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Duplicate zebrafish pth genes are expressed along the lateral line and in the central nervous system during embryogenesis.

PTH plays a critical role in calcium metabolism in tetrapods. The primary site of PTH expression is the parathyroid glands, although it is also detected in the thymus and hypothalamus. Fish lack anatomically distinct parathyroid glands, and the first animals to evolve parathyroid glands were the amphibians. However, fish do have PTH family ligands and receptors, which are functionally similar to their mammalian counterparts. We report the expression patterns of duplicate zebrafish pth genes during embryogenesis. Both zebrafish pth1 and pth2 transcripts are expressed along the lateral line before the migration of the lateral line primordium and later in development Pth protein is detected in lateral line neuromasts by immunohistochemistry. pth1 transcripts are also detected in the central nervous system in the ventral neural tube. These temporally and anatomically restricted expression patterns imply a novel role for PTH family hormones during embryonic development of the zebrafish and allow for the genetic dissection of PTH function in this model organism.

Afferent Pathways↗

Posterior lateral line afferent and efferent pathways within the central nervous system of the goldfish with special reference to the Mauthner cell.

The goldfish posterior lateral line nerve consists of a dorsal and a ventral branch, each of which is associated with a ramus of the sensory branch of the VIIth nerve (ramus recurrens facialis). The afferent and efferent pathways of these nerves within the central nervous system were studied by using horseradish peroxidase (HRP) histochemistry. The afferent fibers of the ramus recurrens facialis travel in the ventral portion of the VIIth nerve as it enters the brain and project predominantly to the ipsilateral half of the facial lobe. The afferent fibers of either the dorsal or ventral branch of the posterior lateral line nerve split into two bundles as they enter the brain. The caudally projecting fascicle terminates predominantly in the nucleus medialis. The fibers of the rostrally projecting bundle terminate predominantly in nucleus medialis and nucleus magnocellularis and in the eminentia granularis. The posterior lateral line efferent somata were located in the diencephalon as well as in the medulla oblongata. The medullary efferent neurons formed two distinct groups, a rostral and a caudal nucleus. The cell bodies of the latter were more numerous and larger than those of the former. The axons of the efferent neurons exit from the brain by one of two routes. The first is at the level of the rostral efferent nucleus and the second at the level of the Mauthner cell. Previous reports have described input of posterior lateral line afferent fibers to the Mauthner cell soma and proximal lateral dendrite of the goldfish. This electrophysiological input was bilateral and was interpreted as monosynaptic. The afferent input described in this study was ipsilateral and ended in the vicinity of the distal lateral dendrite. These differences are discussed in the context of the neuronal circuitry that may be present.

Animals↗

Genome size, secondary simplification, and the evolution of the brain in salamanders.

Compared to other vertebrates, even including lampreys and hagfishes in some respects, salamanders exhibit a relatively simple organization of brain and sense organs which is illustrated here using the visual system as an example. The greatest simplicity is found in the bolitoglossine salamanders, yet all bolitoglossines possess highly projectile tongues and rely on vision for survival; furthermore, some species are agile and acrobatic. The unusual features of the visual system of salamanders include small numbers of large neurons, a low degree of morphological differentiation among neurons, a small proportion of myelinated axons in the optic nerve, and an optic tectum consisting essentially of a periventricular cellular layer and a superficial fiber layer. Similar features are found throughout the central nervous system of salamanders and in the lateral line, auditory and olfactory systems as well. Phylogenetic analysis shows that the most parsimonious interpretation of these data is that the simple organization of the brain and sense organs of salamanders was derived secondarily from a more complex ancestral state. We hypothesize that increased genome size has led to simplification of the nervous system in salamanders. Increased genome size appears to have had profound effects on neural development in salamanders, leading to paedomorphosis, the retention of juvenile or even embryonic characteristics into adulthood. In particular, large genome size is associated with large cell size and reduced rates of cell proliferation, migration and differentiation. Secondary simplification has constrained the function of the salamanders' visual system, primarily by increasing cell size and decreasing cell numbers. However, it also has provided an opportunity for the evolution of compensating mechanisms, which have helped to restore or even enhance visual function. Most apparent among the compensatory mechanisms of bolitoglossine salamanders is the presence of well developed ipsilateral retinotectal projections, which apparently enhance depth perception. It is difficult to explain the unusual history of the nervous system in salamanders solely in terms of natural selection and adaptation. Increasing genome size through selfish replication appears to have played a major role in the evolution of salamander brains by imposing functional constraints as well as creating opportunities for overcoming them.

Animals↗

Laminar organization of the afferent and efferent systems of the torus semicircularis of gymnotiform fish: morphological substrates for parallel processing in the electrosensory system.

The torus semicircularis of Gymnotiform fish is an enlarged laminated midbrain structure which receives lemniscal input from electrosensory, mechanoreceptive lateral line, and auditory systems. The electrosensory input in confined to the dorsal torus, while the auditory and mechanoreceptive systems project to the ventral torus. Anterograde and retrograde techniques were used were used to determine the connections of the dorsal torus in Apteronotus and Eigenmannia. The dorsal torus can be divided into nine major laminae, each of which has distinct afferent and efferent connections. The dorsal torus receives five afferent inputs: (1) A contralateral topographic input from the posterior lateral line lobe (PLLL) projects to laminae III, V, VI, VII, VIIIB, and VIIID. (2) Eurydendroid cells of the caudal lobe of the cerebellum project contralaterally to lamina VIIIB. (3) A portion of the descending nucleus of V projects to laminae VIIIA, VIIIC, and IX. (4) Lamina I is a cap of fine myelinated fibers which may originate in the torus longitudinalis. They project to laminae II and III. (5) The ipsilateral optic tectum projects to the dorsal torus. The dorsal torus projects to six major targets: (1) Laminae VII, VIII, and IX project bilaterally to a lateral region of the diencephalon above n. preglomerulosus, herein named n. electrosensorius. An area below the dorsal thalamus receives a smaller ipsilateral projection. (2) Laminae II, V, VIvn, VII, VIII, and IX project topographically to the deeper laminae of the ipsilateral optic tectum. This projection is in spatial register with the visual map in the superficial layers of the tectum. (3) Lamina VIIID projects ipsilaterally to the lateral reticular formation. (4) All laminae other than I, VI, and VIIIB project topographically to ahe ipsilateral n. praeeminentialis, which provides a powerful descending projection to the PLLL. (5) Lamina IX projects to a dorsal pretectal area. (6) The ipsilateral inferior olive receives a projection from the dorsal torus.

Afferent Pathways↗

Calcium-binding sites on sensory processes in vertebrate hair cells.

Vertebrate lateral line and vestibular systems center their function on highly mechanosensitive hair cells. Each hair cell is equipped with one kinocilium (which resembles a motile cilium) and 50-100 actin-containing stereocilia (which resemble microvilli) at the site of stimulus reception. This report describes electron-microscopic localization of calcium-binding sites on the sensory processes of vertebrate hair cells. Using the Oschman-Wall technique for calcium localization [Oschman, J. L. & Wall, B. J. (1972) J. Cell Biol. 55, 58-73] together with electron-probe x-ray microanalysis of thin sections, we observed: (i) calcium- and iron-containing deposits in the region of the ciliary necklace in goldfish lateral line hair cells, (ii) calcium deposits upon the surface of stereocilia of hair cells of the bullfrog inner ear, and (iii) calcium deposits upon stereocilia of hair cells of the guinea pig vestibular system.

Animals↗

Removal of eyes in early larval stages alters the response of the clawed toad, Xenopus laevis, to surface waves.

The clawed toad, Xenopus laevis, responds to surface waves with a very accurate orienting reaction towards the source of the wave. The importance of visual experience during larval development for this orienting reaction guided by the lateral line was investigated by testing the responses in postmetamorphic animals deprived of vision from an early larval stage by enucleation or rearing in darkness. Control animals were enucleated after metamorphosis. The results show that the orienting response in animals enucleated as larvae is less accurate; the slope of the regression of the turning angle on stimulus angle is only 0.58, compared to 0.82 for the control animals. It is hypothesized that the likely location for the interaction between the visual system and the lateral line is the tectum opticum.

Animals↗

Compression and lateral shift of mental coordinate systems in a line bisection task.

Subjects (N = 18) were required to imagine how far lines of three different lengths which were presented to them previously would extend to the left or to the right of a vertical mark. They were asked to indicate the midpoint of the imagined line length. The frequency of deviations to the left or to the right of the geometrical midpoint of the line which had to be visualized was dependent on the length of the line and on the direction towards which the subjects imagined the line to extend. Whereas a compression of imagined half space compared to geometric half space was observed both for the left and right side, imagined half space on the right side of the visual field was shifted in addition more towards the periphery. It is suggested that the latter result is related to properties of left hemisphere functioning which could explain the occurrence of a typical symptom of unilateral neglect after a right hemisphere lesion.

Adult↗

Peripheral control of acoustic signals in the auditory system of echolocating bats.

Many species of echolocating bats emit intense orientation sounds. If such intense sounds directly stimulated their ears, detection of faint echoes would be impaired. Therefore, possible mechanisms for the attenuation of self-stimulation were studied with Myotis lucifugus. The acoustic middle-ear-muscle reflex could perfectly and transiently regulate the amplitude of an incoming signal only at its beginning. However, its shortest latency in terms of electromyograms and of the attenuation of the cochlear microphonic was 3-4 and 4-8 msec, respectively, so that these muscles failed to attenuate orientation signals by the reflex. The muscles, however, received a message from the vocalization system when the bat vocalized, and contracted synchronously with vocalization. The duration of the contraction-relaxation was so short that the self-stimulation was attenuated, but the echoes were not. The tetanus-fusion frequency of tha stapedium muscle ranged between 260 and 320/sec. Unlike the efferent fibres in the lateral-line and vestibular systems, the olivo-cochlear bundle showed no sign of attenuation of self-stimulation.

Acoustic Stimulation↗

The electroreceptive ampullary organs of urodeles.

The system of lateral-line organs in urodeles was examined by the use of various light- and electron-microscopical techniques. The results show that, in addition to the well-known mechanoreceptive neuromast organs, a second type of receptor can be identified. This second type of organ was presumably seen by earlier workers, but they seemingly failed to point out the distinction between the two organs. The presently described organs are anatomically similar to the ampullary organs of various anamniotic species such as Brachiopterygii, sturgeons, lungfish, and silurids. In all these species the ampullary organs display only one afferent fiber but no efferent innervation and are situated around an ampullary enlargement in or below the epidermis as in urodeles. All ampullary receptors including those of urodeles are very sensitive to weak electrical fields. Similar to the situation in teleosts, the ampullae of urodeles show numerous microvilli but no kinocilia. All other nonteleostean ampullary receptors appear to possess only kinocilia as apical specializations but no microvilli. Current evidence suggests that the electroreceptive ampullary organs are as phylogenetically old as all other vertebrate sensory systems; they are now known to be relatively common among anamniotic vertebrates. Since all ampullary receptors share many common characteristics, it is assumed that they were derived from one phylogenetic precursor but have evolved certain peculiarities in each species not shared by other ampullary receptors.

Animals↗

Paedomorphosis and simplification in the nervous system of salamanders.

Comparative neuroanatomists since Herrick [1914] have been aware of the paradox that the brain of amphibians, especially salamanders, is less complex than one would expect based on their phylogenetic position among the Tetrapoda. Many features of the brain are less differentiated in salamanders than in tetrapod outgroups, including chondrichthyans and bony fishes, and for some brain characters, the salamander brain is even more simple than that of the agnathans. Here, we perform a cladistic analysis on 23 characters of four sensory systems (visual, auditory, lateral line and olfactory) and the brain. Our taxa include myxinoids, lampreys, chondrichthyans, actinopterygians, Latimeria, Neoceratodus and the lepidosirenid lungfishes, amniotes, frogs, caecilians, salamanders and bolitoglossine salamanders. Of the 23 characters we examined, 19 are most parsimoniously interpreted as secondarily simplified in salamanders from a more complex ancestral state, two characters are equally parsimonious under both hypotheses, one character (well developed ipsilateral retinotectal projections) is more complex in bolitoglossine salamanders than in vertebrates generally, and only one character (migration of neurons in the medial pallium) is most parsimoniously interpreted as retention of the plesiomorphically simple condition. Secondary simplification of the salamander brain appears to result from paedomorphosis, or retention of juvenile or embryonic morphology into adulthood. Paedomorphosis is correlated with an increase in genome size, which in turn is positively correlated with cell size, but negatively correlated with cell proliferation and differentiation rates. Available data suggest that, although increasing genome size and paedomorphosis tend to compromise the function of the salamander brain, compensating mechanisms have evolved that may restore or even enhance brain function.

Animals↗

Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe.

The electrosensory lateral line lobe (ELLL) of weakly electric fish, the primary electrosensory processing station, receives a large descending input from the midbrain in addition to the input from the electroreceptor afferents. The role of a major component of this descending input in determining the properties of ELLL output neurons was investigated. The descending input was reduced or eliminated by microinjections of the local anesthetic lidocaine or by small lesions. This treatment increased the responses of the ELLL output neurons to suprathreshold stimuli by about 300% and also increased the size of the neurons' receptive fields for moving electrolocation targets and the resolution with which they encode target distance. The neurons' threshold sensitivity and tuning to amplitude modulation frequency were unchanged by removal of the descending input. The results of this study show that this portion of the descending input to the ELLL normally mediates an inhibition that controls the responsiveness of ELLL output neurons. This descending input could function as a gain control mechanism, allowing the animal to modulate the sensitivity of the electrosensory system in response to changing environmental conditions.

Animals↗

Trk neurotrophin receptor-like proteins in the teleost Dicentrarchus labrax.

In recent years, data have accumulated suggesting that the role of neurotrophins and Trk receptors may not be limited to the nervous system, and the presence of these substances has been detected in a variety of vertebrate and invertebrate non-nervous tissues. This study was designed to map the expression of immunoreactivity (IR) for Trk-like proteins in alevins of the teleost Dicentrarchus labrax, with particular emphasis on non-nervous structures. We used antibodies against specific epitopes of the intracellular domain of these proteins, a region that is highly conserved in phylogeny. Trk-like IR was seen in segregate cell populations of the nervous system, and non-nervous tissues. In the central nervous system TrkA-like and TrkC-like IR was abundant, whereas TrkB-like IR was restricted to a low number of brain areas. Expression of Trk-like protein IR was observed in the peripheral nervous system and sensory organs, with the exception of the lateral line organ. Outside the nervous system, TrkA-like IR was mainly found in different epithelia, TrkB-like IR in the endocrine and digestive system, and TrkC-like IR in the cardiovascular and immune systems. The gills showed IR for all three Trk-like proteins, whereas they were absent from the gonads. Furthermore, scattered cells positive for Trk-like proteins were found in most of the investigated tissues. The distribution of Trk-like IR in this teleost is compared with that of mammals and birds, which it often paralleled, and the possible role of neurotrophins and Trk-like receptor proteins in different non-neuronal tissues is discussed.

Animals↗

The puzzle of hydrodynamic information processing: how are complex water motions analyzed by the lateral line?

We studied the discharges of neurons in the ascending lateral line pathway in response to the complex water motions generated by a moving object. The wave stimulus generated by the object was monitored with a hot-wire anemometer and with a custom-built particle imaging system. Responses of central lateral line neurons differ from those of primary afferent fibers in aspects like temporal discharge patterns and directional sensitivity. The data are consistent with the hypothesis that central lateral line neurons integrate input from many afferents innervating neuromasts distributed across large portions of the body surface.

Animals↗

Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line.

The shape of most complex organ systems arises from the directed migration of cohesive groups of cells. Here, we dissect the role of the chemokine guidance receptor Cxcr4b in regulating the collective migration of one such cohesive tissue, the zebrafish lateral line primordium. Using in vivo imaging, we show that the shape and organization of the primordium is surprisingly labile, and that internal cell movements are uncoordinated in embryos with reduced Cxcr4b signaling. Genetic mosaic experiments reveal that single cxcr4b mutant cells can migrate in a directional manner when placed in wild-type primordia, but that they are specifically excluded from the leading edge. Moreover, a remarkably small number of SDF1a-responsive cells are able to organize an entire cxcr4b mutant primordium to restore migration and organogenesis in the lateral line. These results reveal a role for chemokine signaling in mediating the self-organizing migration of tissues during morphogenesis.

Animals↗

Evolution of posterior lateral line development in fish and amphibians.

The lateral line is a sensory system present in fish and amphibians. It is composed of discrete sense organs, the neuromasts, arranged on the head and body in species-specific patterns. The neuromasts are deposited by migrating primordia that originate from pre- and postotic placodes and follow defined pathways on the head and body. Here we examine the formation of the posterior lateral line (PLL), which extends rostrocaudally on the trunk and tail. In amphibians, the PLL neuromasts are deposited as a single wave from the head to the tip of the tail. In the zebrafish, however, the first wave of neuromast deposition forms but a rudimentary PLL, and several additional waves are needed to form the adult pattern. We show that the amphibian mode is also present in the sturgeon and therefore probably represents the primitive mode, whereas the zebrafish mode is highly conserved in several teleost species. A third mode is found in a subgroup of teleosts, the protacanthopterygians, and may represent a synapomorphy of this group. Altogether, the mode of formation of the embryonic PLL appears to have undergone remarkably few changes during the long history of anamniote evolution, even though large differences can be observed in the lateral line morphology of adult fishes.

Amphibians↗

Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe.

The responses of E-cells, basilar pyramidal cells, of the electrosensory lateral line lobe (ELLL) were studied in normal animals (Apteronotus leptorhynchus) and in fish in which a component of the descending input from the midbrain n. praeeminentialis to the ELLL was interrupted by lesions or by application of local anesthetics. This treatment increased the responsiveness of these neurons by 100 to 300%. A method is described by which the animal's electric organ discharge (EOD) can be increased or decreased in amplitude. Responses of E-cells to a brief stationary electrosensory stimulus and to moving electrolocation targets were studied in normal and in lesioned animals with normal and altered EOD amplitudes. Large reductions in EOD amplitude, approximately 50%, result in no significant changes in the average size of E-cells' responses to either type of electrosensory stimulus in normal animals. Interruption of the descending input, however, results in a loss of the E-cells' ability to maintain constant response size when the EOD amplitude is reduced. Increases in EOD amplitude cause reductions in the size of E-cell responses to the moving electrolocation targets and to the stationary stimulus. The effects of increased EOD amplitude are present in normal animals and in animals in which the descending input is interrupted. The descending input to the ELLL seems to function as a gain control mechanism that is capable of compensating for losses in stimulus strength resulting from reduced EOD amplitude. The component of the descending input studied here does not seem to play a role in the response of the system to increases in EOD amplitude. These results are discussed in conjunction with the known details of the ELLL circuitry and its connections with other brain areas.

Anesthetics, Local↗

Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and of its ligand, SDF1.

Cell migration plays an essential role in many morphogenetic processes, and its deregulation has many dramatic consequences. Yet how migration is controlled during normal development is still a largely unresolved question. We examined this process in the case of the posterior lateral line (PLL), a mechanosensory system present in fish and amphibians. In zebrafish, the embryonic PLL comprises seven to eight sense organs (neuromasts) aligned from head to tail along the flank of the animal and is formed by a primordium that originates from a cephalic placode. This primordium migrates along a stereotyped pathway toward the tip of the tail and deposits in its wake discrete groups of cells, each of which will become a neuromast. We show that a trail of SDF1-like chemokine is present along the pathway of the primordium and that a CXCR4-like chemokine receptor is expressed by the migrating cells. The inactivation of either the ligand or its receptor blocks migration, whereas in mutants in which the normal SDF1 trail is absent, the primordium path is redirected to the next, more ventral sdf1 expression domain. In all cases, the sensory axons remain associated to the primordium, indicating that the extension of the neurites to form the PLL nerve depends on the movement of the primordium. We conclude that both the formation and the innervation of this system depend on the SDF1-CXCR4 system, which has also been implicated in several migration events in humans, including metastasis formation and lymphocyte homing.

Animals↗

The immunocytochemical localization of glutamate in the electrosensory system of the gymnotiform fish, Apteronotus leptorhynchus.

The first processing station of the electrosensory system is the medullary electrosensory lateral line lobe. The electrosensory lateral line lobe of gymnotiform fish is a laminated structure with three anatomically distinct excitatory inputs: primary afferents from electroreceptors, the direct feedback from n. praeminentialis and indirect feedback from n. praeminentialis via a cerebellar lobe--the eminentia granularis posterior. We utilized immunocytochemistry on L-R White-embedded semithin sections, and immunogold on thin sections to localize glutamate and aspartate in the electrosensory lateral line lobe, its afferent inputs and efferent targets. The excitatory inputs and the electrosensory lateral line lobe projection neurons are immunopositive for glutamate only, suggesting that glutamate rather than aspartate is the excitatory transmitter of the electrosensory system.

Animals↗