Lateral Line Nerve Research Articles

The pit organs of elasmobranchs: a review.

Elasmobranchs have hundreds of tiny sensory organs, called pit organs, scattered over the skin surface. The pit organs were noted in many early studies of the lateral line, but their exact nature has long remained a mystery. Although pit organs were known to be innervated by the lateral line nerves, and light micrographs suggested that they were free neuromasts, speculation that they may be external taste buds or chemoreceptors has persisted until recently. Electron micrographs have now revealed that the pit organs are indeed free neuromasts. Their functional and behavioural role(s), however, are yet to be investigated.

Responses of Anterior Lateral Line Afferent Neurones to Water Flow

The mechanoreceptive lateral line system detects hydrodynamic stimuli and plays an important role in a number of types of fish behaviour, including orientation to water currents. The lateral line is composed of hair cell receptor organs called neuromasts that occur as superficial neuromasts on the surface of the skin or canal neuromasts located in subepidermal canals. Both are innervated by primary afferents of the lateral line nerves. Although there have been extensive studies of the response properties of lateral line afferents to vibrating sources, their response to water flow has not been reported. In this study, we recorded extracellularly from anterior lateral line afferents in the New Zealand long-fin eel Anguilla dieffenbachii while stimulating the eel with unidirectional water flows at 0.5-4 cm s(-)(1). Of the afferents, 80 % were flow-sensitive to varying degrees, the response magnitude increasing with flow rate. Flow-sensitive fibres gave non-adapting tonic responses, indicating that these fibres detect absolute flow velocity. Further studies are needed to confirm whether flow-sensitive and flow-insensitive fibres correlate with superficial and canal neuromasts, respectively.

Organization of the lateral line system in embryonic zebrafish

We describe the organization of lateral line nerves and ganglia in the embryonic zebrafish, Danio rerio. Two lateral line nerves are found anterior to the otic vesicle: the anterodorsal nerve innervates neuromasts of the supraorbital, infraorbital, and otic lines, whereas the anteroventral nerve innervates the mandibular and opercular lines. An additional two lateral line nerves are found posterior to the otic vesicle: the middle lateral line nerve innervates the middle line, whereas the posterior nerve innervates the occipital dorsal and posterior trunk lines. Preotic nerves converge on a single entry zone into the central nervous system at the facial motor root (mVII), as do axons of the octaval nerve. Postotic nerves converge to a posterior entry zone at the glossopharyngeal root. Both lateral line ganglia and neuromasts develop on a stereotypical schedule. To examine the segmental relationships among cranial ganglia, neural crest, and hindbrain, lateral line organization was analyzed in valentino mutants, which have disruptions in the development of rhombomeres 5–7 and in the third arch neural crest, and are missing glossopharyngeal motor neurons. The proposed corresponding lateral line nerve for this head segment, the middle lateral line, appears to develop normally. However, the middle and posterior nerves do not form a posterior entry zone in the absence of a glossopharyngeal root in val mutants, but instead course anteriorly to join the preotic nerves. J. Comp. Neurol. 421:189–198, 2000. © 2000 Wiley-Liss, Inc.

Distribution and innervation of lateral line organs in the channel catfish

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

Organization of the lateral line system in embryonic zebrafish

We describe the organization of lateral line nerves and ganglia in the embryonic zebrafish, Danio rerio. Two lateral line nerves are found anterior to the otic vesicle: the anterodorsal nerve innervates neuromasts of the supraorbital, infraorbital, and otic lines, whereas the anteroventral nerve innervates the mandibular and opercular lines. An additional two lateral line nerves are found posterior to the otic vesicle: the middle lateral line nerve innervates the middle line, whereas the posterior nerve innervates the occipital dorsal and posterior trunk lines. Preotic nerves converge on a single entry zone into the central nervous system at the facial motor root (mVII), as do axons of the octaval nerve. Postotic nerves converge to a posterior entry zone at the glossopharyngeal root. Both lateral line ganglia and neuromasts develop on a stereotypical schedule. To examine the segmental relationships among cranial ganglia, neural crest, and hindbrain, lateral line organization was analyzed in valentino mutants, which have disruptions in the development of rhombomeres 5-7 and in the third arch neural crest, and are missing glossopharyngeal motor neurons. The proposed corresponding lateral line nerve for this head segment, the middle lateral line, appears to develop normally. However, the middle and posterior nerves do not form a posterior entry zone in the absence of a glossopharyngeal root in val mutants, but instead course anteriorly to join the preotic nerves.

Pressure and pressure-gradient sensitivity of the tadpole medulla

The dorsal medulla of anuran tadpoles undergoes significant anatomical reorganization over metamorphic development. To examine how functional properties alter in response to anatomical changes, we recorded single and multiple unit activity in the medulla of bullfrog tadpoles to a sinusoidal-oscillating dipole source that traversed the length of the animal’s body. This dipole stimulus has been used previously to distinguish between pressure-sensitive auditory responses in the saccular nerve of the goldfish and pressure-gradient lateral line responses in the lateral line nerves of goldfish and other teleost fish. Recording sites in the developing dorsal lateral nucleus showed pressure-type responses to dipole stimulation near the animal’s head and lung. Evidence for the role of the bronchial columella and the air-filled lungs acting as a sound pressure transducer in mediating these responses was equivocal. Recording sites in the lateral line nucleus and surrounding neuropil showed pressure-gradient-type responses to stimulation near identified lines of superficial neuromasts on the body or tail. These data show that dipole stimulation is effective in eliciting responses from the medulla, and can be used to elucidate changes in function as the lateral line system degenerates and an auditory system adapted to hearing airborne sounds develops.

Expression of zebrafish fkd6 in neural crest-derived glia

The zebrafish fkd6 gene is a marker for premigratory neural crest. In this study, we analyze later expression in putative glia of the peripheral nervous system. Prior to neural crest migration, fkd6 expression is downregulated in crest cells. Subsequently, expression appears initially in loose clusters of cells in positions corresponding to cranial ganglia. Double labelling with a neuronal marker shows that fkd6-expressing cells are not differentiated neurones and generally lie peripheral to neurones in ganglia. Later, expression appears associated with the posterior lateral line and other cranial nerves. For the posterior lateral line nerve, we show that fkd6-labeling extends caudally along this nerve in tight correlation with lateral line primordium migration and axon elongation. Expression in colourless mutant embryos is consistent with these cells being satellite glia and Schwann cells.

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.

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. J. Morphol. 241:265–274, 1999. © 1999 Wiley-Liss, Inc.

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.

Peripheral lateral line responses to amplitude-modulated sinusoidal wave stimuli

This report describes the responses of single afferent fibers in the posterior lateral line nerve of the goldfish, Carassius auratus, to pure tone and to amplitude-modulated sinusoidal wave stimuli generated by a dipole source (stationary vibrating sphere). Responses were characterized in terms of output-input functions relating responses to vibration amplitude, peri-stimulus time histograms relating responses to stimulus duration, and the degree of phase-locking to both the carrier frequency and the modulation frequency of the amplitude-modulated stimulus. All posterior lateral line nerve fibers responded to a pure sine wave with sustained and strongly phase-locked discharges. When stimulated with amplitude-modulated sine waves, fibers responded with strong phase-locking to the carrier frequency and, in addition, discharge rates were modulated according to the amplitude modulation frequency. However, phase-locking to the amplitude modulation frequency was weaker than phase-locking to the carrier frequency. The data indicate that the discharges of primary lateral line afferents encode both the carrier frequency and the modulation frequency of an amplitude-modulated wave stimulus.

Structural and functional aspects of the fast electrosensory pathway in the electrosensory lateral line lobe of the pulse fishGymnotus carapo

The fast electrosensory pathway (FEP) of gymnotiform fish is mediated by tuberous electroreceptor organs innervated by ganglion cells that synapse with spherical cells of the electrosensory lateral line lobe (ELL). Spherical cells project to the magnocellular mesencephalic nucleus. The electrosensory environment was represented somatotopically within ELL. The mandibular (MN) and the supraorbital (SON) nerves projected to rostral ELL (occupying 19-28% and 4-10%, respectively), and the posterior branch of the anterior lateral line nerve (pALLN) projected to caudal ELL (occupying 56-64%). Labeling with horseradish peroxidase or biotinylated dextran-amine demonstrated three kinds of synaptic endings coupling primary afferents to spherical cells: multiple synaptic knobs, medium-sized calyxes, and very large calyxes. Multiple synaptic knobs arose from MN and SON primary afferents and were found in a narrow rostral area covering the centrolateral (CLS) and lateral (LS) segments of ELL. Medium and large calyxes, proceeding from the same nerves, predominated in the remaining parts of the three segments of ELL containing spherical cells. Calyx-type endings were also found in the LS-occupying regions in which the pALLNs projected. Calyx-type endings formed gap junctions but also contained vesicles and showed submembrane specializations typical of chemical synapses. The postsynaptic spherical cells were linked by dendrosomatic gap junctions and were also contacted by unlabeled en passant synaptic boutons, whose fine structure suggested chemical transmission. Electrophysiological studies indicated that spherical cell responsiveness diminished after electrosensory stimulation. This apparently inhibitory phenomenon may be subserved by the unlabeled synaptic boutons, which possibly originate from interneurons that have yet to be identified.

Morphology of the brain and sense organs in the snailfish Paraliparis devriesi: neural convergence and sensory compensation on the Antarctic shelf.

The Antarctic snailfish Paraliparis devriesi (Liparidae) is an epibenthic species, inhabiting depths of 500-650 m in McMurdo Sound. Liparids are the most speciose fish family in the Antarctic Region. We examine the gross morphology and histology of the sense organs and brain of P. devriesi and provide a phyletic perspective by comparing this morphology to that of four scorpaeniforms and of sympatric perciform notothenioids. The brain has numerous derived features, including well-developed olfactory lamellae with thick epithelia, large olfactory nerves and bulbs, and large telencephalic lobes. The retina contains only rods and exhibits a high convergence ratio (82:1). Optic nerves are small and nonpleated. The tectum is small. The corpus of the cerebellum is large, whereas the valvula is vestigial. The rhombencephalon and bulbospinal junction are extended and feature expanded vagal and spinal sensory lobes as well as hypertrophied dorsal horns and funiculi in the rostral spinal cord. The lower lobes of the pectoral fins have taste buds and expanded somatosensory innervation. Although the cephalic lateral line and anterior lateral line nerve are well developed, the trunk lateral line and posterior lateral line nerve are reduced. Near-field mechanoreception by trunk neuromasts may have been compromised by the watery, gelatinous subdermal extracellular matrix employed as a buoyancy mechanism. The expanded somatosensory input to the pectoral fin may compensate for the reduction in the trunk lateral line. The brains of P. devriesi and sympatric notothenioids share well-developed olfactory systems, an enlarged preoptic-hypophyseal axis, and subependymal expansions. Although the functional significance is unknown, the latter two features are correlated with habitation of the deep subzero waters of the Antarctic shelf.

Morphology of the brain and sense organs in the snailfishParaliparis devriesi: Neural convergence and sensory compensation on the Antarctic shelf

The Antarctic snailfish Paraliparis devriesi (Liparidae) is an epibenthic species, inhabiting depths of 500-650 m in McMurdo Sound. Liparids are the most speciose fish family in the Antarctic Region. We examine the gross morphology and histology of the sense organs and brain of P. devriesi and provide a phyletic perspective by comparing this morphology to that of four scorpaeniforms and of sympatric perciform notothenioids. The brain has numerous derived features, including well-developed olfactory lamellae with thick epithelia, large olfactory nerves and bulbs, and large telencephalic lobes. The retina contains only rods and exhibits a high convergence ratio (82:1). Optic nerves are small and nonpleated. The tectum is small. The corpus of the cerebellum is large, whereas the valvula is vestigial. The rhombencephalon and bulbospinal junction are extended and feature expanded vagal and spinal sensory lobes as well as hypertrophied dorsal horns and funiculi in the rostral spinal cord. The lower lobes of the pectoral fins have taste buds and expanded somatosensory innervation. Although the cephalic lateral line and anterior lateral line nerve are well developed, the trunk lateral line and posterior lateral line nerve are reduced. Near-field mechanoreception by trunk neuromasts may have been compromised by the watery, gelatinous subdermal extracellular matrix employed as a buoyancy mechanism. The expanded somatosensory input to the pectoral fin may compensate for the reduction in the trunk lateral line. The brains of P. devriesi and sympatric notothenioids share well-developed olfactory systems, an enlarged preoptic-hypophyseal axis, and subependymal expansions. Although the functional significance is unknown, the latter two features are correlated with habitation of the deep subzero waters of the Antarctic shelf.

Voltage‐gated potassium channels of Schwann cells from trout lateral line nerve: A combined electrophysiological and molecular characterization

Voltage-gated ionic currents were recorded from explant cultured and freshly dissociated SC from trout lateral line nerve using the whole-cell configuration of the patch clamp technique. In the majority of cases a delayed rectifier potassium outward current (KD) was found exclusively, which activated at potentials ≥ −40 mV and reached maximal amplitudes of 240 ± 25.2 nA at 60 mV testpulse potential. This current showed no voltage-dependent kinetics of inactivation and was insensitive to TEA but was effectively blocked by 4-AP. By single cell RT-PCR the transcript of a shaker-related potassium channel gene, termed tsha1 (a fish homologue of Kv1.2), was selectively amplified. In its biophysical and pharmacological properties the native whole cell potassium outward current of trout Schwann cells closely matched those of the cloned tsha1 subunit previously expressed in xenopus oocytes. A small subpopulation of freshly dissociated SC (less than 10%) at hyperpolarizing potentials elicited a potassium inward current instead, which in its kinetics closely resembled the inward rectifier (KIR) of mammalian SC. Neither voltage-gated sodium currents nor membrane currents activated by excitatory amino acids (glutamate, kainate, and quisqualate) were observed. GLIA 23:329–338, 1998. © 1998 Wiley-Liss, Inc.

Voltage-gated potassium channels of Schwann cells from trout lateral line nerve: A combined electrophysiological and molecular characterization

Voltage-gated ionic currents were recorded from explant cultured and freshly dissociated SC from trout lateral line nerve using the whole-cell configuration of the patch clamp technique. In the majority of cases a delayed rectifier potassium outward current (KD) was found exclusively, which activated at potentials > or = -40 mV and reached maximal amplitudes of 240+/-25.2 nA at 60 mV testpulse potential. This current showed no voltage-dependent kinetics of inactivation and was insensitive to TEA but was effectively blocked by 4-AP. By single cell RT-PCR the transcript of a shaker-related potassium channel gene, termed tshal (a fish homologue of Kv1.2), was selectively amplified. In its biophysical and pharmacological properties the native whole cell potassium outward current of trout Schwann cells closely matched those of the cloned tshal subunit previously expressed in xenopus oocytes. A small subpopulation of freshly dissociated SC (less than 10%) at hyperpolarizing potentials elicited a potassium inward current instead, which in its kinetics closely resembled the inward rectifier (KIR) of mammalian SC. Neither voltage-gated sodium currents nor membrane currents activated by excitatory amino acids (glutamate, kainate, and quisqualate) were observed.

PET activation in V5 and fusiform gyrus related to vergence task

The axolotl Mauthner (M) cell receives synapses from the vestibular and lateral line nerves on highly branched regions located ventrally and dorsally, respectively, of its lateral dendrite. One of the pair of M-cells was deprived of all ipsilateral vestibular supply and of some lateral line supply by unilateral ablation of the otic vesicle at stage 34, before nerve outgrowth and M-cell differentiation. Histological reconstruction of such deprived M-cells at stages 42 and 45, following M-cell differentiation, revealed that the deprived dendrite was poorly developed, being thinner and much less ramified than in controls. This effect was specific; no changes were consistently observed in the shape or size of the M-cell body, the medial dendrite, or the axon. Electron microscopic examination of deprived M-cells showed that morphologically normal synapses were present on the lateral dendrite; however, synaptic knobs identifiable as being of vestibular origin were absent. We suggest that patterned growth and branching of the M-lateral dendrite during differentiation is regulated through interactions with afferent axons.

Peripheral encoding of moving sources by the lateral line system of a sit-and-wait predator

Video-tape recordings of prey-capture behaviour were made to demonstrate that stargazers can detect and capture prey in the dark and to determine the range of prey movement velocities that resulted in prey capture. Electrophysiological recording techniques were then used to determine how an artificial source (a sphere), moving at speeds within the range of recorded prey movement velocities, was encoded by anterior lateral line nerve fibres innervating the preopercular-mandibular canals on the head. A vibrating sphere was also used to measure frequency-response characteristics to determine the bandwidth of response and fibre origin (type of neuromast and location). In order to measure the relevant stimulus parameters likely to govern neural responses, the pressure-gradient pattern produced by the moving sphere was characterised with a pair of miniature hydrophones separated by approximately the same distance as head lateral line canal pores on stargazers. At least four different features of neural response patterns, including direction-dependent changes in the overall envelope of the firing rate pattern, could be predicted on the basis of measured pressure-gradient patterns. The dominant features of both the pressure-gradient and neural response patterns were produced by the wake behind the moving sphere, but behavioural observations indicated that stargazers were responding to the bow of an approaching prey, rather than its wake. Although the form of the wake behind the moving sphere is unlikely to be a good match for the stimulus mediating prey detection, these results clearly establish that pressure-gradient patterns are good predictors of neural response patterns. Thus, similar measurements of pressure-gradient patterns produced by more biologically relevant sources can be used to predict peripheral lateral line responses and stimulus features likely to be of key importance.

Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish.

The first stage of information processing in the electrosensory system involves the encoding of local changes in transdermal potential into trains of action potentials in primary electrosensory afferent nerve fibers. To develop a quantitative model of this encoding process for P-type (probability-coding) afferent fibers in the weakly electric fish Apteronotus leptorhynchus, we recorded single unit activity from electrosensory afferent axons in the posterior branch of the anterior lateral line nerve and analyzed responses to electronically generated sinusoidal amplitude modulations of the local transdermal potential. Over a range of AM frequencies from 0.1 to 200 Hz, the modulation transfer function of P-type afferents is high-pass in character, with a gain that increases monotonically up to AM frequencies of 100 Hz where it begins to roll off, and a phase advance with a range of 15-60 degrees. Based on quantitative analysis of the observed gain and phase characteristics, we present a computationally efficient model of P-type afferent response dynamics which accurately characterizes changes in afferent firing rate in response to amplitude modulations of the fish's own electric organ discharge over a wide range of AM frequencies relevant to active electrolocation.

Octavolateral neurons projecting to the middle and posterior rhombencephalic reticular nuclei of larval lamprey: A retrograde horseradish peroxidase labeling study

The octavolateral area of lampreys, which receives primary fibers from the octaval and lateral line nerves, is involved in the premotor organization of body movements through secondary projections to the reticular formation. Here, the typology of neurons of the three octavolateral nuclei (ventral, medial, and dorsal) that putatively project to the middle and posterior rhombencephalic reticular nuclei were studied by retrograde transport of horseradish peroxidase (HRP) applied to these reticular nuclei. Several types of neurons were labeled in the ventral nucleus, both ipsilateral and contralateral to the site of HRP application. Some of these neurons showed a rather simple morphology (octavomotor neurons, monopolar cells), but most had more- or less-branched dendrites that were associated with one, or several, fields of terminal fibers in the octavolateral area. Unlike those of the ventral nucleus, labeled neurons of the medial nucleus were homogeneous in appearance (mostly pear-shaped). The dorsal nucleus was scarcely developed in larvae, as judged from the very simple and small labeled cells. The presence of terminal or “en-passant” boutons of secondary octavolateral fibers in the reticular area and the commissural nature of these fibers were also investigated by means of application of HRP or indocarbocyanine dye to the octavolateral nuclei. In addition, neurons of other alar plate nuclei that were labeled by the HRP application to the reticular nuclei (trigeminal descending root nucleus and solitary nucleus) were also characterized. The functional significance of these results is discussed. J. Comp. Neurol. 384:396–408, 1997. © 1997 Wiley-Liss, Inc.