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Development of the lateral line system in Xenopus laevis. III. Development of the supraorbital system in triploid embryos and larvae.

During normal development of the supraorbital lateral line system of Xenopus, an elongated streak of primordial cells becomes subdivided into a linear series of cell groups containing only about eight cells each, thus forming a row of primary lateral line organs (Winklbauer & Hausen, 1983a,b). In triploid Xenopus embryos, cell size is 1.5 X normal. When the formation of lateral line organs occurs in triploid primordia, the nascent organs contain only about five or six cells each, i.e. about two thirds of normal. Thus, the increase in cell size is compensated for by a corresponding reduction in cell number, keeping constant the organ size in terms of total cell mass or volume. This result excludes a cell counting mechanism for determining organ size. In diploids, the primary organs, although being of equal size initially, differ vastly in their final size and exhibit a peculiar frequency distribution of organ sizes. A detailed quantitative model for supraorbital lateral line development has been proposed, which accounts for this characteristic frequency distribution (Winklbauer & Hausen, 1983b). This model makes precise predictions as to the frequency distribution of the final size of triploid lateral line organs, where the initial organ size is reduced to five or six cells. These predictions were verified experimentally.

Animals↗

S-100 protein is a selective marker for sensory hair cells of the lateral line system in teleosts.

The distribution of S100 protein in the neuromast of the lateral line system (LLS) was investigated immunohistochemically in alevins of three species of teleosts (Salmo trutta, Salmo salar and Dicentrarchus labrax), using a polyclonal antibody. In both the neuromasts of the canals, as well as in the pit organs, the hair cells, regarded as the specific sensory cells, displayed cytoplasmic immunoreactivity for S100 protein. Conversely, the supporting cells, mantle cells and basal cells were devoid of immunoreaction. These results demonstrate for the first time the occurrence of S100 in the LLS of teleosts. Due to the cell specific localization, this protein might serve as a marker for sensory hair cells in neuromasts.

Animals↗

Observations on the development of the lateral line system in the Pacific hagfish (Eptatretus stouti, Myxinoidea).

We investigated the development of the lateral line system of the Pacific hagfish, Eptatretus stouti, using three-dimensional reconstructions from serial sections. Adult hagfishes possess a number of densely innervated skin grooves of unknown function, and these grooves do not contain typical lateral line receptors (i.e. neuromasts). However, three separate lateral line placodes appear to be present during development and these placodes give rise to groups of neuromast primordia. Unlike in other craniates, the neuromast primordia do not develop into neuromasts, but they apparently transform into the skin grooves of adults.

Animals↗

Cadherin-2 function in the cranial ganglia and lateral line system of developing zebrafish.

Cadherins are cell surface molecules that mediate cell-cell adhesion through homophilic interactions. Cadherin-2 (also called N-cadherin), a member of classic cadherin subfamily, has been shown to play important roles in development of a variety of tissues and organs, including the nervous system. We recently reported that cadherin-2 was strongly expressed by the majority of cranial ganglia and lateral line system of developing zebrafish. To gain insight into cadherin-2 role in the formation of these structures, we have used several markers to analyze zebrafish embryos injected with a specific cadherin-2 antisense morpholino oligonucleotide (cdh2MO). We find that development of several cranial ganglia, including the trigeminal, facial, and vagal ganglia, and the lateral line ganglia and neuromasts of the cdh2MO-injected embryos are severely disrupted. These phenotypes were confirmed by analyzing a cadherin-2 mutant, glass onion. Our results suggest that cadherin-2 function is crucial for the normal formation of the zebrafish lateral line system and a subset of cranial ganglia.

Animals↗

Central organization of eighth nerve and mechanosensory lateral line systems in the brainstem of ictalurid catfish.

The octavolateral sensory systems in teleost fish comprise at least four distinct hair-cell sensory modalities which are processed separately within the CNS. Two of these modalities, the mechanosensory lateral line system and the eighth nerve auditory system, have been implicated in the animal's ability to detect and localize underwater vibrations. Distinct mechanosensory lateral line and auditory nuclei are present within the torus semicircularis, the midbrain homologue of the inferior colliculus. The present study utilized horseradish peroxidase tracing techniques to delineate those areas of the lower brainstem which are involved in auditory as opposed to mechanosensory lateral line processes. The primary mechanosensory nucleus of the medulla, n. medialis, projects directly to the optic tectum and to the mechanosensory nucleus of the torus semicircularis. Nucleus medialis receives input from primary lateral line nerve fibers as well as from a number of sites within the CNS: n. praeeminentialis pars ventralis, and the eminentia granularis and lobus caudalis of the cerebellum. The n. praeeminentialis itself receives a descending input from the mechanosensory nucleus of the torus semicircularis. These mechanosensory lateral line pathways are parallel to, but distinct from, those of the electrosensory lateral line system. Auditory signals reach the midbrain via an entirely separate route. The octaval nerve terminates in a column of five medullary nuclei. Of these, only the anterior and descending octaval nuclei maintain a direct but sparse projection to the auditory nucleus of the midbrain. The bulk of the auditory input to the midbrain involves a newly described medullary nucleus, the medial auditory nucleus of the medulla. This nucleus receives input from the descending octaval nucleus and projects bilaterally to the auditory nucleus of the torus semicircularis. It is suggested that the medial auditory nucleus of the medulla is homologous to portions of the superior olivary complex of other vertebrates.

Afferent Pathways↗

Development of the lateral line system in Xenopus laevis. II. Cell multiplication and organ formation in the supraorbital system.

Cell multiplication was studied during development of the supraorbital lateral line system in Xenopus laevis. The increase in cell number is biphasic. The first phase extends from the beginning of primordial elongation to the end of primary organ formation. Cell number increases linearly during this interval. Throughout this phase, a constant number of cells is in S phase of the cell cycle at a given time, despite a more than 10-fold increase in total cell number. After their formation, the number of the primary organs remains essentially constant. The individual primary organs are not clones of cells. Different organs grow at different rates, and become more and more heterogeneous in size. The second phase which is correlated with accessory organ formation is characterized by an elevated growth rate. This phase was not studied in detail. If developing larvae are starved, growth is normal up to completion of the first growth phase but is arrested at this point. The frequency distribution of the sizes of such growth-arrested organs approximates a binominal distribution. From its characteristics, a detailed model of cell proliferation and organ formation can be deduced: cell multiplication occurs through asymmetrically dividing stem cells, which become allocated to the forming organs at random and go through a fixed number of cell divisions.

Animals↗

Choline acetyltransferase activity in the cerebellum and in centers of lateral line system of teleosts.

Using choline acetyltransferase as a marker of cholinergic activity, different cerebellar areas and brainstem nuclei were assayed in the goldfish and the catfish. Enzyme activity resulted remarkedly higher in archicerebellum than in paleocerebellum. In addition three brainstem nuclei related to lateral line system, showed high or very high levels of choline acetyltransferase. The results suggest that cholinergic transmission would play an important role in central circuits of lateral line system, including the projection towards archicerebellar areas.

Animals↗

Ontogeny of the head of the Pacific hagfish (Eptatretus stouti, Myxinoidea): development of the lateral line system.

The head of adult hagfishes (jawless craniates, Myxinoidea) of the family Eptatretidae displays a number of skin grooves of uncertain origin. These grooves have been homologized to the neuromast lines of other craniates, and they are innervated by two ganglionated cranial nerves that have been interpreted as lateral line nerves. The grooves do not, however, contain the compound receptors that are typical of a lateral line (i.e. neuromasts or electroreceptors), and both their development and function have remained enigmatic. To elucidate the embryonic origin of the grooves (which should develop from placodes if they are homologues of the lateral line system), embryos of Pacific hagfish were examined by means of three-dimensional reconstructions from serial sections. Because of the scarcity of specimens of embryonic hagfishes, only two embryos were reconstructed, but these reconstructions clearly show that a number of placodes and placodal derivatives (i.e. sensory ridges, receptor primordia, and cranial ganglia) occur in the head of embryonic eptatretid hagfishes. Some of these placodes correspond to the lens and epibranchial placodes of other craniates, but there are also three other placodes which represent possible homologues of lateral line placodes. The topology of the placodes in this latter group corresponds to the topology of the grooves of adult hagfishes, and we therefore reach three conclusions: (i) that an embryonic lateral line system is present in hagfishes; (ii) that the grooves of adult hagfishes in all probability derive from lateral line placodes; and (iii) that the presence of lateral line placodes is a primitive character of craniates.

Afferent Pathways↗

The cranial lateral-line system in Clarias gariepinus (Burchell, 1822) (Siluroidei:Clariidae): morphology and development of canal related bones.

The cranial lateral-line system, as well as the canal bones are well developed in the African clariid catfish Clarias gariepinus. A generalised cranial lateral-line pattern is present (supraorbital, infraorbital, preoperculo-mandibular, otic, postotic and temporal canals). The supratemporal commissure, however, is missing, although a supraorbital commissure is present (formed through the fusion of the epiphysial branches). In addition to canals, some pit-lines are present which cover both canal regions and non-canal regions (vertical, horizontal, oral, anterior, middle and posterior pit-lines). In this paper, several ontogenetic stages of the canal related bones in C. gariepinus were studied. A description of the canal bones, as well as some considerations concerning their nomenclature are given. All canal bones develop, whereas the parietal bone seems to have fused with the supraoccipital bone during ontogeny, as has been observed in some siluroids. The extrascapulars (= supratemporals) are missing in C. gariepinus, as is the case in many siluroids. The posttemporal and supracleithral bones have fused as well. Surprisingly, some separate splenial bones, enclosing the distal part of the mandibular canal are present. Some secondary modifications indicate the apomorphic features of the Clariidae. The infraorbital bones, from which the antorbital bone has lost the antorbital commissure, and the suprapreopercular bone are enlarged, plate-like bones. The nasal bone has undergone some secondary, plate-like extensions as well.

Animals↗

Development of the mechanoreceptive lateral-line system in the axolotl: placode specification, guidance of migration, and the origin of neuromast polarity.

The mechanosensory lateral-line system offers a unique opportunity to study a wide variety of developmental phenomena, including cell migration, the origin of polarity, and pattern formation. In this study, we use a series of transplantation experiments to examine some of the factors affecting the origin of the lateral-line placodes, the establishment of sensory organ polarity and placement, and the guidance of cell migration in the Mexican axolotl (Ambystoma mexicanum). We find that placode-forming ectoderm is at least partially specified as early as the beginning of neurulation, and we suggest that this may be a result of early processes involved in neural induction. Furthermore, we find that the migration of the primordia on the body depends on the presence of both the ectoderm and the subjacent mesoderm for guidance. Sensory organ polarity on the body appears to be the result of an interaction between the primordia, which deposit organs of set polarity relative to the direction of migration, and the substrate, which determines the direction of migration. Spacing of the organs is independent of the substrate, and may be due to an intrinsic property of either the primordia or the emerging organs themselves. Finally, we suggest that the lateral-line primordia are guided, as they migrate, by a contact guidance mechanism.

Ambystoma↗

The electrical response of the lateral line system of fish to tone and other stimuli.

1. The lateral line of Fundulus heteroclitus and Fundulus majalis is shown to react to tone at an intensity level of 20 dynes per sq. cm. at frequencies up to 200 or 300 cycles per second. 2. Evidence is given that the nerve can reproduce the stimulating tone frequency up to at least 180 cycles per second. 3. The response of the lateral line to the swimming movements of nearby fish is demonstrated. 4. Fundulus and several other species are shown to give strong spontaneous activity of the lateral line nerve.

Animals↗

Organization of the lateral line system in embryonic zebrafish.

We describe the organization of lateral line nerves and ganglia in the embryonic zebrafish, Danio rerio. Two lateral line nerves are found anterior to the otic vesicle: the anterodorsal nerve innervates neuromasts of the supraorbital, infraorbital, and otic lines, whereas the anteroventral nerve innervates the mandibular and opercular lines. An additional two lateral line nerves are found posterior to the otic vesicle: the middle lateral line nerve innervates the middle line, whereas the posterior nerve innervates the occipital dorsal and posterior trunk lines. Preotic nerves converge on a single entry zone into the central nervous system at the facial motor root (mVII), as do axons of the octaval nerve. Postotic nerves converge to a posterior entry zone at the glossopharyngeal root. Both lateral line ganglia and neuromasts develop on a stereotypical schedule. To examine the segmental relationships among cranial ganglia, neural crest, and hindbrain, lateral line organization was analyzed in valentino mutants, which have disruptions in the development of rhombomeres 5-7 and in the third arch neural crest, and are missing glossopharyngeal motor neurons. The proposed corresponding lateral line nerve for this head segment, the middle lateral line, appears to develop normally. However, the middle and posterior nerves do not form a posterior entry zone in the absence of a glossopharyngeal root in val mutants, but instead course anteriorly to join the preotic nerves.

Animals↗

Hindbrain signal processing in the lateral line system of the dwarf scorpionfish Scopeana papillosus

Recordings were made from primary afferent fibres and secondary projection neurones (crest cells) in the mechanosensory lateral line system of the dwarf scorpionfish. Crest cells were identified by antidromic stimulation from the contralateral midbrain. Differences between primary afferent fibre and crest cell response characteristics are indicative of signal processing by the neuronal circuitry of the medial octavolateralis nucleus. There are a number of differences between primary afferent fibres and crest cells. Primary afferents have relatively high levels of spontaneous activity (mean close to 40 impulses s-1) and many of them are strongly modulated by ventilation. By contrast, crest cells have a much lower rate of spontaneous activity that is not obviously modulated by ventilation. Primary afferents show a simple tonic response to a maintained stimulus, whereas crest cells show a variety of temporal response properties, but in general show a phasic/tonic response to the same prolonged stimulus. Afferents are most sensitive to frequencies of stimulation around 100 Hz; in contrast, crest cells show a strong suppression of activity at this frequency. Crest cells are most responsive around 50 Hz. These afferent/secondary comparisons show similarities with those reported for allied electrosensory and auditory pathways.

Journal Article↗

Selective labeling of sensory hair cells and neurons in auditory, vestibular, and lateral line systems by a monoclonal antibody.

This study reports that zn-1, a monoclonal antibody, labels hair cells but not supporting cells in the inner ear and the lateral line of the axolotl salamander, Ambystoma mexicanum. Zn-1 immunocytochemically labels the cytoplasm and stereocilia of mature hair cells in the sacculus, in the utriculus, and in the mechanoreceptive neuromast organs of the lateral line. Lower levels of labeling mark newly formed hair cells in the periphery of the sacculus and in regenerating neuromasts. Zn-1 also selectively labels neuronal processes and perikarya in the lateral line nerves and ganglia and the VIIIth cranial nerve and ganglion. Processes and perikarya are labeled by zn-1 in the dorsolateral medulla oblongata, at sites of termination of the afferent octaval and lateral line neurons. Western blot analysis revealed that zn-1 labels one or more proteins with molecular weights of 80 and 160 kDa. The identity of these protein bands remains to be determined. The presence of a specific epitope expressed in both hair cells and neurons, but not in supporting cells, in the vestibular and auditory epithelia of the ear and in the mechanoreceptive neuromasts of the lateral line suggests shared cytogenetic heritages. These findings are consistent with a close evolutionary relationship between otic and lateral line senses, such as that inherent to the theoretical evolutionary scheme outlined in van Bergeijk's "acousticolateralis hypothesis." The protein recognized by zn-1 is as yet unidentified, but its conservative evolution suggests that it may serve an important function in the statoacoustic and lateral line systems.

Afferent Pathways↗

Analysis of surface wave direction by the lateral line system of Xenopus: source localization before and after inactivation of different parts of the lateral line.

The turning responses of clawed toads (Xenopus laevis) to surface waves were examined in animals with an intact lateral line or with different combinations of lateral lines reversibly inactivated by CoCl2. The responses were characterized with respect to response frequency, turning accuracy, turning side, response time, and swim distance. After the inactivation most animals still responded to surface waves but the responses were different from those of animals with an intact lateral line. They also differed according to the combination of inactivated lines. In all experiments the responses for stimuli in some sectors of the surface did not differ from controls. The location of these sectors co-varied with the position of the intact lines, i.e., normal responses were found for frontal stimulus directions when head lines were intact and for caudolateral stimulus directions when trunk lines were intact. Their size was larger when lines on both sides of the body were intact and smaller when only lines on one side were intact. When the number of functional lines was reduced to one or two on one side of the body the turning angles shown within the sector of normal responses were maintained for stimulus directions outside these sectors. These results can be interpreted as indicating that head and trunk lines represent different "position values". When only a single line was functional the toads still turned towards the stimulus source more often than by chance. It is hypothesized that Xenopus uses two mechanisms to determine the direction of surface waves. One uses the position values of head and trunk lines; this mechanism is comparable to the "place value" postulated for individual head neuromasts of surface feeding fish. The other uses the information encoded in the activity pattern that is elicited in one line when the surface wave travels over the line. This second mechanism yields information about stimulus side but not about stimulus angle.

Animals↗

A Xenopus c-kit-related receptor tyrosine kinase expressed in migrating stem cells of the lateral line system.

The mammalian c-kit receptor tyrosine kinase gene is required during embryogenesis for the survival and/or proliferation of three migrating stem cell populations: primordial germ cells, haematopoietic stem cells and neural crest-derived melanoblasts. We have cloned a Xenopus gene, XKrk1, whose closest relative is c-kit. Differences in the expression pattern suggest that XKrk1 is not the Xenopus homologue of c-kit; however, it is expressed in a migrating stem cell population, the precursor cells for the mechanosensory lateral line system. XKrk1 is the first reported marker for lateral line stem cells.

Amino Acid Sequence↗

Form and function relationships in lateral line systems: comparative data from six species of Antarctic notothenioid fish.

The structure and physiology of the anterior lateral line canal systems were studied in six species of fish belonging to two different families within the suborder of antarctic fish Notothenioidei. Many of the canals within the species belonging to the genus Trematomus are relatively straight sided tubes with diameters around 0.4 mm. Some of the canals in Trematomus, and most of the canals in the icefishes (family Channichthyidae) are more complex. Relatively small pores lead into large tubules, the walls of which appear partially membranous, and the canals not much more than constrictions between adjacent tubules. Dissostichus mawsoni, a large species, has canals with distinctive wide and narrow sections, 1.8 mm and 0.48 mm, respectively. Despite these morphological differences the frequency response characteristics of anterior lateral line units are remarkably similar in all six species. In the case of D. mawsoni, this functional similarity results from narrow sections of the canals, which provide the viscous resistance to flow that preserves the mechanical filtering properties of the canal despite the huge size difference between D. mawsoni and the other species. It is argued that the most appropriate way to view canals is as high pass filters which attenuate lower frequencies, and that this effect is best illustrated by comparing the frequency response characteristics of superficial and canal neuromasts using a sinusoidal stimulus that has a constant peak-to-peak velocity. The functional contribution of canals is to attenuate low frequencies and improve the signal-to-noise ratio for biologically important signals in the presence of low frequency noise produced, for example, by the animal's own movements.

Animals↗