional and behavioural role(s), however, are yet to be investigated.     

Morphology and Growth of Lateral Line Organs of the Rainbow Trout (Oncorhynchus mykiss)

Abstract The morphology and growth of selected lateral line organs of the rainbow trout (Oncorhynchus mykiss) are described. Canal neuromasts of the infraorbital and operculo–mandibular canal of three different–sized trout have been examined by light microscopy. The number of neuromasts and pores, as well as their distribution, is constant in all sizes of fish. However, the area and estimated number of hair cells (HC) of the examined neuromasts increase with size and with a correlation coefficient (r²) of 0.90 and 0.87, respectively. It was found that area and estimated hair cell number of neuromasts increase 6-fold in fish from 10 to 30 cm total length (TL). Based on calculation of the hair cell number in small and large fish, a net addition of 1 and 6 HC per day is suggested for IO and OM neuromasts, respectively.     

中国大鲵侧线器官的研究

本文以光镜和扫描是镜手段研究了中国大鲵幼体，亚成体及成体头部及躯干部表皮中的侧线器官，即电接受壶腹器官，机械接受的表面神经丘和陷器官的分布，形态和发展变化。壶腹器管仅存于幼体头部，变态结束后消失，后两种终生存在，但前者按一定路线和方向排列，后者仅存于头部，陷在表皮中，文章探讨了壶腹器官的原始性，其消失与生活习性以及由水登陆进化的关系；对三种器官的形态及其它有尾类的侧线器官进行了比较。     

Development of sensory organs in larvae of African catfish Clarias gariepinus

African catfish Clarias gariepinus hatched with morphologically immature features; however, sensory organs developed rapidly with fish growth. Although the eyes of newly hatched larvae were immature without pigment, in 2 day‐old larvae, the retina of the eyes had already developed except for the rod cells. No free neuromasts were observed in newly hatched larvae. In 1 day‐old larvae, however, free neuromasts were observed on the head and trunk. Free neuromasts increased with larval growth. Newly hatched larvae had simple round‐shaped otic vesicles; however, all sensory epithelia of the inner ear were observed until the larvae were 3 days old. Two day‐old larvae swam horizontally, had sharp teeth, commenced ingesting rotifers and also artificial feed (small‐size pellets) under both light and dark conditions; by then the larvae already had many taste buds. Three day‐old larvae showed negative phototaxis and cannibalism by eating their conspecifics. Most of the free neuromasts observed in this study had the peculiar feature of many microvilli around the sensory cells on the apical surface. Detected free neuromasts as ordinary type lateral‐line organs were not observed in previous reports in teleosts. In 10 day‐old larvae, there were two lines of free neuromasts on the flank and lower edge of the trunk; presumptive canal neuromasts were oval shaped and had begun to sink under the skin. The direction of maximum sensitivity of the neuromasts was parallel with the longitudinal axis of their elliptical apical surface.     

Observations on the lateral-line sense organs of the Salamander Neurergus crocatus crocatus Cope (Amphibia: Urodela)

The lateral-line system of the subadult and adult Neurergus crocatus crocatus Cope is retained throughout the life. It is constructed of pear-shaped sense organs or neuromasts which in the subadults are confined entirely to the epidermis with their apices opening distally to the exterior at the general level of the epidermal surface whereas in the adults they are embedded proximally more than halfway in the dermis with their distal apices opening into shallow grooves slightly below the regular epidermal surface. Dimensional differences are also observed between these organs in both stages. The neuromasts are constructed of 4 distinct cell types: sense cells, basal cells, sustentacular cells and mantle cells. These cells differ morphologically, structurally, topographically and functionally. The sense cells are clup-shaped, sensory, central in position and couched among the extremely elongated supporting basal and sustentacular cells, all of which are covered laterally by the extremely slender protective mantle cells. In both the mature and larvae, differences are observed among these cells in their size, number, location and arrangement. The sense organs are richly-supplied and well-nourished with vascular and nervous supplies.     

Pattern formation in the lateral line of zebrafish.

The lateral line of fish and amphibians is a sensory system that comprises a number of individual sense organs, the neuromasts, arranged in a defined pattern on the surface of the body. A conspicuous part of the system is a line of organs that extends along each flank (and which gave the system its name). At the end of zebrafish embryogenesis, this line comprises 7-8 neuromasts regularly spaced between the ear and the tip of the tail. The neuromasts are deposited by a migrating primordium that originates from the otic region. Here, we follow the development of this pattern and show that heterogeneities within the migrating primordium prefigure neuromast formation.     

The evolution of the amphibian lateral line system and its bearing on amphibian phylogeny

In modern amphibians that are aquatic the lateral line system is organized, by order, as follows: caecilians have electroreceptive ampullary organs and single rows of mechanoreceptive neuromast organs; generalized anurans have single rows of neuromasts that divide in a transverse plane to form secondary neuromasts or stitches, they do not have ampullary organs; generalized urodeles have ampullary organs, transverse stitches, and double or triple rows of neuromasts. Fossil evidence indicates that early amphibians had both ampullary organs and single rows of neuromasts embedded in bone. With time, receptors became epidermal in all three orders. Modern caecilians have retained the primitive receptor arrangement. I propose that the common ancestor of anurans and urodeles had transverse stitches, and that this character allies these two groups. Subsequent to the anuranurodele split, anurans lost their ampullary organs, perhaps concomitant with developing specializations for herbivory. Urodeles developed orthogonal neuromast couplets und triplets. In modern anurans und urodeles, transverse stitches are correlated with pond dwelling, while ampullary organs are correlated with carnivory, suggesting that the anuran-urodele ancestor(s) was a (were) pond-dwelling carnivore(s).     

版纳鱼螈侧线系统的结构

版纳鱼螈(Ichthyophis bannanica)是我国无足目的仅有代表,应用光镜和扫描电镜对版纳鱼螈的侧线系统进行形态学和组织学观察的研究表明:版纳鱼螈幼体表皮中的侧线器官有接受机械刺激的神经丘和电接受壶腹器官两种,神经丘包括表面神经丘和陷神经丘。侧线分布主要包括:头部的鼻侧线、眶上线、眶下线、眶后线、口侧线、下颌线、咽侧线、鳃孔上线和身体上的背侧线。侧线器官的分布密度、大小和凹陷深度明显与周围表皮的厚度和不同部位有关。幼体的侧线器官退化与鳃孔的退化同步,亚成体以后不保留侧线系统。版纳鱼螈的侧线分布和器官结构与其它无足类的大致相似,仅在眶上线和眶下线的器官分布上存在微小的差别     

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.     

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.     

Sensory trait variation contributes to biased dispersal of threespine stickleback in flowing water

Gene flow is widely thought to homogenize spatially separate populations, eroding effects of divergent selection. The resulting theory of ‘migration–selection balance’ is predicated on a common assumption that all genotypes are equally prone to dispersal. If instead certain genotypes are disproportionately likely to disperse, then migration can actually promote population divergence. For example, previous work has shown that threespine stickleback (Gasterosteus aculeatus) differ in their propensity to move up‐ or downstream (‘rheotactic response’), which may facilitate genetic divergence between adjoining lake and stream populations of stickleback. Here, we demonstrate that intraspecific variation in a sensory system (superficial neuromast lines) contributes to this variation in swimming behaviour in stickleback. First, we show that intact neuromasts are necessary for a typical rheotactic response. Next, we showed that there is heritable variation in the number of neuromasts and that stickleback with more neuromasts are more likely to move downstream. Variation in pectoral fin shape contributes to additional variation in rheotactic response. These results illustrate how within‐population quantitative variation in sensory and locomotor traits can influence dispersal behaviour, thereby biasing dispersal between habitats and favouring population divergence.     

Ultrastructure of the skin mechanoreceptors of the Chinese giant salamander, Andrias davidianus

The ultrastructure of two kinds of mechanoreceptive organs, pit organs and neuromasts, in the skin of adult giant salamanders (Andrias davidianus) was studied by transmission electron microscopy. Neuromasts and pit organs differ in their types of synapses, the spatial distribution of kinocilia on sensory cells, and in the degree to which sensory cells are separated by processes of the supporting cells; the two organs probably serve complementary functions. The neuromasts in A. davidianus differ from those of other salamanders in the orientation of kinocilia, in the extent of intrusion of supporting cells into the sensory layer, in the degree of thickening of the synaptic membranes, in the distribution of synaptic spheres, and by the absence of a cupula.     

Post‐embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes

The relatively simple structural organization of the cranial lateral line system of bony fishes provides a valuable context in which to explore the ways in which variation in post‐embryonic development results in functionally distinct phenotypes, thus providing a link between development, evolution, and behavior. Vital fluorescent staining, histology, and scanning electron microscopy were used to describe the distribution, morphology, and ontogeny of the canal and superficial neuromasts on the head of two Lake Malawi cichlids with contrasting lateral line canal phenotypes (Tramitichromis sp. [narrow‐simple, well‐ossified canals with small pores] and Aulonocara stuartgranti [widened, more weakly ossified canals with large pores]). This work showed that: 1) the patterning (number, distribution) of canal neuromasts, and the process of canal morphogenesis typical of bony fishes was the same in the two species, 2) two sub‐populations of neuromasts (presumptive canal neuromasts and superficial neuromasts) are already distinguishable in small larvae and demonstrate distinctive ontogenetic trajectories in both species, 3) canal neuromasts differ with respect to ontogenetic trends in size and proportions between canals and between species, 4) the size, shape, configuration, physiological orientation, and overall rate of proliferation varies among the nine series of superficial neuromasts, which are found in both species, and 5) in Aulonocara, in particular, a consistent number of canal neuromasts accompanied by variability in the formation of canal pores during canal morphogenesis demonstrates independence of early and late phases of lateral line development. This work provides a new perspective on the contributions of post‐embryonic phases of lateral line development and to the generation of distinct phenotypes in the lateral line system of bony fishes. J. Morphol. 277:1273–1291, 2016. © 2016 Wiley Periodicals, Inc.     

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 the lateral line canal system through a bone remodeling process in zebrafish

The lateral line system of teleost fish is composed of mechanosensory receptors (neuromasts), comprising superficial receptors and others embedded in canals running under the skin. Canal diameter and size of the canal neuromasts are correlated with increasing body size, thus providing a very simple system to investigate mechanisms underlying the coordination between organ growth and body size. Here, we examine the development of the trunk lateral line canal system in zebrafish. We demonstrated that trunk canals originate from scales through a bone remodeling process, which we suggest is essential for the normal growth of canals and canal neuromasts. Moreover, we found that lateral line cells are required for the formation of canals, suggesting the existence of mutual interactions between the sensory system and surrounding connective tissues.     

The lateral line of zebrafish: a model system for the analysis of morphogenesis and neural development in vertebrates

The lateral line of the zebrafish has many of the advantages that made the sensory organs of Drosophila a very productive model system: 1) it comprises a set of discrete sense organs (neuromasts) arranged in a defined, species-specific pattern, such that each organ can be individually recognized; 2) the neuromasts are superficial and easy to visualize, and the innervating neurons are easy to label; 3) the sensory projection is simple yet reproducibly organized. Here we describe some of the tools that can be used to investigate the development of this system, and we illustrate their usefulness with specific examples. We conclude that the lateral line is uniquely suited among vertebrate sensory systems for a molecular, cellular and genetic analysis of pattern formation and of neural development.     

Morphogenesis of free neuromasts in the larvae of brown-marbled grouper Epinephelus fuscoguttatus

Newly hatched larvae had one pair of free neuromasts behind the eyes. As the larvae grew, free neuromasts increased in number. The apical surface of sensory epithelium widened and subsequently elongated. The number of sensory hair cells increased and the directions of maximum sensitivity became both anteroposterior and dorsoventral on the trunk. Before notochord flexion, only the anteroposterior type was observed. After notochord flexion, two types of neuromasts were observed on the trunk. On the head, the orientation of free neuromasts formed a tangential line to concentric circles around the eyes and nostrils. Free neuromasts on the head could therefore receive stimuli from various angles from predators or zooplanktons. This suggests that these free neuromasts play a role in compensating for a dead angle of vision, and an important role in detecting zooplankton under scotopic vision. Canal organs were observed on the head and operculum in 40-d-old animals.     

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.