Innervation of the lateral line system in Rhyacichthys aspro: the origin of superficial neuromast rows in gobioids (Perciformes: Rhyacichthyidae)

The lateral line system and its innervation were examined in the most primitive gobioid taxon, Rhyacichthys aspro (Rhyacichthyidae). The infraorbital canal was present, whereas superficial neuromast rows a and c, typically present on the cheek of gobioids, were absent. Because the infraorbital canal (absent in other gobioids) and the two rows were commonly innervated by the buccal ramus, the latter were categorized as replaced rows from canal neuromasts. On an innervation basis, rows b and d on the cheek were considered to comprise superficial neuromasts only in all gobioids. The trunk lateral line system comprised canal and superficial neuromasts, the former being included in the lateral line scales (each bearing 1–7 neuromasts arranged longitudinally along the direction of a groove). Absence of bony roofs in the lateral line system was proposed as a synapomorphy of Gobioidei, and a progressive neotenic shift in the lateral line system of the suborder discussed.     

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.     

The innervation and adaptive significance of extensively distributed neuromasts in <Emphasis Type="Italic">Glossogobius olivaceus</Emphasis> (Perciformes: Gobiidae)

Components of the lateral line system and their innervation were examined in Glossogobius olivaceus (Gobiidae), with almost all of the trunk scales bearing a row of superficial neuromasts, the latter comprising some 2,900 of the total (ca. 4,800) neuromasts on the body. The relationship between orientation and innervation of the superficial neuromasts on the head showed the buccal and mandibular rami to be clearly separated. On the trunk, the lateral ramus detached a number of branches, typically comprising dorsal, lateral and ventral ramules, to innervate neuromasts. Extensively distributed neuromasts were considered as an adaptation to a nocturnal habit, compensating for reduced vision.     

The cephalic lateral line system and its innervation in <Emphasis Type="Italic">Pardachirus pavoninus</Emphasis> (Soleidae: Pleuronectiformes): comparisons between the ocular and blind sides

The cephalic lateral line system and its innervation were examined and compared between the ocular and blind sides in Pardachirus pavoninus (Soleidae). On the ocular side, the otic and preopercular canals were partly (posteriorly and dorsally, respectively) formed by canalized scales (one and five, respectively), each containing a canal neuromast (i.e., “lateral line scales”) and innervated by the anterior lateral line nerve (otic and mandibular rami, respectively). The canal neuromasts of the five scales were recognized as homologous with superficial neuromasts in other taxa based on innervation. The scales, each with a canal perpendicular to the long axis of the scale, bridged the wide gap between the otic region of the cranium and preopercle. The superficial ophthalmic ramus was bifurcated on both sides, the dorsal ramule emerging from the cranium via a frontal foramen. The buccal ramus on the blind side was intensively ramified in the area made available by migration of the eye to the ocular side. The numbers of canal and superficial neuromasts differed greatly between the sides, being 19 and 173 on the ocular side, and 1 and 465 on the blind side, respectively. Sensory strips of superficial neuromasts on the blind side had clear long and short axes. Numerous dermal papillae occurred on the blind side, forming complex channels, according to directions of the long axes.     

Peripheral nervous system of the ocean sunfish Mola mola (Tetraodontiformes: Molidae)

Dissection of peripheral nerves in the ocean sunfish Mola mola showed the lateral line system to comprise 6 cephalic and 1 trunk lateral lines, all neuromasts being superficial. The trunk line was restricted to the anterior half of the body, the number of neuromasts (27) being fewer than those previously recorded in other tetraodontiforms. The lateral ramus of the posterior lateral line nerve did not form a “serial collector nerve” along the body. The number of foramina in the neurocranium, serving as passages for the cranial nerves, was fewer than in primitive tetraodontiforms, the reduction being related to modifications in the posterior cranium. Some muscle homologies were reinterpreted based on nerve innervation patterns. The cutaneous branch innervation pattern in the claval fin rays was clearly identical with that in the dorsal and anal fin rays, but differed significantly from that in the caudal fin rays, providing strong support for the hypothesis that the clavus comprises highly modified components of the dorsal and anal fins.     

The lateral line system and its innervation in the boxfish Ostracion immaculatus (Tetraodontiformes: Ostraciidae): description and comparisons with other tetraodontiform and perciform conditions

The lateral line system and its innervation were examined in the ostraciid Ostracion immaculatus (Tetraodontiformes), and compared with those in the triacanthodid Triacanthodes anomalus (Tetraodontiformes) and the acropomatid Malakichthys wakiyae (Perciformes). The carapace of O. immaculatus was composed of 6 cephalic and 2 trunk lateral lines, all neuromasts being categorized as “superficial.” Triacanthodes anomalus was identical with O. immaculatus in the absence of the mandibular line and its innervating ramus, whereas in M. wakiyae the line and ramus were present. All neuromasts were “superficial” in the former two, but “canal” in the latter. Judging from the essentially identical lateral line topography and innervation patterns in all three species, the superficial neuromasts in the two tetraodontiforms were considered to have resulted from replacement of canal neuromasts. The number of neuromasts in the cephalic lateral lines of O. immaculatus (106) and T. anomalus (91) were similar, being significantly higher than in M. wakiyae (30). However, the reverse was true for the trunk lateral lines, the two tetraodontiforms having fewer neuromasts (39 in O. immaculatus, 47 in T. anomalus) compared with M. wakiyae (59).     

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.     

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.     

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.     

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.     

Metamorphosis-related changes in the lateral line system of lampreys, <Emphasis Type="Italic">Petromyzon marinus</Emphasis>

Lamprey metamorphosis leads to considerable changes in morphology and behavior. We have recently reported that larval lampreys possess a functional lateral line system. Here we investigated metamorphic morphological changes in the lateral line system using light and electron microscopy. Functional modifications were studied by recording the trunk lateral line nerve activity of larvae and adults while stimulating neuromasts with approximately sinusoidal water motion. We found a general re-patterning of neuromasts on the head and trunk including an increase in numbers, redistribution within the pit lines, and shifts of the pit lines relative to external features. The trunk lateral line nerve response was qualitatively similar in adults and larvae. Both showed two neuronal populations responding to opposite directions of water flow. Magnitude of the response increased monotonically with stimulus amplitude. At low frequencies, the response lag relative to the stimulus maximum was approximately 220°, and the gain depended approximately linearly on frequency, confirming that superficial neuromasts are velocity detectors. Changes in phase lag with increasing stimulus frequency were steeper in larvae, suggesting slower afferent conductance. The response gain with frequency was smaller for adults, suggesting a narrower frequency discrimination range and decreased sensitivity. These changes may be adaptations for the active lifestyle of adult lampreys.     

A comparison of Lateral Line Morphology of Blue Cod and Torrentfish: Two Sandperches of the Family Pinguipedidae

Parapercis colias (blue cod) and Cheimarrichthys fosteri (torrentfish) are two members of the family Pinguipedidae. They reside in habitats with different background levels of hydrodynamic activity and differ in their feeding ecology. The peripheral morphology of the mechanosensory lateral line system was investigated in each species. The torrentfish is the only freshwater member of this otherwise exclusively marine family. It resides in turbulent fast flowing habitats and feeds nocturnally on stream drift. Torrentfish have many superficial neuromasts and a simple unbranched canal system. In comparison the blue cod resides in sub-tidal slow flowing habitats, is a diurnal predator and has relatively few superficial neuromasts and a well-developed branching canal system. For these two species the background level of hydrodynamic activity does not appear to be the dominant selection pressure on lateral line morphology, in the case of the torrentfish in particular it is more compelling to view lateral line morphology in the light of environmental pressures that have favoured the evolution of nocturnal feeding.     

Lateral line system and its innervation in Tetraodontiformes with outgroup comparisons: Descriptions and phylogenetic implications

The lateral line system and its innervation in ten tetraodontiform families and five outgroup taxa were examined. Although some homology issues remained unresolved, tetraodontiforms were characterized by having two types (at least) of superficial neuromasts (defined by the presence or absence of supporting structures) and accessory lateral lines and neuromasts (except Molidae in which “accessory” elements were absent). The preopercular line in Tetraodontiformes was not homologous with that of typical teleosts, because the line was innervated by the opercular ramule that was newly derived from the mandibular ramus, the condition being identical to that in Lophiidae. Within Tetraodontiformes, the number of neuromasts varied between 70 and 277 in the main lines and between 0 and 52 in accessory elements. Variations were also recognized in the presence or absence of the supraorbital commissure, mandibular line, otic line, postotic line, ventral trunk line, and some lateral line nerve rami, most notably the dorsal branch of the opercular ramule, being absent in Aracanidae, Ostraciidae, Tetraodontidae, Diodontidae, and Molidae. Morphological characteristics derived from the lateral line system and its innervation provided some support for a sister relationship of tetraodontiforms with lophiiforms. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Lateral line mediated rheotaxis in the Antarctic fish Pagothenia borchgrevinki

The sensory basis of rheotaxis was investigated in Pagothenia borchgrevinki utilising a laminar flow chamber. The threshold for P. borchgrevinki to exhibit an unconditioned rheotactic response lay between 1 and 2 cm s⁻¹. Disabling the entire lateral line or the superficial neuromast receptors increased the rheotactic threshold to greater than 5 cm s⁻¹. Pharmacological blocking of the lateral line canal system alone had no effect. This study provides a direct demonstration that the superficial lateral line system is involved in mediating rheotaxis. These results, coupled with previous work on Antarctic fishes, suggest a division of labour exists between the two submodalities of the lateral line system. Superficial neuromasts are more responsive to unmodulated flows (DC) and mediate behaviour such as rheotaxis, whereas canal neuromasts detect acceleration components of modulated flows (AC) and are more concerned with behaviour such as feeding. Accepted: 27 October 1998     

The sensory basis of rheotaxis in the blind Mexican cave fish, Astyanax fasciatus

The sensory basis of rheotaxis (orientation to currents) was investigated in the blind Mexican cave fish, Astyanax fasciatus. An unconditioned rheotactic response to uniform velocity flows was exhibited, with a threshold of less than 3 cm s⁻¹. Disabling the entire lateral line or the superficial neuromast receptor class increased the rheotactic threshold to greater than 9 cm s⁻¹. A pharmacological block of the lateral line canal system alone had no effect. These results demonstrate that the superficial lateral line system controls rheotaxis at low current velocities. The effect of pairing an odor stimulant with the water current dropped the rheotactic threshold to less than 0.4 cm s⁻¹. This study provides a clear behavioral role for the superficial neuromasts where none previously existed, and also establishes a link between the mechanosensory lateral line and olfactory systems in the olfactory search behavior of the cave fish. Accepted: 9 January 1999     

The lateral line receptor array of cyprinids from different habitats

The lateral line system of teleost fishes consists of an array of superficial and canal neuromasts (CN). Number and distribution of neuromasts and the morphology of the lateral line canals vary across species. We investigated the morphology of the lateral line system in four diurnal European cyprinids, the limnophilic bitterling (Rhodeus sericeus), the indifferent gudgeon (Gobio gobio), and ide (Leuciscus idus), and the rheophilic minnow (Phoxinus phoxinus). All fish had lateral line canals on head and trunk. The total number of both, CN and superficial neuromasts (SN), was comparable in minnow and ide but was greater than in gudgeon and bitterling. The ratio of SNs to CNs for the head was comparable in minnow and bitterling but was greater in gudgeon and ide. The SN‐to‐CN ratio for the trunk was greatest in bitterling. Polarization of hair cells in CNs was in the direction of the canal. Polarization of hair cells in SNs depended on body area. In cephalic SNs, hair cell polarization was dorso‐ventral or rostro‐caudal. In trunk SNs, it was rostro‐caudal on lateral line scales and dorso‐ventral on other trunk scales. On the caudal fin, hair cell polarization was rostro‐caudal. The data show that, in the four species studied here, number, distribution, and orientation of CNs and SNs cannot be unequivocally related to habitat. J. Morphol. 275:357–370, 2014. © 2013 Wiley Periodicals, Inc.     

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 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.     

Lateral line reception in still- and running water

The lateral line of fish is composed of neuromasts used to detect water motions. Neuromasts occur as superficial neuromasts on the skin and as canal neuromasts in subepidermal canals. Fibres of the lateral line nerves innervate both. There have been extensive studies on the responses of lateral line nerve fibres to dipole stimuli applied in still water. However, despite the fact that many fish live in rivers and/or swim constantly, responses of lateral line nerve fibres to dipole stimuli presented in running water have never been recorded. We investigated how the peripheral lateral line of still water fish ( Carassius auratus) and riverine fish ( Oncorhynchus mykiss) responds to minute sinusoidal water motions while exposed to unidirectional water flow. Both goldfish and trout have two types of posterior lateral line nerve fibres: Type I fibres, which most likely innervate superficial neuromasts, were stimulated by running water (10 cm s(-1)). The responses of type I fibres to water motions generated by a vibrating sphere were masked if the fish was exposed to running water. Type II fibres, which most likely innervate canal neuromasts, were not stimulated by running water. Consequently, responses of type II fibres to a vibrating sphere were not masked under flow conditions.