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Central lateral line pathways in a vocalizing fish.

The organization of the central lateral line pathways in the midshipman fish, Porichthys notatus, was identified following biotin injections into physiologically identified sites in the lateral line-recipient nucleus ventrolateralis in the midbrain. Retrogradely filled neurons are located primarily in nucleus medialis, the principal termination site of lateral line nerve afferents in the medulla, whereas terminal fields are mainly identified in isthmal (nucleus praeeminentialis) and diencephalic (posterior thalamic) nuclei. Compared to other teleosts, nucleus medialis has a distinctive cytoarchitecture in that most of its somata are confined to a dense cell plate adjacent to the fourth ventricle. Injections into nucleus ventrolateralis reveal a caudal (MEDc) and a rostral (MEDr) division of nucleus medialis which are separated by a dorsomedial division of the descending octaval nucleus. MEDc is further divisible into a caudal spherical and a more extensive rostral Purkinje-like cell division. MEDr includes a caudal division of Purkinje-like cells and a rostral division of round and fusiform-shaped cells that form a lateral band under the cerebellar crest. In addition to labeling terminals in nucleus ventrolateralis, biotin injections into MEDc and MEDr further distinguish intrinsic connectivity within nucleus medialis, and also label somata and terminals within other octavolateralis nuclei in the medulla. Injections into both nucleus ventrolateralis and nucleus medialis identify sites which may be processing information from both the auditory and lateral line systems, including the eighth nerve-recipient descending octaval nucleus, the acoustic division of the midbrain, and nucleus praeeminentialis which receives auditory input from the midbrain in midshipman.

Afferent Pathways↗

[Imaging the development of the zebrafish line].

The lateral line system of the zebrafish offers the qualities of simplicity, accessibility and reproducibility which are most appropriate for the analysis of neural development and pattern formation in vertebrates. Furthermore, the transparency of the fish embryos allows the application of a variety of optical and molecular methods in the living animal, which is essential for a more complete analysis of the system.

Animals↗

Larval development of tectal efferents and afferents in Xenopus laevis (Amphibia Anura).

The development of tectal connections in Xenopus laevis had been investigated using the degeneration technique to demonstrate the efferent pathways and the retrograde HRP transport to label the afferent pathways. Bilateral tectal efferents were present as soon as the beginning of metamorphosis. Ascending efferents originated from the anterior tectal part terminate in the secondary visual thalamic centres whereas the descending efferents coming from the posterior tectal part reached the tegmentum and the medulla oblongata. At this same time, the optic tectum already received secondary visual afferents originating in the ipsilateral pretectum and non-visual afferents from the ipsilateral semicircular torus and tegmentum. Some sparse bilateral isthmotectal connections were also present. Later, efferent pathways showed an increasing number of fibres whereas the sites of origin of afferents became more diversified: the dorsal thalamus, the suprachiasmatic area, the tegmental nuclei and in the medulla oblongata, the reticular and octavolateral areas sent bilateral projections to the optic tectum. At the end of metamorphosis, we noted ipsilateral olivotectal fibres and reciprocal connections between the tectum and the area of the Vth nerve. These last findings and the presence of the following direct projections, not previously reported in Anurans: the reciprocal connections between the tectum and the semicircular torus or the octavolateral area, underline the implication of the optic tectum in the multisensory (visual, acoustic, vibratory) integration elicited during the larval behavior. Also, the relations between the optic tectum and the lateral line system are particularly examined in the discussion.

Afferent Pathways↗

Action of the octavolateralis efferent system upon the lateral line of free-swimming toadfish, Opsanus tau.

The activation and action of the octavolateralis efferent system was studied by chronic recordings of discharge patterns from putative efferent and single primary afferent neurons in alert, free-swimming toadfish. Efferent axons isolated in the anterior lateral line nerve showed phasic discharges following touch stimuli applied to the head or trunk and demonstrated sustained discharges to visual stimuli. Resting discharge patterns of primary afferents were categorized into irregular, burster, regular, and silent classes. Afferent discharges were often modulated by low frequency (less than 1 Hz) water movement around the head generated during respiratory movements. When fish with recording electrodes implanted in the lateral line nerve were visually stimulated, modulated peak discharges and average (DC) firing rates were inhibited in irregular-type units only. Inhibition of irregular-type afferent neurons also followed visual presentation of natural prey and persisted long after prey stimuli were removed from view. The inhibitory action upon lateralis afferents when activated by biologically significant visual stimuli leads to the hypothesis that the octavolateralis efferent system functions in the peripheral processing of information carried by the lateral line in natural settings.

Animals↗

Effective stimulus for the Xenopus laevis lateral-line hair-cell system.

An in vitro preparation of the lateral-line organ of the African clawed toad Xenopus laevis was used to evaluate the properties of the physiological stimuli which are most effective in evoking neural responses in this simple hair-cell system. Changes in the mean firing rate and the amount of modulation of the neural activity in the fibers innervating the hair cells were determined during the presentation of well-controlled pressure or water-movement stimuli in a specially designed chamber that prevented movement and deformation of the organ during stimulation. It was shown that the most effective stimulus for the preparation was a varying flow of fluid past the organ. Sinusoidally varying water movements over a frequency range of 1 to 100 Hz were effective in evoking neural responses at stimulus amplitudes less than 10 mu peak-to-peak; in addition, a small response to a constant-velocity flow was found. Since no movement or deformation of the organ was present during the water-movement stimuli, it was concluded that these aspects of normal physiological stimuli were not necessary to evoke neural responses. Finally, it was demonstrated that the preparation was sensitive to neither constant nor varying-pressure stimuli.

Action Potentials↗

Developmental expression of the POU domain transcription factor Brn-3b (Pou4f2) in the lateral line and visual system of zebrafish.

Members of the class IV POU domain transcription factors are important regulators of neural development. In mouse, Brn-3b (Pou4f2, Brn3.2) and Brn-3c (Pou4f3, Brn3.1) are essential for the normal differentiation and maturation of retinal ganglion cells (RGCs) and hair cells of the auditory system, respectively. In this report, the cloning and expression profile of brn-3b in the zebrafish (Danio rerio) were assessed as the first step for understanding its role in the development of sensory systems. Two brn-3b alternative transcripts exhibited different onset of expression during development but shared overlapping expression domains in the adult visual system. The brn-3b expression in the zebrafish retina was consistent with a conserved role in differentiation and maintenance of RGCs. Expression was also observed in the optic tectum. Unexpectedly, brn-3b was prominently expressed in the migrating posterior lateral line primordium and larval neuromasts. For comparison, brn-3c expression was limited to the otic vesicle and was not detected in the lateral line during embryonic development. The expression of brn-3b in the mechanosensory lateral line of fish suggests a conserved function of a class IV POU domain transcription factor in sensory system development.

Amino Acid Sequence↗

Duplicate sfrp1 genes in zebrafish: sfrp1a is dynamically expressed in the developing central nervous system, gut and lateral line.

The secreted frizzled-related proteins (Sfrp) are a family of soluble proteins with diverse biological functions having the capacity to bind Wnt ligands, to modulate Wnt signalling, and to signal directly via the Wnt receptor, Frizzled. In an enhancer trap screen for embryonic expression in zebrafish we identified an sfrp1 gene. Previous studies suggest an important role for sfrp1 in eye development, however, no data have been reported using the zebrafish model. In this paper, we describe duplicate sfrp1 genes in zebrafish and present a detailed analysis of the expression profile of both genes. Whole mount in situ hybridisation analyses of sfrp1a during embryonic and larval development revealed a dynamic expression profile, including: the central nervous system, where sfrp1a was regionally expressed throughout the brain and developing eye; the posterior gut, from the time of endodermal cell condensation; the lateral line, where sfrp1a was expressed in the migrating primordia and interneuromast cells that give rise to the sensory organs. Other sites included the blastoderm, segmenting mesoderm, olfactory placode, developing ear, pronephros and fin-bud. We have also analysed sfrp1b expression during embryonic development. Surprisingly this gene exhibited a divergent expression profile being limited to the yolk syncytium under the elongating tail-bud, which later covered the distal yolk extension, and transiently in the tail-bud mesenchyme. Overall, our studies provide a basis for future analyses of these developmentally important factors using the zebrafish model.

Amino Acid Sequence↗

Hot-film anemometry for measuring lateral line stimuli.

A hot-film anemometer system has been calibrated and evaluated for the measurement of sinusoidal water motions used in stimulating the mechanosensory lateral line system of a teleost fish. The response of the anemometer system to water motions created by a vibrating sphere was measured over a wide range of frequencies, intensities, and distances from the sphere. The amplitude response of the system to signals along the axis of sphere vibration was found to be linear over a 50-dB range for frequencies from 10-200 Hz, with the lowest end of the dynamic range (between 10(-8) and 10(-9) m) corresponding to physiological measures of best sensitivity in the lateral line system of the mottled sculpin, Cottus bairdi. The measured attenuation of the signal with distance was also linear over this frequency range out to distances of six times the radius ( = 3 mm) of the sphere and followed the predicted falloff rate for a dipolar source. The linear response of the anemometer system over a wide dynamic range encompassing the detection range of the lateral line system, and the match between predicted and measured motions at varying distances from a dipolar source, indicates that hot-film anemometry is a useful technique for measuring low-level, low-frequency signals likely to stimulate the lateral line system and other hydrodynamic detectors.

Animals↗

Physiological characterization of lateral line function in the Antarctic fish Trematomus bernacchii.

The Antarctic notothenioids are a monophyletic radiation of fishes that have evolved under conditions of low light and cold, where non-visual sensory systems, such as the mechanosensory lateral line system, would be of importance. As part of a study of the structure and function of the mechanosensory lateral line system in these fishes we systematically characterized the function of the anterior lateral line system in one of the common benthic species, Trematomus bernacchii. Frequency-response and threshold-tuning curve methods yield similar functional characterizations of single afferent fibre responses to vibrational stimulation. Curve fitting of generalized transfer function to frequency-response curves allows an objective splitting of responses into velocity and acceleration sensitive populations thought to correspond to superficial and canal neuromasts, respectively. Both response types are characterized by a low-pass frequency-response curve, with a relatively low upper frequency cut-off when compared with data from temperate species. The sensitivity of the lateral line system of T. bernacchii is comparable to that of the mottled sculpin Cottus bairdi.

Acceleration↗

The lateral line of zebrafish: a model system for the analysis of morphogenesis and neural development in vertebrates.

The lateral line of the zebrafish has many of the advantages that made the sensory organs of Drosophila a very productive model system: 1) it comprises a set of discrete sense organs (neuromasts) arranged in a defined, species-specific pattern, such that each organ can be individually recognized; 2) the neuromasts are superficial and easy to visualize, and the innervating neurons are easy to label; 3) the sensory projection is simple yet reproducibly organized. Here we describe some of the tools that can be used to investigate the development of this system, and we illustrate their usefulness with specific examples. We conclude that the lateral line is uniquely suited among vertebrate sensory systems for a molecular, cellular and genetic analysis of pattern formation and of neural development.

Animals↗

Organization of the primary projections of the lateral line nerves in the lamprey Lampetra japonica.

The lateral line sensory system of Lampetra japonica is innervated by the anterior and posterior lateral line nerves. The anterior lateral line nerve innervates all electroreceptors throughout the body and mechanoreceptors of the head. The posterior lateral line nerve innervates trunk mechanoreceptors. The anterior lateral line nerve consists of two ganglia (anterior lateral line and intracapsular) and four major peripheral branches (superficial ophthalmic, buccal, hyomandibular, and recurrent nerves). The posterior lateral line nerve has one posterior lateral line ganglion and one peripheral branch. The location and central projection patterns of the primary sensory neurons of these branches of the lateral line nerves were studied with the aid of horseradish peroxidase labeling. The ganglion cells of the buccal nerve were found in the rostral half, and those of the hyomandibular nerve were found in the caudal half of the medial part of the anterior lateral line ganglion. The lateral part of the anterior lateral line ganglion contains ganglion cells of the recurrent nerve and the superficial ophthalmic nerve. The rostral half of the intracapsular ganglion contains ganglion cells of the recurrent, hyomandibular, and buccal nerves. The ganglion cells of the posterior lateral line nerve were found in the posterior lateral line ganglion. The buccal nerve afferents terminated mainly in the lateral part of the ipsilateral mechanoreceptive medial nucleus. The peripheral part of the electroreceptive dorsal nucleus also received several afferents. The hyomandibular afferents terminated ipsilaterally in the central part of the medial nucleus and in the dorsolateral part of the dorsal nucleus. Some afferents of the hyomandibular nerve ascended and descended in the descending nucleus of the trigeminal nerve near its dorsal margin. The ventral nucleus, the primary nucleus of the VIIIth nerve, received a few fibers of the buccal and hyomandibular nerves. In the recurrent nerve, the fibers of the lateral part of the anterior lateral line ganglion terminated throughout the entire dorsal nucleus, and the fibers of the intracapsular ganglion projected to the dorsolateral part of the nucleus. The afferents of the posterior lateral line nerve terminated in the medial part of the ipsilateral medial nucleus and in the lateral part of the contralateral medial nucleus. In the cerebellar area, afferents of the anterior lateral line nerve were located laterally to those of the posterior lateral line nerve. Several fibers terminated in some branchiomotor nuclei, the cerebellar crest, and the dorsal gray near the obex level. No efferent cell bodies were found in the place where efferent neurons of the VIIIth nerve have been previously reported.

Afferent Pathways↗

Multimodal integration in the feeding behaviors of predatory teleost fishes.

The search for useful model systems to study sensory processing in vertebrate nervous systems has resulted in many neuroethological studies investigating the roles played by a single sensory modality in a given behavior. However, animals behaving in a complex, three-dimensional environment receive a large amount of information from external and internal receptor arrays. Clearly, the integration of sensory afference arising from different modalities into a coherent 'gestalt' of the world is essential to the behaviors of most animals. Over the past several years researchers in my laboratory have examined the roles played by the visual and lateral line sensory systems in organizing the feeding behavior of two species of predatory teleost fishes, the largemouth bass, Micropterus salmoides and the muskellunge, Esox masquinongy. The free-field feeding behaviors of these fishes was studied quantitatively in intact animals and compared to animals in which the lateral line and visual systems had been selectively suppressed. The data show that both bass and muskie employ similar approach and strike behaviors. Vision is crucial to the initial detection of, and orientation to, prey. Lateral line and vision together determine the optimum distance and angular deviation for the initiation of a rapid strike toward the prey. Blinded animals are able to strike accurately at prey at very close ranges and small angular deviations, indicating that this modality presents sufficient information to direct the behavior during the final phases of the strike. The results demonstrate that there is a hierarchy of senses involved in feeding behavior, with different modalities playing critical roles in succeeding phases.

Animals↗

Multimodal sensory integration in the strike-feeding behaviour of predatory fishes.

The search for useful model systems for the study of sensory processing in vertebrate nervous systems has resulted in many neuroethological studies investigating the roles played by a single sensory modality in a given behaviour. However, behaviours relying solely upon information from one sensory modality are relatively rare. Animals behaving in a complex, three-dimensional environment receive a large amount of information from external and internal receptor arrays. Clearly, the integration of sensory afference arising from different modalities into a coherent 'gestalt' of the world is essential to the behaviours of most animals. In the last several years our laboratory team has examined the roles played by the visual and lateral line sensory systems in organizing the feeding behaviour of two species of predatory teleost fishes, the largemouth bass, Micropterus salmoides, and the muskellunge, Esox masquinongy. The free-field feeding behaviours of these fishes were studied quantitatively in intact animals and compared to animals in which the lateral line and visual systems had been selectively suppressed. All groups of animals continued to feed successfully, but significant differences were observed between each experimental group, providing strong clues as to the relative role played by each sensory system in the organization of the behaviour. Furthermore, significant differences exist between the two species. The differences in behaviour resulting when an animal is deprived of a given sensory modality reflect the nature of central integrative sensory processes, and these behavioural studies provide a foundation for further neuroanatomical and physiological studies of sensory integration in the vertebrate central nervous system.

Animals↗

Brain areas in abyssal demersal fishes.

Four areas of the brain which receive primary projections from chemical senses ([1] olfactory bulb, [2] gustatory area including facial and vagal lobes), the eye ([3] optic tectum), and mechanosensory, and-hair-cell based systems i.e. the lateral line, vestibular and auditory systems ([4] trigeminal and octavolateral regions) have been studied and relative size differences used to make deductions on the sensory preferences of 35 fish species living on or near the bottom of the deep sea. Furthermore the relative volumes of the telencephalon and the corpus cerebelli were determined. Two evaluation modes were applied: (1) the relative mean of each system was calculated and species with above-average areas identified; (2) a cluster analysis established multivariate correlations among the sensory systems. The diversity of sensory brain areas in this population of fish suggests that the benthic and epibenthic environment of the abyss presents a rich sensory environment. Vision seems to be the single most important sense suggesting the presence of relevant bioluminescent stimuli. However, in combination the chemical senses, smell and taste, surpass the visual system; most prominent among them is olfaction. The trigeminal/octavolateral area indicating the role of lateral line input and possibly audition is also well represented, but only in association with other sensory modalities. A large volume telencephalon was often observed in combination with a prominent olfactory system, whereas cerebella of unusually large sizes occurred in species with above-average visual, hair-cell based, but also olfactory systems, confirming their role as multimodal sensorimotor coordination centers. In several species the predictions derived from the volumetric brain analyses were confirmed by earlier observations of stomach content and data obtained by baited cameras.

Adaptation, Physiological↗

Wide-aperture, line-focused ultrasonic material characterization system based on lateral scanning.

We present a new wide-aperture, line-focused ultrasonic material characterization system. The foci of the transmitting and receiving transducers are located in the specimen-immersion liquid interface; and the output voltage V(x,t) of the system is recorded as a function of the lateral position of the receiving transducer. The two-dimensional spectrum of V(x, t) can be expressed as a product of the transfer function of the system and the reflectance function of the interface. In comparison with a system based on scanning in the z direction, the angular resolution of the proposed technique increases with decreasing angle of incidence. There are no geometrical restrictions on the length of the recorded spatial data and the angle of incidence in the case of lateral scanning. The temperature coefficient of the measurement error is low because of the constancy of the propagation distance of ultrasound in the immersion fluid during data acquisition.

Journal Article↗

Dissolved copper triggers cell death in the peripheral mechanosensory system of larval fish.

Dissolved copper is an increasingly common non-point source contaminant in urban and urbanizing watersheds. In the present study, we investigated the sublethal effects of dissolved copper on the peripheral mechanosensory system, or lateral line, of larval zebrafish (Danio rerio). Zebrafish larvae were exposed to copper (0-65 microg/L), and the cytotoxic responses of individual lateral line receptor neurons were examined using a combination of in vivo fluorescence imaging, confocal microscopy, scanning electron microscopy, and conventional histology. Dissolved copper triggered a dose-dependent loss of neurons in identified lateral line neuromasts at concentrations > or = 20 microg/L. The onset of cell death in the larval mechanosensory system was rapid (< 1 h). When copper-exposed zebrafish were transferred to clean water, the lateral line regenerated over the course of 2 d. In contrast, the lateral line of larvae exposed continuously to dissolved copper (50 microg/L) for 3 d did not recover. Collectively, these results show that peripheral mechanosensory neurons are vulnerable to the neurotoxic effects of copper. Consequently, dissolved copper in non-point source storm-water runoff has the potential to interfere with rheotaxis, schooling, predator avoidance, and other mechanosensory-mediated behaviors that are important for the migration and survival of fish.

Animals↗

Pattern formation in the urodele mechanoreceptive lateral line: what features can be exploited for the study of development and evolution?

The lateral line is a specialized system of mechano- and electrosensory organs found in anamniotes. This system develops from ectodermal placodes, which migrate extensively along specific routes and deposit sensory organ anlagen at regular intervals, making it ideal for examining several important aspects of pattern formation. Urodele embryos are excellent model organisms for studies of pattern formation in the lateral-line system. The results of such studies are also important for understanding the evolutionary control of changes in pattern. The developmental mechanisms which control pattern formation in the urodele lateral line are reviewed, and some of the broader evolutionary implications of these mechanisms are discussed.

Ambystoma mexicanum↗