The lateral line system of sense organs.
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The effect of metacaine (MS-222) on the activity of the efferent and afferent nerves in the teleost lateral-line system.
1. Free-swimming fish (Tilapia leucosticta and Rutilus rutilus) were used to determine threshold concentrations required for general anesthesia with metacaine (MS-222). The criterion for anesthesia was reached at a concentration of 1:1500 (w/w) with both fish, although the symptoms were somewhat more pronounced in Rutilus. 2. Recordings of efferent spontaneous activity in the lateral-line nerve were used as a measure of the central effect of metacaine during administration in the respiratory stream, as compared with respiration of fresh water. The reduction of activity at the end of a 3-min exposure to the drug was 70%. 3. Maximum recovery (90% of the initial activity) was reached after 30 min application of fresh water. 4. The various efferent impulse types were differentially affected by the anesthetic. 5. Direct recordings from sound-sensitive neurons in the medulla confirm the strong central effect of metacaine. 6. Irrigation of the lateral-line system with anesthetic solution also produced a reduction in afferent spontaneous activity; there was a distinct peripheral effect even at the threshold concentration. 7. Reactions of trigeminal nerve fibers to mechanical stimulation of the skin were reduced after application of a metacaine solution to the skin. This finding confirms the local anesthetic effect of the drug. 8. The anesthetic solution at a given concentration had a greater effect on the CNS than on the peripheral receptors. 9. The implications of the results with respect to the risk of misjudging the depth of general anesthesia are discussed. 10. Because of the complexity of its anesthetic efficacy, it is recommended that metacaine not be used for neurophysiological investigations, but rather that the animals be immobilized by means of muscle relaxants.
Action Potentials↗
The development of lateral-line receptors in Eigenmannia (Teleostei, Gymnotiformes). II. The electroreceptive lateral-line system.
Weakly electric fish of the genus Eigenmannia were induced to spawn in conditions simulating the tropical rainy season. The skin of embryos of different ages was prepared for histological examination, and whole animals were examined by various histological methods and scanning electron microscopy. It was found that the electrosensory system develops after the first mechanoreceptive lines have formed. The tuberous and ampullary organs initially form adjacent to the lines of the lateral-line system. The tuberous organs develop at a rate 5 times higher than that of the ampullary organs. The rate of development for both classes of electroreceptors is 4 times higher on the head than on the trunk. The first tuberous organs develop on the head at day 7 and on the trunk at day 8. They increase in number and size during the growth of the fish. The ampullary organs begin to form on the head and on the most rostral part of the trunk at day 8. They are deeply sunk into the corium and have the same number of receptor cells as in adults. There are both ampullary and tuberous organs within fields of receptors that are innervated by a single nerve branch.
Animals↗
Development of the lateral line system in Xenopus laevis. IV. Pattern formation in the supraorbital system.
The periodic pattern of the supraorbital lateral line organs forms in the epidermis of Xenopus by the subdivision of a streak-like primordium into a linear series of small cell groups. In normal development, each such organ initially contains about 8 cells (Winklbauer & Hausen, 1983a,b). To see whether this initial organ size depends on the size of the streak-like primordium at the time of organ segregation, primordium size was reduced experimentally before the onset of pattern formation. In such small primordia, the size of the primary organs formed is not adjusted so as to allow the formation of a normal number of organs. Instead, the initial organ size is kept approximately normal, and the number of organs is correspondingly reduced, i.e. the pattern forming mechanism is not capable of 'size regulation'.
Animals↗
Efferent neurons of the lateral-line system and the VIII cranial nerve in the brainstem of anurans. A comparative study using retrograde tracer methods.
The octavo-lateral efferent system of several anuran species was studied by means of retrograde transport of horseradish peroxidase. This system is organized similarly in all larval anurans and in all adult aglossids. All have two groups of efferent neurons in the nucleus reticularis medialis between the VIIIth and the IXth motor nucleus. The caudal group consists of efferent neurons that supply the posterior lateral-line nerve (NLLp) and a considerably smaller group of neurons supplying both the NLLp and the anterior lateral-line nerve (NLLa). The rostral group is composed of efferent neurons supplying the NLLa, neurons projecting to the inner ear and neurons supplying both the inner ear and the NLLa. Efferent neurons of the VIIIth cranial nerve exhibit a rostrocaudal cytoarchitectonic differentiation. Caudal perikarya, which are rounder in shape than those of the rostral part, have a dendritic projection to the superior olive. It is suggested that this differentiation reflects a functional differentiation of acoustic and vestibular efferent neurons. Labeled neurons were ipsilateral to the site of application of HRP. None were found in the vestibular nuclei or in the cerebellum. Efferent axons projecting to neuromasts of the NLLa leave the medulla with the VIIth nerve, axons projecting to neuromasts of the NLLp exit via the IXth nerve. Cell counts and the observation of axonal branching revealed that efferent units of both the lateral-line and the VIIIth-nerve system supply more than one receptor organ. In contrast to the lateral-line system, dendrites of efferent neurons of the VIIIth nerve project dorsally onto its nuclei, and afferents of the VIIIth nerve project onto efferent neurons. These structures most probably represent a feedback loop between the afferent and efferent systems of the VIIIth cranial nerve.
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Central organization of the electrosensory lateral line system in bullhead catfish Ictalurus nebulosus.
The connections of the electrosensory lateral line lobe (ELL) of ictalurid catfish were examined by means of horseradish peroxidase tracing methods. The ELL receives direct input from the anterior and posterior lateral line nerves. Some of these nerve fibers continue through the ELL to end as mossy fibers in the lateral portion of the eminentia granularis. Granule cells in this area as well as those in lobus caudalis of the cerebellum project back to the ELL as parallel fibers in the upper molecular layer. The lower molecular layer of the ELL receives its input from the n. praeeminentialis. The ELL projects via the lateral lemniscus to the n. praeeminentialis and torus semicircularis bilaterally, but more heavily on the contralateral side. In addition, the n. praeeminentialis receives the bulk of its input from the ipsilateral torus semicircularis. The caudal lobe of the cerebellum both projects to the electrosensory portion of the torus semicircularis and receives indirect input from the torus semicircularis via the anterior olivary nucleus. In summary, the central organization of this ampullary receptor electrosensory system in catfish is similar to that of the ampullary-tuberous receptor electrosense of mormyrids and gymnotids.
Animals↗
Larval lampreys possess a functional lateral line system.
Morphology of larval lampreys' neuromasts was found to be very similar to that of adults. Activity in the lateral line nerve, elicited by a vibrating ball, indicated a functional lateralis system. Analysis revealed at least two populations of afferents, responding to opposite directions of water flow, with adapting responses. The response magnitude increased monotonically with stimulus amplitude. Larval lampreys' neuromasts were less sensitive than those of teleosts. At low frequencies the response showed a phase lead of 200-220 degrees with respect to the maximum of the ball displacement and a gain that was approximately linearly proportional to frequency.
Afferent Pathways↗
Thalamic center for the lateral line system in the catfish Ictalurus nebulosus: evoked potential evidence.
By means of evoked potential methods, a lateral line center in the thalamus of the bullhead catfish is here identified. The locus of this lateral line center corresponds to the mechanoreceptive thalamic zone and/or torothalamic tract identified by anatomical means. The thalamic lateral line area responds to acoustic stimuli as well as lateral line nerve shock but fails to respond to electroreceptor inputs that do cause responses in their special part of the midbrain torus semicircularis. The latency of the first peak of response to lateral line nerve shock, which is also the main response peak, is 30 ms for the thalamic zone compared to 15 ms for the earliest peak response in the mechanoreceptive part of the torus semicircularis. The thalamic response fatigues much more quickly than the toral response and has different dynamic properties to closely spaced stimulus pairs as well.
Animals↗
Hydrodynamic image formation by the peripheral lateral line system of the Lake Michigan mottled sculpin, Cottus bairdi.
Lake Michigan mottled sculpin (Cottus bairdi) have a lateral-line-mediated prey-capture behaviour that consists of an initial orientation towards the prey, a sequence of approach movements, and a final strike at the prey. This unconditioned behaviour can be elicited from blinded sculpin in the laboratory by both real and artificial (vibrating sphere) prey. In order to visualize what Lake Michigan mottled sculpin might perceive through their lateral line when approaching prey, we have combined anatomical, neurophysiological, behavioural and computational modelling techniques to produce three-dimensional maps of how excitation patterns along the lateral line sensory surface change as sculpin approach a vibrating sphere. Changes in the excitation patterns and the information they contain about source location are consistent with behavioural performance, including the approach pathways taken by sculpin to the sphere, the maximum distances at which approaches can be elicited, distances from which strikes are launched, and strike success. Information content is generally higher for laterally located sources than for frontally located sources and this may explain exceptional performance (e.g. successful strikes from unusually long distances) in response to lateral sources and poor performance (e.g. unsuccessful strikes) to frontal sources.
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Anatomy of the posterior lateral line system in young larvae of the zebrafish.
We studied the anatomy of neuromasts, afferent sensory neurons, and efferent neurons of the midbody branch of the posterior lateral line in larvae of the zebrafish (Brachydanio rerio), 5 days after fertilization. This simple sensory system consists of ten or 11 neuromasts, 15-20 sensory neurons, and about nine efferent neurons. The neuromasts are typical free neuromasts and both afferent and efferent synapses are present on hair cells within them. The sensory neurons project into a single longitudinal column of neuropil in the hindbrain. The sensory terminals appear by light microscopy to contact the dorsolateral dendrite of the ipsilateral Mauthner cell. Three types of efferent neurons are present; two types in the hindbrain and one type in the diencephalon. We provide several lines of evidence that demonstrate that these central neurons are efferent to the lateral line. We conclude from this morphology that the larval system includes all of the components of the adult system and is probably functional at this early stage. We also found that larvae have all of the efferent neurons found in adult zebrafish, while the number of neuromasts and sensory neurons will increase during subsequent development.
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Peripheral and central aspects of the acoustic and lateral line system of a bottom dwelling catfish, Ancistrus sp.
The topographical relationship between the swim bladder, the inner ear, and the otic lateral line was studied in the bottom dwelling catfish, Ancistrus sp. In addition, afferent and efferent subcomponents of the eighth and lateral line nerves were labelled with horseradish peroxidase (HRP) or with differently fluorescing dextran amines. The swim bladder of Ancistrus consists of two separate, transversely oriented parts of each of which is connected to the sinus impar of the inner ears via two Weberian ossicles and the perilymphatic sac. The osseous capsula of the ear has two foramina other than the nerve foramina. One is for the sinus impar. The other foramen, which also separates two fluid-filled spaces, exits where the horizontal canal of the ear contacts the otic lateral line. Both the otic and the postotic lateral line canal run deep below the epidermis. Each canal contains a neuromast that is innervated by the middle lateral line nerve. Further caudally, the otic lateral line canal gives rise to the postotic and finally to the truck canal whose nonossified anterior part travels through an ossified chamber that surrounds the swim bladder. Thus the anterior part of each trunk lateral line canal is in contact with a bipartite sound pressure receiver, the swim bladder. Anterior and posterior lateral line afferents terminate ipsilaterally throughout the neuropil of the electroreceptive lateral line nucleus and the mechanoreceptive nuclei medialis and caudalis of the medulla. Middle lateral line afferents terminate between the projection sites of anterior and posterior lateral line afferents. Some primary mechanosensory anterior lateral line nerve fibers continue into the ipsilateral eminentia granularis and the valvula cerebelli. In the electroreceptive lateral line projection, anterior lateral line fibers terminate more medially and posterior fibers more laterally. This somatotopy is not as clear-cut in the mechanosensory lateral line. Afferents of the sacculus and the lagena terminate predominantly in the saccular nucleus. Afferents of the utriculus, the horizontal canal, and the anterior vertical canal terminate in the magnocellular vestibular nucleus and in the medial octavolateral nucleus. The projection sites of the anterior part and the posterior part of the eighth nerve show little overlap. Eighth nerve projections to the valvula cerebelli are less prominent than the projections from the lateral line. Eighth nerve and lateral line nerve efferents arise from a common nucleus, the octavolateralis efferent nucleus. Axons of efferent cells may divide to supply two or more branches of the eighth nerve and some axons supply both lateral line and eighth nerve endorgans.(ABSTRACT TRUNCATED AT 400 WORDS)
Afferent Pathways↗
Regeneration of sensory cells after laser ablation in the lateral line system: hair cell lineage and macrophage behavior revealed by time-lapse video microscopy.
The regeneration of sensory hair cells in lateral line neuromasts of axolotls was investigated via nearly continuous time-lapse microscopic observation after all preexisting hair cells were killed by a laser microbeam. The laser treatments left neuromasts with one resident cell type, which was supporting cells. Over the course of 1 week, replacement hair cells arose either directly via differentiation of cells present in the epithelium from the beginning of the time-lapse period or via the development of cells produced after one or two divisions of supporting cells. All of the cell divisions that produced hair cells were asymmetrical. During the first hour after the treatment, macrophages and smaller leukocytes were attracted to the laser-treated neuromasts. The smaller leukocytes returned to control levels 48-60 hr after the treatment, whereas macrophages remained active there throughout the period of hair cell replacement. Macrophage incidence peaked 36-48 hr after the laser treatment. Macrophages phagocytosed damaged hair cells and supporting cells, as well as new cells and preexisting cells without recognizable damage. The results provide direct evidence of hair cells arising as progeny produced from the divisions of supporting cells, evidence of hair cells and supporting cells arising from the same cell division, evidence relating to the timing of hair cell differentiation, and indirect evidence pertaining to proposals that hair cells sometimes arise via conversion of cells without an intervening division. The results also suggest that macrophages may influence early stages in the process of hair cell regeneration.
Ambystoma↗
Neural transduction in Xenopus laevis lateral line system.
1. The process of neural excitation in hair cell systems was studied in an in vitro preparation of the Xenopus laevis (African clawed toad) lateral line organ. A specially designed stimulus chamber was used to apply accurately controlled pressure, water movement, or electrical stimuli, and to record the neural responses of the two afferent fibers innervating each organ or stitch. The objective of the study was to determine the characteristics of the neural responses to these stimuli, and thus gain insight into the transduction process. 2. A sustained deflection of the hair cell cilia due to a constant flow of water past the capula resulted in a maintained change in the mean firing rate (MFR) of the afferent fibers. The data also demonstrated that the neural response was proportional to the velocity of the water flow and indicated that both deflection and movement of the cilia were the effective physiological stimuli for this hair cell system. 3. The preparations responded to sinusoidal water movements (past the capula) over the entire frequency range of the stimulus chamber, 0.1-130 Hz, and were most sensitive between 10 and 40 Hz. The variation of the MFR and the percent modulation indicated that the average dynamic range of each organ was 23.5 dB. 4. The thresholds, if any, for sustained pressure changes and for sinusoidal pressure variations in the absence of water movements were very high. Due to the limitations of the stimulus chamber it was not possible to generate pressure stimuli of sufficient magnitude to elicit a neural response without also generating suprathreshold water-movement stimuli. Sustained pressures had no detectable effect on the neural response to water-movement stimuli. 5. The preparations were very sensitive to electrical potentials applied across the toad skin on which the hair cells were located. Potentials which made the ciliated surfaces of the hair cells positive with respect to their bases increased the MFR of the fibers, whereas negative potentials decreased it. The responses to sinusoidal electrical stimuli were similar to responses to water-movement stimuli with respect to frequency and dynamic ranges. Thresholds as low as 100 muV peak to peak (p-p) for 16-Hz stimuli were found. 6. The characteristics of the neural responses to electrical stimulation as well as supporting data obtained from the studies of the effects of anoxia on the evoked responses indicate that the electrical stimulus acts on the hair cells or on the synapses, rather than directly on the nerve fibers. This finding suggests that receptor potentials or their associated currents play an important role in the process of neural excitation in hair cell systems.
Animals↗
Fibers innervating different parts of the lateral line system of an Antarctic notothenioid, Trematomus bernacchii, have similar frequency responses, despite large variation in the peripheral morphology.
Regional differences in the architecture and size of lateral line canals and neuromasts were measured in an Antarctic fish, Trematomus bernacchii, and the data were used in models of canal and cupular mechanics to predict the frequency response of these two peripheral structures. These modeled predictions were then compared to frequency response functions measured with single unit recording techniques from anterior and posterior lateral line fibers innervating different canals on the head and trunk of fish of various sizes. Despite large variations in the peripheral morphology of head and trunk canals in fish of different sizes, lateral line fibers were relatively homogeneous in their frequency response properties. In response to stimuli of equal pk-pk acceleration levels, all canal neuromast fibers responded with equal and maximum responsiveness in the 10-45 Hz range, after which responsiveness fell off at about 18 dB/octave. Whereas the biomechanical models of cupular and canal responsiveness predicted the region of equal and maximum responsiveness in the 10-45 Hz range, they did not predict the high frequency cutoff nor the slope. Rather, these models predicted responsiveness out to at least 540 Hz, and a high frequency slope of 12 dB/octave. In terms of the frequency response of peripheral fibers, we conclude that (1) there can be considerable morphological variability, with little consequence for function, as long as some minimum standards for maintaining constant acceleration responsiveness in the 10-45 Hz range are met, and (2) there must be additional filters between the cupula and primary afferent fibers.
Acceleration↗
Regenerated hair cells can originate from supporting cell progeny: evidence from phototoxicity and laser ablation experiments in the lateral line system.
The mechanisms that lead to the production of sensory hair cells during regeneration have been investigated by using 2 different procedures to ablate preexisting hair cells in individual neuromast sensory epithelia of the lateral line in the tails of salamanders, then monitoring the responses of surviving cells. In one series of experiments, fluorescent excitation was used to cause the phototoxic death of hair cells that selectively take up the pyridinium dye DASPEI. In the other experiments, the ultraviolet output of a pulsed neodymium-YAG laser was focused to a microbeam through a quartz objective lens in epi-illumination mode and used to selectively kill individual unlabeled hair cells while the cells were simultaneously imaged by transmitted light DIC microscopy. Through observation of the treated neuromasts in vivo, these experiments demonstrated that mature sensory epithelia that have been completely depleted of hair cells can still generate new hair cells. Preexisting hair cells are not necessary for regeneration. Immediately after the ablations the only resident cells in the sensory epithelia were supporting cells. These cells were observed to divide at rates that were increased over control values, and eventually those cell divisions gave rise to progeny that differentiated as hair cells, replacing those that had been killed. Macrophages were active in these epithelia, and their phagocytic activity had a significant influence on the standing population of cells. The first new hair cells appeared 3-5 d after the treatments, and additional hair cells usually appeared every 1-2 d for at least 2 weeks. We conclude that the fate of the progeny produced by supporting cell divisions is plastic to a degree, in that these progeny can differentiate either as supporting cells or as hair cells in epithelia where hair cells are missing or depleted.
Ambystoma↗
Minimal model of prey localization through the lateral-line system.
The clawed frog Xenopus is an aquatic predator catching prey at night by detecting water movements caused by its prey. We present a general method, a "minimal model" based on a minimum-variance estimator, to explain prey detection through the frog's many lateral-line organs, even in case several of them are defunct. We show how waveform reconstruction allows Xenopus' neuronal system to determine both the direction and the character of the prey and even to distinguish two simultaneous wave sources. The results can be applied to many aquatic amphibians, fish, or reptiles such as crocodiles.
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A newly described organ associated with the eye and lateral line system in the marine teleost, Stenotomus chrysops.
A hitherto undescribed type of organ, possibly sensory, is reported. It is in the form of small cylindrical projections primarily concentrated on the surface in the area of the reticular lateral-line complex and around the eye of the scup (Stenotomus chrysops). The projection is composed of a central core cell surrounded by an epithelium. Enveloped within the epithelium and parallel to the core cell are six to eight symmetrically arranged 'bulbs' with cytoplasmic stems extending to cell bodies within the epidermis proper. A circle of 'collar' cells at the base of the cylinder facilitates the observed bending of the projection. Detection of the direction of water movement is hypothesized.
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Mutations affecting the formation of posterior lateral line system in Medaka, Oryzias latipes.
We performed a systematic screen for mutations affecting the trajectory of axons visualized by immunohistochemical staining of Medaka embryos with anti-acetylated tubulin antibody. Among the mutations identified, yanagi (yan) and kazura (kaz) mutations caused specific defects in projection of the posterior lateral line (PLL) nerve. In yan and kaz mutant embryos, the PLL nerve main bundle was misrouted ventrally and dorsally or anteriorly. Medaka semaphorin3A, sdf1, and cxcr4 cDNA fragments were cloned to allow analysis of these mutants. There were no changes in semaphorin3A or sdf1 expression in mutant embryos, suggesting that the tissues expressing semaphorin3A or sdf1 that are involved in PLL nerve guidance are present in these mutant embryos. Double staining revealed that the mislocated PLL primordium and growth cone of the ectopically projected PLL nerve were always colocalized in both yan and kaz mutant embryos, suggesting that migration of PLL primordia and PLL nerve growth cones are not uncoupled in these mutants. Although homozygous yan larvae showed incomplete migration of the PLL primordium along the anteroposterior axis, ventral proneuromast migration was complete, suggesting that ventral migration of the proneuromast does not require the signaling affected in yan mutants. In addition to the PLL system, the distribution of primordial germ cells (PGCs) was also affected in both yan and kaz mutant embryos, indicating that yan and kaz genes are required for the migration of both PLL primordia and PGCs. Genetic linkage analysis indicated that kaz is linked to cxcr4, but yan is not linked to sdf1 or cxcr4. These mutations will provide genetic clues to investigate the molecular mechanism underlying formation of the PLL system.
Animals↗