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PubMed1999

Loss of ectodermal competence for lateral line placode formation in the direct developing frog Eleutherodactylus coqui.

In the direct-developing frog Eleutherodactylus coqui neuromasts and ganglia of the lateral line system never develop. We show here that this absence of the lateral line system, which is evolutionarily derived in anurans, is due to very early changes in development. Ectodermal thickenings, which are typical of lateral line placodes, and from which neuromasts and ganglion cells of the lateral line originate, never form in E. coqui, although other neurogenic placodes are present. Moreover, although NeuroD is expressed in the lateral line placodes of Xenopus laevis, corresponding expression sites are lacking in E. coqui. Heterospecific transplantation experiments show that axolotl ectoderm can be induced to form lateral line placodes after transplantation to E. coqui hosts but that E. coqui ectoderm does not form lateral line placodes on axolotl hosts. This suggests that the loss of the lateral line system in E. coqui is due to the specific loss of ectodermal competence to form lateral line placodes in response to inductive signals. Our results (1) indicate that the competence for lateral line placode formation is distinct and dissociable from the competence to form other neurogenic placodes and (2) support the idea that the lateral line system acts as a module in development and evolution.

Animals↗
PubMed2002

Development and evolution of lateral line placodes in amphibians. - II. Evolutionary diversification.

The amphibian lateral line system develops from a series of lateral line placodes. The different phases of development from early induction, to pattern formation, differentiation, morphogenesis, and metamorphic fate were summarized in the first part of this review (Schlosser, 2002a). Here, a survey of the diversity of lateral line systems in amphibians is presented indicating that most phases of lateral line development have been subject to evolutionary changes. Several trends suggest important roles for both adaptive changes and internal constraints in amphibian lateral line evolution. Many of these trends involved the coordinated modification of different derivatives of lateral line placodes suggesting that these placodes are not only autonomous developmental modules, but also units of evolutionary variation that tend to be modified in a coherent and largely context-independent fashion.

Journal Article↗
PubMed1983

The acoustic and lateral line nuclei are distinct in the premetamorphic frog, Rana catesbeiana.

The transition from aquatic to terrestrial hearing in the frog occurs during metamorphosis and during the disappearance of the lateral line system. The coincidence in time of these two processes and morphological similarities between the acoustic and lateral line systems has led to the suggestion (Larsell, '34) that the lateral line nuclei are transformed into the acoustic nuclei. The relation between the acoustic and lateral line systems was investigated by studying the distribution of primary afferents, the dendritic patterns of the cells in the primary nuclei, and the development of the nuclei in the premetamorphic bullfrog, Rana catesbeiana. The posterior and anterior lateral line roots distribute to a neuropil located medial to the dorsal medullary nucleus. Horseradish peroxidase (HRP) injections into the contralateral tegmentum fill cells in the periventricular region whose dendrites ramify within the neuropil. These cells constitute the lateral line nuclei. The amphibian and basilar papillary roots of the acoustic system distribute to the more lateral nuclear region. The dendrites of these cells arborize within the nucleus and not in the lateral line neuropil. The dorsal medullary nucleus is, therefore, the acoustic nucleus (AcN). [3H]-thymidine labeling reveals that newly generated cells occupy the AcN within a few hours of their formation throughout the period when anatomical analysis shows the parallel growth and diminution of the lateral line neuropil and nuclei. This study indicates that the lateral line and acoustic systems are morphologically independent at the level of the primary afferents and primary nuclei throughout early development.

Animals↗
PubMed2005

Impact of acute cadmium exposure on the trunk lateral line neuromasts and consequences on the "C-start" response behaviour of the sea bass (Dicentrarchus labrax L.; Teleostei, Moronidae).

Behavioural responses of sea bass Dicentrarchus labrax were investigated after exposure to cadmium ions in laboratory-controlled conditions. The aim of this study was to discover whether environmental exposure to cadmium ions inactivates fish lateral line system neuromasts, and to determine the behavioural consequences of such a sensory blockage. For this, fish escape behaviour in response to an artificial water jet was recorded using a 25-frames s(-1) analog video camera before and after cadmium exposure. Experimental set up was tested with fish whose lateral line system was artificially inactivated by antibiotics (gentamicin and streptomycin). Histological analyses with scanning electron microscopy showed antibiotic treatment destroyed lateral line system neuromasts. In addition, these fish did not respond to stimulations provoked by the water jet after antibiotic treatment. Fish escape behaviour was then recorded before and after cadmium exposure at two different concentrations. When fish were exposed to the first concentration of cadmium tested (0.5 microg l(-1), which represents the maximal cadmium concentration encountered in contaminated estuaries), no alteration in neuromast tissue was observed. In addition, before cadmium exposure, fish responded positively in 98.41 +/- 4.95% of lateral line system stimulations (escape behaviour in response to the water jet). After cadmium exposure, no behavioural modification could be detected: the fish responded positively in 95.16 +/- 9.79% of stimulations (chi(2) = 2.464, p = 0.116). In contrast, the high cadmium concentration used (5 microg l(-1), which represents 10 times the concentration occurring in highly polluted estuarine areas) involved severe neuromast tissue damage. Just after such cadmium exposure, fish showed only 41.67 +/- 35.36% of positive responses to their lateral line system stimulations, while they responded positively in 95.93 +/- 9.10% of stimulations under control conditions (chi(2) = 24.562, p < 0.0001). Their lateral line system neuromasts seemed to regenerate about 1 month after cadmium exposure. Associated with this regeneration, from the 21st day after cadmium exposure, their escape behaviour had recovered and was not significantly different from that recorded under control conditions (86.74 +/- 20.82%, chi(2) = 2.876, p = 0.090). This study shows that although 5 microg l(-1) cadmium is able to damage lateral line system neuromasts and causes fish behavioural alterations, fish exposed to 0.5 microg l(-1) cadmium displayed neither tissue neuromast nor behavioural modification.

Animals↗
PubMed1995

Fusarium solani fungal infection of the lateral line canal system in captive scalloped hammerhead sharks (Sphyrna lewini) in Hawaii.

Two of five scalloped hammerhead sharks (Sphyrna lewini) captured May 1987 in Hawaii (USA) developed granulomatous exudative mycotic dermatitis localized in the lateral line canal system. The lesion initially was noted in the cephalic canals, but over a period of months extended into the lateral canal. Fusarium solani and Vibrio spp. were isolated from the canal exudate of both sharks. Bacterial colonies were not observed in the canal walls or surrounding tissues. Fusarium solani infection resulted in a chronic physical and behavioral deterioration of the two sharks; one shark was euthanized in September 1988 and the other in July 1989. This is the first report of Fusarium solani infection in the lateral line canal system and the third account in hammerhead sharks.

Animals↗
PubMed1989

Development of the electrosensory nervous system in Eigenmannia (Gymnotiformes): I. The peripheral nervous system.

The nerves of the anterior lateral line system in embryonic and larval stages of the weakly electric gymnotiform fish Eigenmannia were visualized by injection of the fluorescent marker DiI into the primordium of the anterior (ALLN) and posterior (PLLN) lateral line nerves. Examination of developmental series reveals that the nerve fibers that innervate the electrosensory and mechanosensory components of the anterior lateral line system are present before the first mechanoreceptors and electroreceptors have differentiated. This suggests that nerve fibers might induce the formation of lateral line receptors. Whereas the innervation of the mechanoreceptive system is already established at an early stage, the afferent innervation of electroreceptors continues to arborize in the periphery, presumably by following pioneer axon pathways. The earliest recognizable stage of the anterior lateral line nerve ganglion (ALLNG) is evident 2 days after spawning. The ganglion shows two germinal cell masses that develop into the supraorbital-infraorbital and the hyomandibular placodes. The supraorbital-infraorbital placode forms the dorsal part of the ALLNG; the hyomandibular placode forms the ventral part of the ALLNG. Counts of ALLNG cells in embryonic, larval, and adult stages of Eigenmannia show that, at each stage examined, the number of ganglion cells is always significantly larger than the number of mechanoreceptors and electroreceptor units in the periphery. During development, the distribution of ALLNG cell diameters shifts from a unimodal distribution in juveniles to a bimodal distribution in adults, peaking at 8 microns and 18 microns. These results suggest that tuberous electroreceptive organs, which are innervated by the large ALLNG cells, may not be functional prior to day 18. Our results further suggest that the number of ALLNG cells correlates with the rate of induction of lateral line receptors in the periphery.

Animals↗
PubMed1996

Pigment patterns of larval salamanders (Ambystomatidae, Salamandridae): the role of the lateral line sensory system and the evolution of pattern-forming mechanisms.

In many species of salamanders, pigment cells derived from the neural crest give rise to a horizontal stripe pattern in hatchling larvae. A defining element of these horizontal stripe patterns is a region over the middle of the myotomes that is relatively free of melanophores. This study shows that formation of a "melanophore-free region" and horizontal stripe pattern in Ambystoma tigrinum tigrinum (family Ambystomatidae) correlates with the development of the trunk lateral line sensory system. Moreover, prevention of lateral line development results in greater densities of melanophores in the middle of the flank, essentially eliminating the melanophore-free region in this taxon. A phylogenetic survey also revealed that ablation of the lateral lines has qualitatively similar effects on melanophores in seven of eight additional taxa (Ambystomatidae: A. barbouri, A. maculatum, A. talpoideum; Salamandridae: Notophthalmus viridescens, Pleurodeles waltl, Taricha granulosa, T. rivularis). In Taricha torosa, however, a superficially similar melanophore-free region forms prior to lateral line development, and ablation of the lateral lines does not perturb the horizontal stripe pattern. Finally, heterospecific grafting experiments demonstrated that T. torosa lateral lines are competent to generate a melanophore-free region, and T. torosa melanophores are competent to respond to cues associated with the lateral lines. These results indicate that lateral line-dependent pattern-forming mechanisms are common and probably ancestral within the families Ambystomatidae and Salamandridae and suggest that these ancestral mechanisms have been retained in T. torosa as redundant, lateral line-dependent mechanisms for stripe formation have evolved.

Ambystomatidae↗
PubMed2005

Sub-lethal concentrations of waterborne copper are toxic to lateral line neuromasts in zebrafish (Danio rerio).

In teleosts, the lateral line system is composed of neuromasts containing hair cells that are analogous to those present in the inner ear of all vertebrates. In the zebrafish embryo and early larva, this system is composed of the anterior lateral line (ALL), which covers the head, and the posterior lateral line (PLL), present in the trunk and tail. The mechanosensory hair cells found in neuromasts can be labeled in vivo using fluorescent dyes such as 4-di-2-Asp (DiAsp) or FM1-43. We have studied the effects of water-borne copper exposure on the function of the lateral line system in zebrafish larvae. Our results show that transient incubation of post-hatching larvae for 2h with non-lethal concentrations of copper (1-50 microM CuSO4) induces cellular damage localized to neuromasts, apoptosis, and loss of hair cell markers. This effect is specific to copper, as other metals did not show these effects. Since hair cells in fish can regenerate, we followed the reappearance of viable hair cells in neuromasts after copper removal. In the PLL, we determined that there is a threshold concentration of copper above which regeneration does not occur, whereas, at lower concentrations, the length of time it takes for viable hair cells to reappear is dependent on the amount of copper used during the treatment. The ALL behaves differently though, as regeneration can occur even after treatments with concentrations of copper an order of magnitude higher than the one that irreversibly affects the PLL. Regeneration of hair cells is dependent on cell division within the neuromasts as damage that precludes proliferation prevents reappearance of this cell type.

Animals↗
PubMed2006

The laterophysic connection and swim bladder of butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae).

The laterophysic connection (LC) is an association between bilaterally paired, anterior swim bladder extensions (horns) and medial openings in the supracleithral lateral line canals that diagnoses butterflyfishes in the genus Chaetodon. It has been hypothesized that the LC makes the lateral line system sensitive to sound pressure stimuli that are transmitted by the swim bladder horns and converted to fluid flow into the lateral line system via a laterophysic tympanum. The purpose of this study was to define variation in the morphology of the LC, swim bladder and swim bladder horns among 41 Chaetodon species from all 11 Chaetodon subgenera and a species from each of four non-Chaetodon genera using gross dissection, histological analysis as well as 2D or 3D CT (computed tomographic) imaging of live, anesthetized fishes. Our results demonstrate that the lateral line system appears rather unspecialized with well-ossified narrow canals in all species examined. Two LC types (direct and indirect), defined by whether or not the paired anterior swim bladder horns are in direct contact with a medial opening in the supracleithral lateral line canal, are found among species examined. Two variants on a direct LC and four variants of an indirect LC are defined by combinations of soft tissue anatomy (horn length [long/short] and width [wide/narrow], number of swim bladder chambers [one/two], and presence/absence of mucoid connective tissue in the medial opening in the supracleithrum). The combination of features defining each LC variant is predicted to have functional consequences for the bioacoustics of the system. These findings are consistent with the recent discovery that Chaetodon produce sounds during social interactions. The data presented here provide the comparative morphological context for the functional analysis of this novel swim bladder-lateral line connection.

Air Sacs↗
PubMed2004

Lateral line-mediated rheotactic behavior in tadpoles of the African clawed frog (Xenopus laevis).

Tadpoles (Xenopus laevis) have a lateral line system whose anatomical structure has been described, but whose functional significance has not been closely examined. These experiments tested the hypothesis that the lateral line system is involved in rheotaxis. Tadpoles in developmental stages 47-56 oriented toward the source of a water current. Orientation was less precise after treatment with cobalt chloride or streptomycin, but was similar to that of untreated animals after exposure to gentamicin. In no current conditions, tadpoles exhibited a characteristic head-down posture by which they held themselves in the water column at an angle around 45 degrees. This body posture became significantly less tilted in the presence of water current. Treatment with cobalt chloride or streptomycin increased the angle of tilt close to that seen in no current conditions, while gentamicin treatment tended to decrease tilt angle. The data are consistent with anatomical and physiological findings that tadpole neuromasts are similar to superficial, but not canal, neuromasts in fishes, and they suggest that the lateral line system is involved in both directional current detection and current-related postural adjustments in Xenopus.

Animals↗
PubMed2005

Estimating position and velocity of a submerged moving object by the clawed frog Xenopus and by fish--a cybernetic approach.

The lateral-line system is a unique facility of aquatic animals to locate predator, prey, or conspecifics. We present a detailed model of how the clawed frog Xenopus, or fish, can localize submerged moving objects in three dimensions by using their lateral-line system. In so doing we develop two models of a slightly different nature. First, we exploit the characteristic properties of the velocity field, such as zeros and maxima or minima, that a moving object generates at the lateral-line organs and that are directly accessible neuronally, in the context of a simplified geometry. In addition, we show that the associated neuronal model is robust with respect to noise. Though we focus on the superficial neuromasts of Xenopus the same arguments apply mutatis mutandis to the canal lateral-line system of fish. Second, we present a full-blown three-dimensional reconstruction of the source on the basis of a maximum likelihood argument.

Animals↗
PubMed1991

Morphology, distribution and innervation of the lateral-line receptors of the Florida gar, Lepisosteus platyrhincus.

The lateral-line system of gars consists of superficial neuromasts, which are arranged in lines termed pit lines, canal neuromasts and spiracular organs, which are located within diverticula of the hyoid gill pouch. Both canal and superficial neuromasts possess polarized hair cells whose directional sensitivity parallels the long axis of their respective lines. However, the apical surfaces of canal neuromasts are larger and possess far more hair cells than do those of superficial neuromasts, but superficial neuromasts have longer kinocilia and, presumably, longer cupulae. The receptors of the lateral-line system are innervated by three pairs of cranial nerves: anterior, middle and posterior lateral-line nerves. The anterior lateral-line nerves innervate neuromasts of the supraorbital, infraorbital and preoperculo-mandibular canals as well as dorsally located anterior pit lines, cheek (horizontal, vertical and mandibular) and gular pit lines of superficial neuromasts and the spiracular organ. The middle lateral-line nerves innervate dorsally located middle pit lines and a single neuromast in each temporal canal. The posterior lateral-line nerves innervate dorsally located posterior pit lines, neuromasts of the supratemporal commissures and all remaining postotic and trunk neuromasts. The ganglion of the anterior lateral-line nerve is divided into dorsal and ventral subganglia; the single ganglion of the middle lateral line nerve has no recognizable subdivisions, and the ganglion of the posterior lateral-line nerve consists of rostral and caudal subganglia. Analysis of the roots of these nerves and review of the embryonic origin of their ganglia as well as comparisons with cranial nerves in other anamniotes suggest that the anterior and posterior lateral-line nerves of gars may represent the fusion of four to five separate lateral-line nerves at some stage in vertebrate phylogeny. Thus, with the addition of the middle lateral-line nerve, and the possible existence of a ventral lateral-line nerve of the trunk, it is possible that the earliest jawed vertebrates possessed six or even seven pairs of lateral-line nerves.

Afferent Pathways↗
PubMed2006

Neural responses of goldfish lateral line afferents to vortex motions.

The lateral line system of fish is sensitive to weak water motions. We recorded from posterior lateral line nerve afferents while stimulating goldfish, Carassius auratus, with unidirectional water flow and with a vortex ring. Posterior lateral line afferents of goldfish were either flow sensitive or flow insensitive. Both types of afferents responded to a vortex ring that passed the fish laterally with one to three reproducible patterns of neural activity, followed by activity patterns that were less reproducible. Using particle image velocimetry, we visualized and quantified the water motions in the vertical plane next to the surface of the fish while recording from lateral line afferents. Early response components correlated with the direction of water motions that occurred at the position of the neuromast recorded from. By contrast, neural activity that occurred after the vortex had passed the fish barely predicted the direction of water motions. These results are in agreement with the known directional sensitivity of hair cells and indicate that fish might be able to extract sensory information from complex stimuli like vortices by comparing the activity of a whole array of neuromasts. The stimulus used in this study is novel to lateral line research and resembles some of the hydrodynamic stimuli that fish might encounter in their natural environments. We expect that by combining naturalistic hydrodynamic stimuli and central nervous recordings, we will learn if and how hydrodynamic feature detection is accomplished by the lateral line system.

Action Potentials↗
PubMed2000

The overlapping roles of the inner ear and lateral line: the active space of dipole source detection.

The problems associated with the detection of sounds and other mechanical disturbances in the aquatic environment differ greatly from those associated with airborne sounds. The differences are primarily due to the incompressibility of water and the corresponding increase in importance of the acoustic near field. The near field, or hydrodynamic field, is characterized by steep spatial gradients in pressure, and detection of the accelerations associated with these gradients is performed by both the inner ear and the lateral line systems of fishes. Acceleration-sensitive otolithic organs are present in all fishes and provide these animals with a form of inertial audition. The detection of pressure gradients, by both the lateral line and inner ear, is the taxonomically most widespread mechanism of sound-source detection amongst vertebrates, and is thus the most likely primitive mode of detecting sound sources. Surprisingly, little is known about the capabilities of either the lateral line or the otolithic endorgan in the detection of vibratory dipole sources. Theoretical considerations for the overlapping roles of the inner ear and lateral line systems in midwater predict that the lateral line will operate over a shorter distance range than the inner ear, although with a much greater spatial resolution. Our empirical results of dipole detection by mottled sculpin, a benthic fish, do not agree with theoretical predictions based on midwater fishes, in that the distance ranges of the two systems appear to be approximately equal. This is almost certainly as a result of physical coupling between the fishes and the substrate. Thus, rather than having a greater active range, the inner ear appears to have a reduced distance range in benthic fishes, and the lateral line distance range may be concomitantly extended.

Animals↗
PubMed1987

Primary neurons of the lateral line nerves and their central projections in hagfishes.

The hagfish lateral line system was studied by horseradish peroxidase transganglionic transport. The anterior lateral line nerve innervates the group of lateral line canals situated anteriorly to the eye, and the posterior lateral line nerve innervates the group of canals situated posteriorly to the eye. Although both nerves pass through the muscle fascia at the same point, each runs a different course to the brain. The anterior lateral line nerve runs near the trigeminal nerve and its ganglion is closely attached to the trigeminal ganglion, but both systems are completely independent. The posterior lateral line nerve runs independently of any other cranial nerve and makes a peculiar U-turn at the point of entry to the brain capsule. The anterior lateral line ganglion contains both cutaneous sensory cells (small to large cells) and lateral line sensory cells (small cells); from this ganglion projections run to both the trigeminal sensory nucleus (fine and thick fibers) and medial nucleus of the area acousticolateralis (fine fibers). The posterior lateral line ganglion contains only small lateral line cells that project fine fibers to the medial nucleus of the area acousticolateralis. There are no efferent components in this lateral line system, and its only afferent terminal field is the medial nucleus of the area acousticolateralis.

Afferent Pathways↗
PubMed2002

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.

Anguilla↗
PubMed2001

Strike feeding behavior in the muskellunge, Esox masquinongy: contributions of the lateral line and visual sensory systems.

The muskellunge, Esox masquinongy, is a predatory esocid fish with well-developed visual and lateral line systems. The purpose of this study was to determine the relative roles of these two sensory modalities in organizing the strike behavior of the animal. Subadult muskellunge were videotaped in a test arena while feeding on fathead minnows (Pimephales promelas). Animals were tested under five conditions: (i) control animals in which the visual and lateral line systems were intact; (ii) animals with lateral line afference suppressed by immersion for 12-24 h in 0.1 mmol l(-1) CoCl2; (iii) animals blinded by bilateral optic nerve transection; (iv) animals that had been unilaterally blinded; and (v) animals in which the lateral line system had been unilaterally denervated. The feeding behavior of the muskellunge consists of two phases: a slow stalk of the prey with minimal body movement followed by an explosive C- or S-start lunge at the prey. Quantitative comparisons of animals in the five test groups indicate that, although vision is used in the initial acquisition of the prey, both vision and the lateral line system play important roles in determining the initiation of the rapid strike. The lateral line system may play a critical role in the final capture of the prey at the end of the strike. In addition, lateral-line-suppressed muskellunge strongly alter their approaches to more distant prey. Bilaterally blinded muskellunge do not stalk their prey, but will lunge only at prey that are at close range. Unilaterally blinded or denervated muskellunge also alter their detection of and approach to prey, attending to a wider region of the intact sensory hemisphere. Our data suggest not only that the visual and lateral line systems play complementary roles in the feeding behavior sequence but also that each system plays a more or less dominant role during consecutive phases of the behavior.

Animals↗
PubMed2000

The cytoskeletal effector xPAK1 is expressed during both ear and lateral line development in Xenopus.

xPAK1, a probable effector of stress activated MAP-kinase SAPK1/JNK activation and cytoskeletal dynamics, was found to be ubiquitously expressed within the Xenopus laevis ear and lateral line system during the development and differentiation of these organs. xPAK1 expression was very strong in the otic placode from its condensation, and expression continued in the otic vesicle up until stage 35/36, after which it abruptly ceased. At stage 29/30 expression occurred specifically in the epithelium of the otic vesicle, which includes the prospective sensorial epithelium. Expression of xPAK1 was also observed in the lateral line system from stage 35/36, at which stage the lateral line primordia have begun to migrate from the region of the otic vesicle. Lateral line expression continued at least until stage 37/38, at which time xPAK1 was noted in association with the differentiating lateral line organs. To our knowledge, xPAK1 is the first ubiquitous lateral line marker that is also expressed in the ear. In the context of previous studies, our data suggest that xPAK1 either plays a role in the differentiation of the mechano-sensors of the auditory system or in the formation of the otic vesicle epithelium and the lateral line primordia.

Age Factors↗