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Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe.

The first-order CNS processing region within the electrosensory system, the electrosensory lateral line lobe, receives massive descending inputs from the nucleus praeeminentialis as well as the primary afferent projection. The n. praeeminentialis receives its input from the electrosensory lateral line lobe as well as from higher centers; hence this nucleus occupies an important position in a feedback loop within the electrosensory system. This report describes the physiological properties of a category of n. praeeminentialis neurons characterized by very high spontaneous firing frequency, but relatively poor sensitivity to electrolocation targets as compared to neurons in the electrosensory lateral line lobe. These neurons are specialized to encode long-term changes in electric organ discharge amplitude with high resolution. Intracellular recording and Lucifer yellow staining of these neurons show that they are the previously described multipolar neurons of the n. praeeminentialis, and they project bilaterally to the posterior eminentia granularis. Posterior eminentia granularis efferents project to the electrosensory lateral line lobe forming its dorsal molecular layer. Hence, these multipolar cells influence the electrosensory lateral line lobe circuitry indirectly. The information that the multipolar cells encode regarding the electric organ discharge amplitude may be needed for a gain control mechanism operative within the electrosensory lateral line lobe. Previous studies have shown that the indirect projection from the n. praeeminentialis to the electrosensory lateral line lobe must be intact for this gain control mechanism to operate.

Animals↗

Experimental analysis of character coupling across a complex life cycle: pigment pattern metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum.

Developmental relationships among characters are expected to bias patterns of morphological variation at the population level. Studies of character development thus can provide insights into processes of adaptation and the evolutionary diversification of morphologies. Here I use experimental manipulations to test whether larval and adult pigment patterns are coupled across metamorphosis in the tiger salamander, Ambystoma tigrinum tigrinum (Ambystomatidae). Previous investigations showed that the early larval pigment pattern depends on interactions between pigment cells and the lateral line sensory system. In contrast, the results of this study demonstrate that the major features of the adult pigment pattern develop largely independently of both the early larval pattern and the lateral lines. These results suggest that ontogenetic changes that occur across metamorphosis decouple larval and adult pigment patterns and could thereby facilitate independent evolutionary modifications to the patterns during different stages of the life cycle.

Ambystoma↗

Distant touch hydrodynamic imaging with an artificial lateral line.

Nearly all underwater vehicles and surface ships today use sonar and vision for imaging and navigation. However, sonar and vision systems face various limitations, e.g., sonar blind zones, dark or murky environments, etc. Evolved over millions of years, fish use the lateral line, a distributed linear array of flow sensing organs, for underwater hydrodynamic imaging and information extraction. We demonstrate here a proof-of-concept artificial lateral line system. It enables a distant touch hydrodynamic imaging capability to critically augment sonar and vision systems. We show that the artificial lateral line can successfully perform dipole source localization and hydrodynamic wake detection. The development of the artificial lateral line is aimed at fundamentally enhancing human ability to detect, navigate, and survive in the underwater environment.

Animals↗

The laterophysic connection in chaetodontid butterflyfish: morphological variation and speculations on sensory function.

The laterophysic connection is a novel specialization in chaetodontid butterflyfish, in which paired diverticula of the swim-bladder ('horns') extend anteriorly and approach or directly contact a medial fossa in the lateral line canal contained within the supracleithrum. This study examined the morphology of the laterophysic connection in eight ecologically diverse species belonging to five subgenera within Chaetodon. Two types of laterophysic connections, indirect and direct, were found among Chaetodon species. Intraspecific variation (including sexual dimorphism) in the morphology of the laterophysic connection was not found. The type of laterophysic connection is not correlated with ecological characteristics among Chaetodon species, but appears to be correlated with subgeneric affinities of Chaetodon species. The presence of swim-bladder horns probably increases pressure sensitivity to the inner ear. It is suggested that the presence of a direct laterophysic connection, and possibly an indirect laterophysic connection, imparts pressure sensitivity to the lateral line canal system as well.

Air Sacs↗

Homology and evolutionary novelty in the deployment of extracellular matrix molecules during pigment pattern formation in the salamanders Taricha torosa and T. rivularis (Salamandridae).

Salamander larvae exhibit a diverse array of pigment patterns shortly after hatching. Previous studies have identified roles for the extracellular matrix and lateral line sensory system in promoting the development of a phylogenetically common pattern of horizontal melanophore stripes. In contrast, salamanders in the genus Taricha exhibit evolutionarily derived pigment patterns and pattern-forming mechanisms. Taricha torosa larvae exhibit compact melanophore stripes that develop via redundant, lateral line-independent mechanisms, whereas T. rivularis larvae lack stripes and instead have melanophores uniformly distributed over the flank. In this study, I test roles for candidate patterning molecules of the extracellular matrix in promoting the development of species-specific pigment patterns in Taricha. I show that tenascin deposition is negatively correlated with melanophore distributions both intraspecifically and interspecifically: this matrix molecule is present where melanophores do not localize in T. torosa and is absent from these same regions where melanophores are abundant in T. rivularis. Embryological manipulations further indicate that transient expression of tenascin in a prospective interstripe region of T. torosa reflects a phylogenetically conserved effect of lateral line development. Finally, anti-laminin immunoreactivity is negatively correlated with melanophore distributions in T. torosa, and this species exhibits a general retardation of extracellular matrix development that may allow persistent, evolutionarily novel melanophore motility in this species. Together these findings identify tenascin and laminin, or molecules co-regulated with these matrix components, as candidates for promoting early larval pigment pattern development in Taricha.

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Development of the electrosensory nervous system of Eigenmannia (gymnotiformes): II. The electrosensory lateral line lobe, midbrain, and cerebellum.

The somatotopically and functionally organized electrosensory system of gymnotiform teleosts provides a model for the study of the formation of ordered nerve connections. This paper describes the development of the major electrosensory nuclei within the hind- and midbrain. All three main electrosensory nuclei--the electrosensory lateral line lobe (ELL), dorsal torus semicircularis (torus), and tectum--grow by adding cells at their caudolateral borders. Toral and tectal germinal zones arise from lateral ventricular outpocketings that either completely or partially close by maturity. In the ELL before day 5 postspawning, germinal cells form from an initial periventricular germinal zone, then migrate to the caudolateral border of the hindbrain and begin dividing. The ELL grows from two main germinal zones, one for the medial segment, and one for the three lateral tuberous segments. Within each ELL germinal zone, newly formed cells arise from two areas: granular cells arise from a ventral subzone, pyramidal cells are generated more dorsally. Granular cells remain in situ, whereas pyramidal cells may migrate rostromedially. Cells begin differentiating as soon as they are formed. Spherical and pyramidal cells send ascending axons into the internal plexiform layer by day 14-18 and the ELL gradually begins to assume its mature laminar appearance. The ELL grows caudally, preceding the caudal lobe of the cerebellum, which will eventually lie over and fuse with it. Primary electrosensory afferents enter the ELL by day 6; incoming afferents form four fascicles within the ELL, suggesting the formation of separate ELL segments. Unlabelled projections between labelled fields from a single nerve branch filled with HRP on day 7 suggest that somatotopic order is already present at this early age. In the periphery, receptor addition is unordered, occurring along nerve branch pathways. Meanwhile the ELL adds cells in an orderly fashion at its caudolateral border. This suggests that primary afferents shift position caudally with growth to maintain their somatotopic relationships. Because all three central nuclei are in topographic register and grow by adding cells caudally, during growth ELL efferents to the torus and toral efferents to the tectum may utilize passive mechanisms, such as fiber-fiber interactions, to guide axons.

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Role of SDF1 chemokine in the development of lateral line efferent and facial motor neurons.

Most sensory systems are innervated by efferent neurons as well as by afferent neurons. The efferent innervation modulates the sensitivity of the receptor cells or of the sensory terminals. In the posterior lateral line system of the zebrafish, two efferent nuclei have been described in the hindbrain. Here we examine the development of the efferent neurons. We show that their axons are guided toward the target organ along the lateral line nerve while their cell bodies migrate posteriorward across rhombomeres to achieve their final position in rhombomeres 6/7. This migration depends on the SDF1 chemokine. We show that the migration of motor neurons of the facial nucleus from rhombomere 4 to 6 is also affected in sdf1a morphants (embryos injected with morpholine-conjugated antisense oligonucleotides). We propose that SDF1/CXCR4-mediated cell migration is preferentially associated with movement along the anteroposterior axis of the animal.

Afferent Pathways↗

Development of the supraorbital and mandibular lateral line canals in the cichlid, Archocentrus nigrofasciatus.

The development of two of the cranial lateral line canals is described in the cichlid, Archocentrus nigrofasciatus. Four stages of canal morphogenesis are defined based on histological analysis of the supraorbital and mandibular canals. "Canal enclosure" and "canal ossification" are defined as two discrete stages in lateral line canal development, which differ in duration, an observation that has interesting implications for the ontogeny of lateral line function. Canal diameter in the vicinity of individual neuromasts begins to increase before ossification of the canal roof in each canal segment; this increase in canal diameter is accompanied by an increase in canal neuromast size. The mandibular canal generally develops later than the supraorbital canal in this species, but in both of these canals development of the different canal segments contained within a single dermal bone is asynchronous. These observations suggest that a dynamic process requiring integration and interaction among different tissues, in both space and time, underlies the development of the cranial lateral line canal system. The supraorbital and mandibular canals appear to demonstrate a "one-component" pattern of development in Archocentrus nigrofasciatus, where the walls of each canal segment grow up from the underlying dermal bone and then fuse to form the bony canal roof. This is contrary to numerous published reports that describe a "two-component" pattern of development in teleosts where the bony canal ossifies separately and then fuses with an underlying dermal bone. A survey of the literature in which lateral line canal development is described using histological analysis suggests that the occurrence of two different patterns of canal morphogenesis ("one-component" and "two-component") may be due to phylogenetic variation in the pattern of the development of the lateral line canals.

Animals↗

The zebrafish dog-eared mutation disrupts eya1, a gene required for cell survival and differentiation in the inner ear and lateral line.

To understand the molecular basis of sensory organ development and disease, we have cloned and characterized the zebrafish mutation dog-eared (dog) that is defective in formation of the inner ear and lateral line sensory systems. The dog locus encodes the eyes absent-1 (eya1) gene and single point mutations were found in three independent dog alleles, each prematurely truncating the expressed protein within the Eya domain. Moreover, morpholino-mediated knockdown of eya1 gene function phenocopies the dog-eared mutation. In zebrafish, the eya1 gene is widely expressed in placode-derived sensory organs during embryogenesis but Eya1 function appears to be primarily required for survival of sensory hair cells in the developing ear and lateral line neuromasts. Increased levels of apoptosis occur in the migrating primordia of the posterior lateral line in dog embryos and as well as in regions of the developing otocyst that are mainly fated to give rise to sensory cells of the cristae. Importantly, mutation of the EYA1 or EYA4 gene causes hereditary syndromic deafness in humans. Determination of eya gene function during zebrafish organogenesis will facilitate understanding the molecular etiology of human vestibular and hearing disorders.

Animals↗

Disaptation and recovery in the evolution of Antarctic fishes.

The radiation of notothenioid fishes provides an excellent system to explore issues of evolution and adaptation. Most studies emphasize adaptation to the extreme Antarctic environment; however, recent work provides cogent examples of disaptation or evolutionary loss of function. The nature and extent of regressive change is revealed by subsequent adaptive recovery. Ancestral notothenioids were benthic but some became secondarily pelagic through the retention of larval characters. Paedomorphosis has produced detrimental changes in lateral-line sensory systems that have been made good by compensatory adaptation. In the icefish family, compensatory adaptation has followed the loss of the oxygen-binding pigments haemoglobin and myoglobin.

Journal Article↗

Zebrafish as a model for hearing and deafness.

The zebrafish is an especially attractive model for the study of the development and function of the vertebrate inner ear. It combines rapid and accessible embryogenesis with a host of genetic and genomic tools for systematic gene discovery and analysis. A large collection of mutations affecting development and function of the ear and a related sensory system, the lateral line, have been isolated; several of these have now been cloned, and at least five provide models for human deafness disorders. Disruption of multiple genes, using both forward and reverse genetic approaches, has established key players--both signaling molecules and autonomous factors--responsible for induction and specification of the otic placode. Vestibular and auditory defects have been detected in adult animals, making the zebrafish a useful system in which to tackle the genetic causes of late onset deafness and vestibular disease.

Animals↗

Visually mediated inhibition of lateral line primary afferent activity by the octavolateralis efferent system during predation in the free-swimming toadfish, Opsanus tau.

The activity of single lateral line afferent neurons was chronically recorded in free-swimming toadfish. CNS efferent neurons, known to be inhibitory upon peripheral lateral line mechanoreceptors, were activated by stroboscopic and natural visual stimuli. Discharges from irregular-type afferents caused by water movement relative to lateral line neuromasts decreased following stroboscopic stimulation of unrestrained and behaving fish. Visual presentation of natural prey also decreased mechanically evoked afferent firing rates. We show that visual stimuli can activate the efferent system and function in the peripheral processing of mechanical stimuli to the lateral line in biologically relevant contexts.

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Mutations affecting development of the zebrafish inner ear and lateral line.

Mutations giving rise to anatomical defects in the inner ear have been isolated in a large scale screen for mutations causing visible abnormalities in the zebrafish embryo (Haffter, P., Granato, M., Brand, M. et al. (1996) Development 123, 1-36). 58 mutants have been classified as having a primary ear phenotype; these fall into several phenotypic classes, affecting presence or size of the otoliths, size and shape of the otic vesicle and formation of the semicircular canals, and define at least 20 complementation groups. Mutations in seven genes cause loss of one or both otoliths, but do not appear to affect development of other structures within the ear. Mutations in seven genes affect morphology and patterning of the inner ear epithelium, including formation of the semicircular canals and, in some, development of sensory patches (maculae and cristae). Within this class, dog-eared mutants show abnormal development of semicircular canals and lack cristae within the ear, while in van gogh, semicircular canals fail to form altogether, resulting in a tiny otic vesicle containing a single sensory patch. Both these mutants show defects in the expression of homeobox genes within the otic vesicle. In a further class of mutants, ear size is affected while patterning appears to be relatively normal; mutations in three genes cause expansion of the otic vesicle, while in little ears and microtic, the ear is abnormally small, but still contains all five sensory patches, as in the wild type. Many of the ear and otolith mutants show an expected behavioural phenotype: embryos fail to balance correctly, and may swim on their sides, upside down, or in circles. Several mutants with similar balance defects have also been isolated that have no obvious structural ear defect, but that may include mutants with vestibular dysfunction of the inner ear (Granato, M., van Eeden, F. J. M., Schach, U. et al. (1996) Development, 123, 399-413,). Mutations in 19 genes causing primary defects in other structures also show an ear defect. In particular, ear phenotypes are often found in conjunction with defects of neural crest derivatives (pigment cells and/or cartilaginous elements of the jaw). At least one mutant, dog-eared, shows defects in both the ear and another placodally derived sensory system, the lateral line, while hypersensitive mutants have additional trunk lateral line organs.

Animals↗

Lateral line morphology and cranial osteology of the rubynose brotula, Cataetyx rubrirostris.

Cranial osteology, canal neuromast distribution, superficial neuromast distribution and innervation, and cephalic pore structure were studied in cleared and stained specimens of the deep sea brotulid Cataetyx rubrirostris. The cranial bone structure of C. rubrirostris is similar to other brotulids (Dicrolene sp.) and zoarcids (Zoarces sp.), except for an unusual amount of overlapping of the bones surrounding the cranial vault. The superficial neuromasts are innervated by the anterodorsal, anteroventral, middle and posterior lateral line nerves and are organized similarly to those of the blind ophidioid cave fish Typhliasina pearsei. The cephalic pores open into a widened lateral line canal system. The canal is compartmentalized into a series of neuromast-containing chambers that probably amplify signals received by the system.

Animals↗

Phylogenetic relationships of orders within the class colpodea (Phylum ciliophora) inferred from small subunit rRNA gene sequences

Molecular analyses have been used recently to refine our knowledge of phylogenetic relationships within the ciliated protozoa (phylum Ciliophora). A current Hennigian phylogeny of the orders in the class Colpodea, based on light and electron microscopic analyses, makes three important assumptions with regard to apomorphic character states, namely, (1) that the kreyellid silver line evolved early in colpodean phylogeny, separating bryometopids, such as Bryometopus, from all other colpodeans; (2) that the macro-micronuclear complex is an autapomorphy of the cyrtolophosidids, such as Platyophrya; and (3) that merotelokinetal stomatogenesis is an apomorphic character of colpodids, such as Colpoda, Bresslaua, and Pseudoplatyophrya. These predictions of relationships within the class Colpodea were investigated by determining the complete small subunit rRNA gene sequences for the colpodid Bresslaua vorax, the grossglockneriid Pseudoplatyophrya nana, and the cyrtolophosidid Platyophrya vorax and a partial sequence for the bryometopid Bryometopus sphagni. These sequences were combined with the previously published complete SSrRNA sequences for the colpodid Colpoda inflata and the bursariomorphid Bursaria truncatella. The affiliations were assessed using both distance matrix and maximum-parsimony analyses. The tree topologies for the class Colpodea were identical in all analyses, with bootstrap support for bifurcations always exceeding 60%. The results suggest the following. (1) Since the clade including Bryometopus and its sister taxon, Bursaria, is never basal, the kreyellid silver-line system evolved later in colpodean phylogeny and does not separate bryometopids from all other colpodeans. (2) Since Platyophrya is always the sister taxon to the other five genera, there is a fundamental phylogenetic significance for its macro-micronuclear complex. (3) Since the colpodids, Colpoda, Bresslaua, and Pseudoplatyophrya, always group in one clade, merotelokinetal stomatogenesis appears to be a derived character state.

Journal Article↗

Responses to dipole stimuli of anterior lateral line nerve fibres in goldfish, Carassius auratus, under still and running water conditions.

We investigated how fibres in the anterior lateral line nerve of goldfish, Carassius auratus, respond to sinusoidal water motions in a background of still or running water. Two types of fibres were distinguished: type I fibres, which most likely innervate superficial neuromasts, were stimulated by running water (10 cm s(-1)) while type II fibres, which most likely innervate canal neuromasts, were not stimulated by running water. The responses of type I fibres to sinusoidal water motions were masked in running water whereas responses of type II fibres were not masked. These findings are in agreement with previous data obtained from the posterior lateral line nerve of goldfish. Furthermore, we demonstrate here that for type I fibres the degree of response masking increased with increasing flow velocity. Finally, the ratio between responses that were masked in running water (type I) and those that were not masked (type II) increases with increasing flow velocity. Flow fluctuations that were generated by a cylinder in front of the fish did not affect ongoing activity in the flow, nor the dipole-evoked responses. The findings are discussed with respect to particle image velocimetry data of the water motions generated in the experiments.

Animals↗

Hydrodynamic detection by cupulae in a lateral line canal: functional relations between physics and physiology.

In the present review, signal-processing capabilities of the canal lateral line organ imposed by its peripheral architecture are quantified in terms of a limited set of measurable physical parameters. It is demonstrated that cupulae in the lateral line canal organ can only partly be described as canal fluid velocity detectors. Deviation from velocity detection may result from resonance, and can be characterized by the extent to which a single dimensionless resonance number, N ( r ), exceeds 1. This number depends on four physical parameters: it is proportional to cupular size, cupular sliding stiffness and canal fluid density, and inversely proportional to the square of fluid viscosity. Situated in a canal, a cupula may benefit from its resonance by compensating for the limited frequency range of water motion that is efficiently transferred into the lateral line canal. The peripheral transfer of hydrodynamic signals, via canal and cupula, leads to a nearly constant sensitivity to outside water acceleration in a bandwidth that ranges from d.c. to a cut-off frequency of up to several hundreds of Hertz, significantly exceeding the cut-off frequency of the lateral line canal. Threshold values of hydrodynamic detection by the canal lateral line organ are derived in terms of water displacement, water velocity, water acceleration and water pressure gradients and are shown to be close to the detection limits imposed by hair cell mechano-transduction in combination with the physical constraints of peripheral lateral line signal transfer. The notion that the combination of canal- and cupular hydrodynamics effectively provides the lateral line canal organ with a constant sensitivity to water acceleration at low frequencies so that it consequently functions as a low-pass detector of pressure gradients, supports the appropriateness of describing it as a sense organ that "feels at a distance" (Dijkgraaf in Biol Rev 38:51-105, 1963).

Animals↗