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PubMed2002

What is the nature of multisensory interaction between octavolateralis sub-systems?

The octavolateralis system consists of several submodalities, including the inertial-sensitive inner ear, the pressure-sensitive ear/air cavity complex (when present), and acceleration- and velocity-sensitive components of the lateral line system (canal and superficial neuromasts, respectively). All four of these channels are responsive to many of the same stimulus sources, particularly moving or vibrating objects within a short distance from the receiver. We therefore argue that the octavolateralis system is an excellent model for the study of multisensory interactions. We focus on the possible ways in which these channels may contribute to source localization mechanisms and to the multisensory guidance of behaviors with strong directional components (e.g., predator avoidance, prey capture and mate attraction). Finally, we define four ways in which information from multiple senses might interact. These include fractionation, synergy, accessory stimulation, and complementation. Although evidence for all types of octavolateralis interactions can be found, the primary modes of interaction appear to be complementation and fractionation. For example, the inertial and pressure-sensitive submodalities of the auditory system provide complementary pieces of information about the direction (e.g., left/right) and polarity (advancing or receding) of a moving source. In contrast, the lateral line canal system subserves short-range localization tasks, whereas the auditory system may subserve longer-range detection and localization tasks.

Animals↗
PubMed1998

Mechanoelectrical transduction assisted by Brownian motion: a role for noise in the auditory system.

The organs of the vestibular, auditory and lateral line systems rely on a common strategy for the stimulation of their primary receptors, the hair cells: stimuli induce shear between hair cell epithelia and accessory structures to which hair bundles, the hair cells' mechanosensitive organelles, are attached. The inner hair cells of the cochlea, whose hair bundles are not attached to the overlying tectorial membrane, are a notable exception. Because their hair bundles are not restrained, they undergo significant Brownian motion, a characteristic traditionally thought to blunt the sensitivity of hearing. Contrary to this view, the work reported here indicates that Brownian motion of the hair bundle serves to enhance the sensitivity of mechanoelectrical transduction.

Animals↗
PubMed1983

Primary lateral line response to water surface waves in the topminnow Aplocheilus lineatus (Pisces, Cyprinodontidae).

1. The function of supraorbital organ II/2 of the head lateral line system of the surface feeding fish Aplocheilus lineatus is characterized here by the lateral line nerve response evoked by biologically relevant surface wave trains. 2. A single organ is particularly sensitive to the high frequency, low amplitude cycles at the beginning of a click evoked wave train. By using gated sinusoidal signals it was shown that the following mechanisms are responsible: a. a strong phasic component superimposed on the tonic response component, b. high sensitivity of the organ in the frequency range between 70 and 120 Hz (corresponding to the frequency range of the first cycles of a prey evoked wave), c. the organ is responsive to the acceleration component of wave stimulation (b approximately f2). 4. As the time structure of a surface wave is encoded in a corresponding discharge pattern in the lateral line nerve it is probable that the time structure ('stimulus pattern') of a signal is used by A. lineatus to estimate the distance to its source.

Animals↗
PubMed2002

Development and evolution of lateral line placodes in amphibians I. Development.

Lateral line placodes are specialized regions of the ectoderm that give rise to the receptor organs of the lateral line system as well as to the sensory neurons innervating them. The development of lateral line placodes has been studied in amphibians since the early 1900s. This paper reviews these older studies and tries to integrate them with more recent findings. Lateral line placodes are probably induced in a multistep process from a panplacodal area surrounding the neural plate. The time schedule of these inductive processes has begun to be unravelled, but little is known yet about their molecular basis. Subsequent pattern formation, morphogenesis and differentiation of lateral line placodes proceeds in most respects relatively autonomously: Onset and polarity of migration of lateral line primordia, the type, spacing, size and number of receptor organs formed, as well as the patterned differentiation of different cell types occur normally even in ectopic locations. Only the pathways for migration of lateral line primordia depend on external cues. Thus, lateral line placodes act as integrated and relatively context-insensitive developmental modules.

Journal Article↗
PubMed2006

Proneural gene requirement for hair cell differentiation in the zebrafish lateral line.

The lateral line system comprises an array of mechanosensory organs, the neuromasts, distributed over the body surface. Each neuromast consists of a patch of mechanosensory hair cells surrounded by support cells. We show that, in the zebrafish, two proneural genes are essential for differentiation of the hair cells, neuroD (nrd) and atonal homolog 1 (ath1). Gene knockdown experiments demonstrate that loss of function of either gene, but not of the related proneural gene neurogenin1 (ngn1), abrogate the appearance of hair cell markers. This is in contrast to other sensory systems, such as the neurons of the lateral line ganglion, where nrd is regulated by ngn1 and not by ath1. Overexpression of ath1 can induce nrd, and the phenotype produced by loss of ath1 function can be partially rescued by injection of nrd mRNA. This supports the conclusion that the activation of nrd probably requires ath1 in the hair cell lineage, whereas in sensory neurons nrd activation requires ngn1. We propose that the emergence of two atonal homologs, ath1 and ngn1, allowed the cellular segregation of mechanoreception and signal transmission that were originally performed by a single cell type as found in insects.

Animals↗
PubMed2006

Neural responses to water surface waves in the midbrain of the aquatic predator Xenopus laevis laevis.

Many aquatic vertebrates use mechano-sensory lateral lines to decipher water movements. The peripheral and central organization of the lateral line system has much in common with the auditory system. Therefore, it was hypothesized that the information processing of both systems could be related. Analogous to acoustic objects, for instance, object representations along the central lateral line pathway must be generated from patterns of particle motion across peripheral receivers. Thus, the lateral line offers insight into key features of neural computation beyond a specific sensory system. Here, central processing of water surface waves was described in the African clawed frog which depends on wave signals for prey detection, recognition and localization. Neural responses to surface wave stimuli were recorded in the brainstem and midbrain of Xenopus. A total of 109 units displayed either excitatory or inhibitory responses to surface waves. The response pattern distribution differed significantly across the optic tectum and torus semicircularis magnocellularis (chi-square test, P < 0.05). Stimulus frequencies from 10 to 40 Hz were represented equally across lateral line nuclei but best frequencies were systematically distributed along the rostrocaudal axis of the midbrain (chi-square test, P < 0.05). Forty-one percent of 102 widely distributed units phase locked significantly to stimulus frequencies (Rayleigh test, P < 0.05; vector strength > 0.3) and 41% of 39 tested units featured non-monotone rate-level functions. These neurones were registered mainly in the dorsal tectum and magnocellular torus semicircularis (chi-square test, P < 0.05). Across all tested nuclei, 16 of 17 discreetly distributed units showed a directional response to spatial stimulation. The results suggest midbrain subdivisions with respect to processing of stimulus timing, frequency and amplitude.

Animals↗
PubMed2004

Expression patterns of three estrogen receptor genes during zebrafish (Danio rerio) development: evidence for high expression in neuromasts.

The estrogen receptor (ER) genes encode a group of nuclear enhancer proteins, which are important ligand-activated transcription factors, modulating estrogen-target gene transcription. In this study we analyzed expression patterns of three zebrafish ER genes, esr1, esr2a, and esr2b, during development using whole-mount in situ hybridization. High levels of esr2a and esr2b of maternal origin are inherited and segregated to the blastomers. After the mid-blastula transition, the three genes exhibit similar spatio-temporal patterns of expression. In 24 h postfertilization (hpf) embryos, high levels of esr2a and esr2b and low levels of esr1 mRNAs are detected in the epidermis, pectoral fin buds, hatching gland and, to a lesser extent, developing brain. From 24 hpf onward, the expression of the three genes is down-regulated in the epidermis. By 60 hpf, esr2a mRNA is abundant in mature primary neuromasts of the anterior line system and by 3 days postfertilization (dpf), all mature primary neuromasts in both the anterior and posterior lateral line systems express significant levels of esr2a and esr2b transcripts. Histological sections show a high level of esr2a transcripts in both mechanoreceptive hair cells and supporting cells. The transcripts are still detected after neomycin-induced hair cell death, consistent with the presence of esr2a transcripts in supporting cells. From 6 dpf onward, esr2a and esr2b transcripts are robustly co-expressed in primary neuromasts, branchial arches, pectoral fins, and anal papilla, while slight labeling is observed for esr1 transcripts.

Animals↗
PubMed2003

A hydrodynamic topographic map in the midbrain of goldfish Carassius auratus.

Sensory systems often consist of several parallel pathways. Within each pathway, sensory information may be processed in topographically arranged maps or in maps derived by neuronal computation. Parallel pathways have so far not been described in the central lateral line system of teleost fish at levels higher than the medulla, and evidence for midbrain lateral line maps in fish is still weak. We found two classes of units with different response patterns in the central lateral line nucleus in the torus semicircularis of the goldfish Carassius auratus. Units of one class responded to a passing sphere and to the wake caused by that sphere with excitation. Units of the second class also responded to the moving sphere. However, these units did not respond to the wake behind the sphere. Hydrodynamic information received by class two units was topographically organized in the torus semicircularis of goldfish in that anterior body areas projected to rostral midbrain and posterior body areas to caudal midbrain. Units that responded only to the passing sphere were on average located more ventrally in the lateral TS than the units that responded exclusively to a vibrating sphere.

Afferent Pathways↗
PubMed1993

Reaction to surface waves by Xenopus laevis Daudin. Are sensory systems other than the lateral line involved?

The turning response to surface waves of clawed toads (Xenopus laevis) with an inactivated lateral line was reinvestigated to examine whether sensory systems other than the lateral line ("second systems") are involved. Two methods were used to block the lateral line input: selective and reversible inactivation of the lateral line periphery using CoCl2 or chronic destruction with thermocautery. The time-course of the response recovery (response frequency, turning accuracy and reaction time) was recorded. Following CoCl2 inactivation 10 out of 13 animals did not respond to surface waves for at least 2 days. The remaining 3 animals gave sporadic turning responses. It is assumed that in these individuals a "second system" is permanently involved in the detection of surface waves parallel to the lateral line. Five days after the chronic destruction of the lateral line all animals again turned to the centre of surface waves. It is suggested that by this time the "second system" had become capable of substituting for the missing lateral line input. The response frequency and the accuracy of the turning response of lesioned animals varied considerably among individuals but was always lower than in untreated animals (tested up to 120 days).

Animals↗
PubMed1995

Initiation of locomotion by lateral line photoreceptors in lamprey: behavioural and neurophysiological studies

The lateral line system of lampreys includes photoreceptors distributed in the skin of the tail region. These are innervated by the trunk lateral line nerves, and the afferents terminate bilaterally in the medial octavolateral nucleus, crossing the midline through the cerebellar commissure. Stimulation of the dermal photoreceptors by tail illumination initiates locomotion. The present study was performed to characterize the response to illumination in larval and adult lampreys in detail and to elucidate the neuronal pathways responsible for the activation of locomotion. In both larval and adult quiescent lampreys, the response to unilateral illumination of the tail was found to consist of an initial turn followed by rectilinear swimming. The sign and magnitude of the turning angle were not correlated with the laterality of the optic stimulus. In mechanically restrained lampreys, spinalized at the level of segments 15&shy;20, tail illumination evoked a complex motor response in the rostral part of the body, with switches between different patterns of coordination (turns in different directions, locomotion, and turns combined with locomotion). Thus, the response to tail illumination is not a simple reflex, but includes a behavioural choice. Reticulospinal neurones play a crucial role in the initiation of locomotion in lampreys. The response to unilateral tail illumination in rhombencephalic reticular cells was studied with extracellular single-unit recordings. It was found that neurones in the middle and posterior rhombencephalic reticular nuclei were activated bilaterally. Tonic activity or slow bursts (<0.5 Hz) were evoked, in some cases lasting up to 60 s after the stimulation. The response remained bilateral after transection of one lateral line nerve and the cerebellar commissure. Afferents from one side can thus activate reticulospinal cells on both sides through a pathway outside the cerebellar commissure. This bilateral activation of reticulospinal neurones is presumably responsible for the activation of spinal locomotor networks, without any directional bias to the left or the right side, and for the rectilinear swimming observed in behavioural experiments. In the caudal part of the termination area of the lateral line nerve afferents, neurones with contralateral projections were retrogradely stained with horseradish peroxidase. These neurones appear to be likely candidates for mediating the contralateral effects of the lateral line fibres.

Journal Article↗
PubMed1990

Anatomical connections and electrophysiological properties of toral and dorsal tegmental neurons in the terrestrial urodele Salamandra salamandra.

Fire salamanders (Salamandra salamandra) are strictly terrestrial urodele amphibians, having lost electroreception and the lateral line system during metamorphosis. The present study demonstrates that (i) the lateral lemniscus is supplied by fibers of the medullary acoustic nucleus (nucleus intermedius) and the superior olive; (ii) the subtectal dorsal tegmentum can be clearly separated into a dorsally located torus semicircularis and a ventrally situated dorsal tegmental nucleus, the former processing auditory and vibratory, the latter vestibular signals; and (iii) the hearing capabilities of this animal, as estimated from the tuning of toral units, are comparable to those of anurans with extratympanic sound transmission. It is concluded that vibration sensitivity and hearing are involved in defensive reactions in the non-vocalizing fire salamander. The vestibular cells in the dorsal tegmentum probably relay a head-velocity input to the optic tectum, thus providing a self-motion signal for the visual localization center.

Action Potentials↗
PubMed1981

The pattern of lateral-line afferents in urodeles. A horseradish-peroxidase study.

The organization of posterior and anterior afferents of the lateral-line system was studied in several species of urodeles by means of transganglionic transport of horseradish peroxidase. The afferents of each lateral-line nerve form distinct fascicles in the medullary alar plate. Each of the two branches of the anterior lateral-line nerve is organized in two long and one short fascicles. The posterior lateral-line afferents form only two long fascicles. Each ordinary neuromast is supplied by only two afferents, which run in the two ventral medullary fiber bundles. It is suggested that afferents to hair cells displaying one type of polarity form together one bundle, but those contacting hair cells polarized in the opposite way form the second ventral bundle of one lateral-line branch. Thus, the lateral-line afferents may be organized in a directotopic fashion. The short dorsal fascicle formed only by the anterior lateral-line afferents receives fibers exclusively from small pit organs. Each pit organ is supplied by only one afferent. Anatomically, these pit organs resemble in many respects the electroreceptive ampullary organs of certain fish. Neurons labeled retrogradely via the anterior lateral-line nerve afferents have been attributed to the nervus trigeminus or facialis. In addition to the posterior lateral-line afferents, only few centrifugally projecting neurons were labeled. These neurons are discussed as efferents to the posterior lateral-line neuromasts.

Afferent Pathways↗
PubMed1988

The lateral-line and inner-ear afferents in larval and adult urodeles.

The inner-ear and lateral-line afferents were studied in members of almost all urodele families and in two primitive representatives of anurans and gymnophionans by means of transganglionically transported horseradish peroxidase. The lateral-line projection patterns are, when present, identical in all urodeles and gymnophionans. This is in agreement with the presence of ampullary organs in all urodeles and gymnophionans which possess a lateral-line neuromast system. In contrast, even the most primitive anurans lack both ampullary organs and the dorsal projection of afferents from these organs. In urodeles the inner-ear afferents are found to enter the rhombencephalon via the octaval nerve and bifurcate in the neuropil lateral to the nucleus magnocellularis into a short ascending and a longer descending subpial fascicle. Fibers of the ascending fascicle reach the tip of the lateral recess and terminate in the eminentia granularis. Collaterals are confined to the ipsilateral lobulus lateralis and end presumably as mossy fibers. The descending fascicle ends at the obex level with only a few fibers reaching the second spinal segment. Besides extensive fiber supply to the cells of the ipsilateral ventral-zone column, collaterals are found to reach the reticular formation, nucleus cerebelli, nucleus fasciculus solitarius, intermediate nucleus and several motor nuclei. Differences in the octaval projection among urodele families are limited to variation in its size relative to that of the lateral-line projection. Only species that develop without free-living larvae differ markedly with respect to the absence of lateral-line projections and, presumably, the lateral-line nuclei of the alar plate that exists in larvae. Almost all urodeles that possess a lateral-line system as larvae retain a complete lateral-line system, including neuromasts and ampullary organs, after metamorphosis. Only Salamandra and Chioglossa lose most of their lateral-line afferents and presumably all lateral-line organs around metamorphosis. The octavolateralis projections in urodeles are found to be strikingly similar to those in lampreys, sharks, sturgeons, and, especially, gymnophionans. This points to a great conservatism of this pattern, at least among anamniotic vertebrates. However, even primitive anurans such as Ascaphus differ markedly from these patterns in that they show no ampullary organs or dorsal lateral-line projection but a dorsal projection of the inner ear. Outgroup comparison with other anamniotic vertebrates indicates that the pattern in anurans is derived from the more generalized lateral-line and inner-ear projection pattern as represented in many urodeles and gymno

Amphibians↗
PubMed2000

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.

Anguilla↗
PubMed1987

Distribution and morphological characteristics of efferent neurons innervating end organs in the ear and lateral line of the European eel.

Neurons that provide the efferent innervation to the labyrinthine and lateral line sense organs of the eel were located by applying horseradish peroxidase to branches of the appropriate cranial nerves. Retrogradely labeled neurons were found in a single median column, the octavolateralis efferent nucleus (OEN), located immediately rostral to and overlapping with the facial nucleus of the branchiomotor column. We estimate that on each side of the brain the efferent nucleus contains about 60-70 neurons, most of which supply the ear and the lateral line system of the head. Most neurons (approximately 90%) are ipsilateral to the targets they innervate. There is no crisp topographical order within the nucleus because neurons supplying different end organs intermingle. However, the head lateral line is supplied by rostrally located neurons, and the body system by more caudal neurons. There are no marked differences in cell form between neurons supplying different targets. Most are multipolar, relatively uniform in size, and have extensive dendrites. The dendrites of some cells extend to the contralateral side of the brain. Efferent axons are of small diameter (approximately 3 micron). Two neurons are sufficiently constant in size and location that they can be consistently recognized from fish to fish. Their axons branch to supply more than one target. Nearly all efferent neurons stain for acetylcholinesterase and some, bordering the midline, consistently stain weakly.

Acetylcholinesterase↗
PubMed1994

Formation of new sensory cells in deafferented tuberous organs of the gymnotid fish Eigenmannia virescens.

The cutaneous electroreceptor "tuberous organs" of the lateral line system of Eigenmannia virescens were studied at light and electron microscopic levels with immunohistochemical and autoradiographic techniques after sectioning of the posterior branch of the lateral line nerve. After deafferentation total degeneration of the sensory cells was observed. The accessory cells of the basal platform, however, remain intact and undergo a process of differentiation. The cytoplasms and nuclei of these cells increase in volume, and the nuclei incorporate tritiated thymidine. In control tuberous organs with intact innervation, tritiated thymidine is absorbed by the nuclei of the elongated epidermal cells surrounding the sensory cavity. The newly formed sensory cells, but not those of the intact organs, are substance P immunoreactive. They have synaptic bars surrounded by vesicles and their free membrane surface is covered with microvilli. The new sensory cells are fully differentiated 35 days after the lateral line was cut. These results demonstrate that in the tuberous organs of E. virescens new sensory cells are formed in the absence of an innervation.

Afferent Pathways↗
PubMed1996

Modeling and measuring lateral line excitation patterns to changing dipole source locations.

In order to determine excitation patterns to the lateral line system from a nearby 50 Hz oscillating sphere, dipole flow field equations were used to model the spatial distribution of pressures along a linear array of lateral line canal pores. Modeled predictions were then compared to pressure distributions measured for the same dipole source with a miniature hydrophone placed in a small test tank used for neurophysiological experiments. Finally, neural responses from posterior lateral line nerve fibers in the goldfish were measured in the test tank to demonstrate that modeled and measured pressure gradient patterns were encoded by the lateral line periphery. Response patterns to a 50 Hz dipole source that slowly changed location along the length of the fish included (1) peaks and valleys in spike-rate responses corresponding to changes in pressure gradient amplitudes, (2) 180 degrees phase-shifts corresponding to reversals in the direction of the pressure gradient and (3) distance-dependent changes in the locations of peaks, valleys and 180 degrees phase-shifts. Modeled pressure gradient patterns also predict that the number of neural amplitude peaks and phase transitions will vary as a function of neuromast orientation and axis of source oscillation. The faithful way in which the lateral line periphery encodes pressure gradient patterns has implications for how source location and distance might be encoded by excitation patterns in the CNS. Phase-shift information may be important for (1) inhibitory/excitatory sculpting of receptive fields and (2) unambiguously encoding source distance so that increases in source distance are not confused with decreases in source amplitude.

Acoustic Stimulation↗
PubMed1987

Distribution of afferent fibers in the brainstem from end organs in the ear and lateral line in the European eel.

Sensory nerve fibers from the lateral line system and labyrinth of Anguilla anguilla were labeled with horseradish peroxidase and traced to various targets in the ipsilateral brainstem. The three rami of the anterior lateral line nerve and the supratemporal ramus of the posterior lateral line nerve form overlapping terminal zones in the ventral portion of nucleus medialis. The posterior lateral line nerve on the body is represented exclusively in the dorsal half of the nucleus medialis. Eighth nerve fibers from the otolithic end organs in the inner ear send fibers into dorsal portions of three octavus nuclei: anterior, magnocellular, and descending, and saccular fibers lie most medial and utricular fibers most lateral. Fibers from vestibular organs, especially the semicircular canals and utricle, end densely in ventral portions of these nuclei and in the tangential nucleus. All labyrinthine sense organs send fibers into the region of a Mauthner-like neuron, and all except the saccule terminate in the reticular formation, tangential nucleus, and eminentia granularis of the cerebellum. Primary sensory input to the octavolateralis efferent nucleus comes only from the labyrinth, and fibers from the saccule alone penetrate the region of efferent neuronal somata. Fibers from labyrinthine end organs except the saccule project to the reticular formation where they may contact the dendrites of efferent somata. Fibers from the lateral line and the eighth nerve overlap most extensively at the rostral pole of the nucleus medialis and in the eminentia granularis of the cerebellum.

Afferent Pathways↗