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Second-order projection from the posterior lateral line in the early zebrafish brain.

BACKGROUND: Mechanosensory information gathered by hair cells of the fish lateral-line system is collected by sensory neurons and sent to the ipsilateral hindbrain. The information is then conveyed to other brain structures through a second-order projection. In the adult, part of the second-order projection extends to the contralateral hindbrain, while another part connects to a midbrain structure, the torus semicircularis. RESULTS: In this paper we examine the second-order projection from the posterior lateral-line system in late embryonic/early larval zebrafish. At four days after fertilization the synaptic field of the sensory neurons can be accurately targeted, allowing a very reproducible labeling of second-order neurons. We show that second-order projections are highly stereotyped, that they vary according to rhombomeric identity, and that they are almost completely lateralized. We also show that the projections extend not only to the contralateral hindbrain and torus semicircularis but to many other brain centers as well, including gaze- and posture-controlling nuclei in the midbrain, and presumptive thalamic nuclei. CONCLUSION: We propose that the extensive connectivity observed in early brain development reveals a basic scaffold common to most vertebrates, from which different subsets are later reinforced in various vertebrate groups. The large repertoire of projection targets provides a promising system to study the genetic encoding of this differential projection capacity.

Afferent Pathways↗

Lateral line, nervous system, and maternal expression of Frizzled 7a during zebrafish embryogenesis.

We have isolated and mapped a new wnt receptor frizzled family member, zebrafish frizzled 7a. Fz7a and a previously reported zebrafish fz7 (El-Messaoudi and Renucci, 2001) make an orthologous gene pair, however, they display distinct expression patterns. Fz7a shows strong maternal as well as zygotic expression. Fz7a transcript is enriched dorsally starting with the shield stage. At the end of gastrulation, Fz7a is abundantly expressed within anterior neuroectoderm and expressed more weakly within lateral mesoderm. Fz7a is detected during somitogenesis within the central nervous system, somatic and posterior lateral mesoderm. At 24hpf, fz7a is expressed in migrating lateral line primordium. At 48hpf, fz7a is detected in the ear, pectoral fin bud, and within neuromasts, which had originated from the lateral line primordium. Radiation hybrid mapping using panel LN54 (Hukriede et al., 1999) places fz7a on linkage group 6, linked to the marker fi11h08 (distance 0.00cR, LOD score 14.1). To prove that fz7 and fz7a are indeed different genes we mapped fz7 as well using the same LN54 panel. Fz7 mapped to linkage group 9 with a LOD of 12.5, 27.31 cR from wnt 10a in between markers IBD2759 and fb50e04.

Amino Acid Sequence↗

Evolution of gnathostome lateral line ontogenies.

An outgroup analysis of multiple ontogenies provides the most robust approach to understanding phylogeny. Such an analysis of the lateral line system among extinct and extant gnathostomes reveals that lateral line placodes constitute the basic ontogenetic unit responsible for the development of this system. Six pairs of lateral line placodes appear to have existed in the earliest gnathostomes, and eight stages (stages A-H) can be recognized in their differentiation. Terminal truncation (heterochronic changes) in the primitive sequence of placodal development has occurred in one or more placodes in each gnathostome radiation, with the most extensive truncations occurring in arthrodire placoderms, lepidosirenid lungfishes and extant amphibians. The most extensive nonterminal changes in the primitive sequence of placodal development involve the failure of electroreceptors to form within the lateral zones of the elongatiang sensory ridges of the placodes. This nonterminal change appears to have occurred independently in ancestral neopterygian bony fishes, in many amphibians and, possibly, in the extinct acanthodians. At least two teleost radiations, osteoglossomorphs and ostariophysines, have re-evolved electroreceptors which may represent additional nonterminal changes in placodal patterning or, possibly, a change in the embryonic source of these receptors.

Animals↗

Segregation of electroreceptive and mechanoreceptive lateral line afferents in the hindbrain of chondrostean fishes.

The anterior lateral line nerve (ALLN) in the chondrostean fishes (sturgeon and paddlefishes) consists of both fibers innervating ampullary electroreceptors and fibers innervating the mechanoreceptive neuromasts of the cephalic lateral line system. The fibers of the posterior lateral line nerve (PLLN) innervate only mechanoreceptive neuromasts on the body trunk. The ALLN enters the medulla via dorsal and ventral roots; the dorsal root projects to the dorsal octavolateralis nucleus (DON), whereas the ventral root and the PLLN project principally to the medial octavolateralis nucleus (MON). Previous studies in elasmobranchs have demonstrated that fibers of the dorsal root of the ALLN convey electrosensory information, and fibers of the ventral root are concerned with mechanoreceptive information. Electrophysiological and neuroanatomical methods are employed in this study in order to determine if there exists a similar segregation of electroreceptive and mechanoreceptive lateral line afferents within the chondrostean medulla. In specimens of shovelnose, Scaphirhynchus platorynchus, and Atlantic sturgeon, Acipenser oxyrhynchus, and paddlefish, Polyodon spathula, evoked potentials recorded from the hindbrain and elicited by electric fields reached maximum amplitude within the DON and decreased in amplitude through the cerebellar crest. Evoked potentials elicited by stimulation of the posterior lateral line nerve achieved maximum amplitude within the MON. Single and multiple unit recordings revealed that units within the DON responded only to electric field stimulation, whereas units recorded in the MON responded only to mechanical stimulation. Horseradish peroxidase implanted beneath isolated patches of ampullae in Polyodon revealed fibers innervating electroreceptors projecting to the DON via the dorsal root of the ALLN. These results demonstrate a segregation of electroreceptive and mechanoreceptive lateral line afferent fibers in the chondrostean hindbrain, similar to that seen in elasmobranchs. This supports the contention that the electrosensory systems of elasmobranchs and chondrosteans are homologous, and are derived from the common ancestor of elasmobranch and actinopterygian fishes.

Animals↗

Signal detection theory, lateral-line excitation patterns and prey capture behaviour of mottled sculpin.

The frequency with which blinded mottled sculpin, Cottus bairdi, oriented towards a dipole current source (50-Hz vibrating sphere) was measured as a function of source distance (2-18 cm) and azimuth (either 0 degrees in front or 90 degrees to the side of the fish). The orienting frequency declined from over 70% to under 50% as source distance increased from 4 to 12 cm for both frontal and lateral sources. When response biases (frequency of responding in the absence of the signal) were taken into account with the performance metric d', threshold distances (distances at which d' fell to 1) for frontal (12.5 cm) and lateral (11.6 cm) sources were 1.35-1.45 times the mean standard length of fish used in this study. At distances less than 8 cm, d' values were considerably higher (i.e. performance was better) for the lateral source, despite the fact that peak stimulus levels at the fish were twice as high for frontal as for lateral sources at any given distance. Performance differences may be related to differences in spatial excitation patterns, in particular the distribution of opposing pressure gradient directions along the lateral-line system, present for lateral sources, but absent for frontal sources. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

The three-sided romance of the lateral line: glia love axons love precursors love glia.

The lateral line system of fish and amphibians is closely related to the inner ear in terms of evolution, morphology and physiology. Several recent papers have shed new light on the postembryonic development of this system, and have revealed an unexpected triangular relationship where migrating sensory precursors guide axons, axons guide glia and glia, in turn, control the formation of sensory organs. They have also revealed the crucial importance of controlled cell migration not only for patterning the system, but also for determining polarity (and therefore directional sensitivity) of the mechanosensory hair cells. The remarkable accessibility of the lateral line system may allow a detailed analysis of cell migration and polarization, and may help us better understand the complex interactions between sensory precursor cells, neurons and glia during development.

Animals↗

[Morphofunctional features of the catfish lateral line analyzer].

The peripheral and central portions of the catfish lateral line system were investigated by conventional light microscopical and electrophysiological methods. N. lat. post. X supplying the neuromasts and the small pit organs of the fish body consists of myelinated nerve fibres with the axonal diameters between 2 and 9 mum. The nerve also contains a number of unmyelinated fibres as well as lateral line nerves in other species. Axon conduction velocities were distributed within a range of 10-15 m/s. All afferents pass through the n. lat post. X to the area acoustico-lateralis of the medulla oblongata. Nucleus medialis is associated with the lateral line system. It consists of n. med. p. dors, and n. med. p. med. The former consists of medium size cell bodies (6-14 mum), which are of an oval or triangle shape. The latter consists of small (4-6 mum) oval cells. N. med. p. dors. and n. med. p. med. are the most distinct at the level caudally to the enter of auditory nerve VIII. Rostrally and caudally the both portions of the n. med. overlap each other. Responses to electrical and mechanical stimulation of the lateral line organs were recorded in the entire area acoustico-lateralis. All the neurons under study were situated at a depth of 400-800 mum in the area nucleus medialis.

Animals↗

Brain and sensory organ morphology in Antarctic eelpouts (Perciformes: Zoarcidae: Lycodinae).

Eelpouts of the family Zoarcidae comprise a monophyletic group of marine fishes with a worldwide distribution. Centers of high zoarcid diversity occur in the North Atlantic and North Pacific, with important radiations into the Arctic, along southern South America, and into the Southern Ocean around Antarctica. Along with snailfishes (Liparidae), zoarcids form an important component of the non-notothenioid fauna in the subzero shelf waters of Antarctica. We document the anatomy and histology of the brains, cranial nerves, olfactory apparatus, cephalic lateral lines, taste buds, and retinas of three Antarctic zoarcid species, living at depths of 310-939 m, representing three of the nine genera from this region. The primary emphasis is on Ophthalmolycus amberensis, and we provide a detailed drawing of the brain and cranial nerves of this species. Although this brain reflects general perciform neural morphology, it exhibits a reduction of the (optic) tecta and the eminentia granulares and crista cerebellares of the lateral line system. Interspecific differences among the three species are slight. The olfactory rosette consists of three to four lamellae and the nasal sac, contrary to the claim of Fanta et al. ([2001] Antarct Rec, Natl Inst Polar Res, Tokyo 45:27-42), is not in communication with the cephalic lateral line system. Primary olfactory neurons are abundant and converge on branches of the olfactory nerve. Numerous taste buds are located in the lips. All three species lack an ocular choroid rete and have relatively thin retinas with a low cell density and a single bank of rods as the only type of photoreceptor. Neural diversification among Antarctic zoarcids has not involved the evolution of sensory specialists; brain and sensory organ morphologies do not approach the condition seen in primary deep-sea fishes, or even that of some sympatric non-perciform secondary deep-sea fishes, including liparids and muraenolepidids (eel cods). There may be phylogenetic constraints on brain morphology in perciforms such that we do not see extreme specialization in sensory and neural systems for deep habitats. We suggest that the brains and sensory organs of Antarctic zoarcids reflect habitation of 500-2,000-m depths and likely reflect morphologies seen in zoarcids living on continental slopes elsewhere in the world. This balance among the sensory modalities makes zoarcids relatively generalized among secondary deep-sea fishes and may be one of the reasons this opportunistic and adaptable group has been successful in colonizing a variety of emergent and ephemeral habitats.

Animals↗

Diversification of brain and sense organ morphology in Antarctic dragonfishes (Perciformes: Notothenioidei: Bathydraconidae).

In the subzero shelf waters of Antarctica, fishes of the perciform suborder Notothenioidei dominate the fish fauna and constitute an adaptive radiation and a species flock. The 16 species of dragonfishes of the family Bathydraconidae live from surface waters to nearly 3,000 m and have the greatest overall depth range among notothenioid families. We examined the anatomy and histology of the brain, retina, and cephalic lateral line system of nine bathydraconid species representing 8 of the 11 known genera. We evaluate these data against a cladogram identifying three clades in the family. We provide a detailed drawing of the brain and cranial nerves of Gymnodraco acuticeps and Akarotaxis nudiceps. Bathydraconid brain morphology falls into two categories. Brains of most species are similar to those of generalized perciforms and some basal notothenioids (Class I). However, brains of deep-living bathydraconids (members of the tribe Bathydraconini minus Prionodraco) have a reduced telencephalon and tectum that renders the neural axis visible - the stalked brain morphology (Class II). All bathydraconids have duplex (rod and cone) retinae but there is considerable interspecific variation in the ratio of cones:rods and in the number of cells in the internal nuclear layer. Retinal histology reflects habitat depth but is not tightly coupled to phylogeny. Although the deep-living species of Bathydraconini have rod-dominated retinae, the retinae of some sister species are photopic. An expanded cephalic lateral line system is also characteristic of all members of the Bathydraconini as exemplified by Akarotaxis. This morphology includes large lateral line pores, wide membranous canals, hypertrophied canal neuromasts, and large anterodorsal lateral line nerves, eminentia granulares, and crista cerebellares. The saccular otoliths are also enlarged in members of this tribe. Neural diversification among bathydraconids on the Antarctic shelf has not involved the evolution of sensory specialists. Brain and sense organ morphologies do not approach the specialized condition seen in primary deep-sea fishes or even that of some secondary deep-sea fishes including sympatric non-notothenioids such as liparids (snailfishes) and muraenolepidids (eel cods). The brains and sense organs of bathydraconids, including the deep-living species, reflect their heritage as perciform shorefishes.

Anatomy, Comparative↗

Moringua edwardsi (Moringuidae: Anguilliformes): cranial specialization for head-first burrowing?

The order Anguilliformes forms a natural group of eel-like species. Moringua edwardsi (Moringuidae) is of special interest because of its peculiar fossorial lifestyle: this species burrows head-first. Externally pronounced morphological specializations for a fossorial lifestyle include: reduced eyes, lack of color, low or absent paired vertical fins, elongated, cylindrical body, reduced head pores of the lateral line system, etc. Many fossorial amphibians, reptiles, and even mammals have evolved similar external specializations related to burrowing. The present study focuses on osteological and myological features of M. edwardsi in order to evaluate the structural modifications that may have evolved as adaptations to burrowing. Convergent evolutionary structures and possible relations with head-first burrowing, miniaturization, feeding habits, etc., were investigated. Body elongation, reduction of the eyes, modified cranial lateral line system, and modified skull shape (pointed though firm) can be considered specializations for head-first burrowing. Hyperossification can probably be regarded more as a specialization to both head-first burrowing and feeding, even though an impact of miniaturization cannot be excluded. Hypertrophied adductor mandibulae muscles and the enlarged coronoid process can be associated with both feeding requirements (it enhances bite forces necessary for their predatory behavior) and with a burrowing lifestyle, as well as miniaturization.

Adaptation, Biological↗

The role of the lateral line and vision on body kinematics and hydrodynamic preference of rainbow trout in turbulent flow.

The ability to detect water flow using the hair cells of the lateral line system is a unique feature found in anamniotic aquatic vertebrates. Fishes use their lateral line to locate prey, escape from predators and form cohesive schooling patterns. Despite the prevalence of complex flows in nature, almost nothing is known about the function of the lateral line and its relationship to other sensory modalities for freely swimming fishes in turbulent flows. Past studies indicate that under certain conditions the lateral line is not needed to swim steadily in uniform flow. This paper examines how the lateral line and vision affect body kinematics and hydrodynamic habitat selection of rainbow trout (Oncorhynchus mykiss) exposed to vortices generated behind a cylinder. Trout Kármán gaiting (i.e. exploiting vortices to hold station in a vortex street) with a pharmacologically blocked lateral line display altered kinematics; body wavelength and wave speed increase compared to control animals. When visual cues are withheld by performing experiments in the dark, almost all Kármán gait kinematics measured for fish with and without a functional lateral line are the same. The lateral line, rather than vision, plays a larger role in affecting body kinematics when trout hold station in a vortex street. Trout show a preference to Kármán gait in the light but not in the dark, which may be attributed to physiological state rather than hydrodynamic or sensorimotor reasons. In the dark, trout both with and without a functional lateral line hold station near the downstream suction region of the cylinder wake (i.e. entraining) and avoid the vortex street. Vision therefore plays a larger role in the preference to associate with a turbulent vortex street. Trout in the light with a blocked lateral line show individual variation in their preference to Kármán gait or entrain. In the dark, entraining trout with an intact lateral line will alternate between right and left sides of the cylinder throughout the experiment, showing an ability to explore their environment. By contrast, when the lateral line is blocked these fish display a strong fidelity to one side of the cylinder and are not inclined to explore other regions of the flow tank. Both entraining and Kármán gaiting probably represent energetically favorable strategies for holding station relative to the earth frame of reference in fast flows. The ability to decipher how organisms collect and process sensory input from their environment has great potential in revealing the mechanistic basis of how locomotor behaviors are produced as well as how habitat selection is modulated.

Animals↗

Distribution and innervation of lateral line organs in the channel catfish.

The lateral line system of the channel catfish is formed by mechanoreceptive neuromasts located within five pairs of cephalic and one pair of trunk canals, as well as superficial lines of neuromasts, termed accessory and/or pit lines. Five pairs of pit lines occur on the head, and three pairs of superficial lines occur on the trunk. In addition to these mechanoreceptors, which are found in most teleost fishes, catfish also possess a total of over 4000 electroreceptive ampullary organs scattered over the entire body. The lateral line receptors are innervated by five pairs of lateral line nerves whose rami are secondarily associated with facial and trigeminal fibers that innervate taste buds and the dermis of the skin, respectively. The neuromasts of the trunk canal and the ramules of the posterior lateral line nerve that innervate them seem to be organized in a segmental pattern. The same is true for the intervertebral ramules of the recurrent facial ramus, which innervate the external taste buds on the trunk. The fibers of the gustatory and lateral line systems may use the neural crest, the developing spinal nerves, or both, to establish this segmental pattern. In this context, it may not be surprising that there is an intimate relationship among each of the sensory systems in the trunk.

Animals↗

Organisation of lateral line and auditory areas in the midbrain of Xenopus laevis.

Lateral line areas in the midbrain of Xenopus laevis were identified by recording evoked potentials and neural activity elicited by stimulating anterior and posterior lateral line nerves. Spike activity was found in the lateral half of the optic tectum, ventrolateral tectum, and torus semicircularis. Contra- and ipsilateral lateral line pathways to these regions were identified. Spike discharge was associated with an evoked potential (EP) consisting of a large negative-positive wave sometimes preceded by a small positive-negative deflection. EP depth profiles varied according to electrode position within the lateral line midbrain projection field. In the middle of the field a dramatic increase in EP growth occurred as the electrode passed through the torus semicircularis, with peak amplitudes being achieved 900-1,100 micron from the surface within nucleus principalis and magnocellularis. Tracks at the lateral edge of the field showed a steady growth of EP, with peak amplitudes around 600 micron as the electrode passed through ventrolateral tectum. Auditory responses to tone pips were found in the nucleus laminaris and principalis in caudomedial regions of the torus semicircularis, in areas lying medial to the main centers of lateral line evoked activity; this is a similar organisation to that found in teleost fish. The results indicate the torus semicircularis and deep layers of the lateral tectum to be involved in lateral line processing Some topographic separation of the representation of anterior and posterior lateral line systems is indicated. The possible involvement of these areas in lateral line stimulus localisation is discussed.

Animals↗

Peripheral distribution and central projections of the lateral-line nerves in goldfish, Carassius auratus.

The lateral-line system of the goldfish, Carassius auratus, is described from the receptor distribution on the body surface to the termination of the primary afferents within the octavolateralis column. Goldfish have a continuous lateral-line canal system which consists of supraorbital, infraorbital, operculomandibular and supratemporal commissural canals on the head and a trunk canal extending the length of the trunk. There is a single neuromast between each 2 canal pores. The total number of canal neuromasts on the head ranges from 74 to 100. On the body the total number of canal neuromasts ranges from 52 to 60. Associated with each canal are populations of superficial neuromasts. There are approximately 1,000 superficial neuromasts on the head which are arranged in clusters or rows oriented perpendicular to the long axis of the associated canal. On the body there are 3-9 superficial neuromasts on each scale. Further, there is a total of 1,000 superficial neuromasts arranged in horizontal lines between the fin rays of the caudal fin. The neuromasts are innervated by branches of four lateral-line nerves. The dorsal anterior lateral-line nerve innervates the supraorbital and infraorbital canals and associated superficial neuromasts. The ventral anterior lateral-line nerve innervates the operculomandibular canal and associated superficial neuromasts, as well as superficial neuromasts on the operculum. The middle lateral-line nerve innervates the postotic canal and a cluster of associated superficial neuromasts. The posterior lateral-line nerve innervates the supratemporal commissural canal and associated superficial neuromasts, as well as the canal and superficial neuromasts on the trunk and caudal fin. Application of horseradish peroxidase to the individual branches of the lateral-line nerves shows that the posterior lateral-line nerve projects to the dorsal portion of the medial and caudal nuclei, whereas the anterior lateral-line branches project to the ventral portion. Lateral-line projections to the magnocellular and descending nuclei of the octaval column were also observed. The projections to the eminentia granularis are also segregated such that the anterior lateral-line nerves project to the anterolateral portion and the posterior lateral-line nerve to the caudal portion. Thus, there appears to be a topographic organization of the lateral-line projections to the lateralis column and eminentia granularis. However, this topography does not appear to be precise as the projections of the branches of the anterior lateral-line nerves overlap extensively, as do the branches of the posterior lateral-line nerves.

Afferent Pathways↗

Nerve dependency of developing and mature sensory receptor cells.

Old and recent data concerning development of sensory cells and trophic interdependency of sensory neurons and sensory cells is reviewed for the ear, the lateral line system, the electroreceptive system, and the taste system. All sensory neurons originate from placodes. However, only most ear, lateral line and electrosensory cells derive from placodes, while the taste sensory cell originate locally. All sensory cells apparently are nerve independent for their formation, and at least sensory cells in the ear and the taste system share the neurotrophic support for their specific sensory neurons. Later, most of these sensory cells appear to depend, to a variable degree, on some innervation for maintenance. While the molecular nature of the signal cascade from sensory cells to sensory neurons is known in at least two systems, nothing is known about the molecular nature of the signal cascade from the sensory neurons back to the sensory cells.

Animals↗