Responses of the goldfish head lateral line to moving objects

We investigated how fibers in the anterior lateral line nerve of goldfish, Carassius auratus, respond to water motions generated by an object that was moved alongside the fish. Motion direction was from anterior to posterior or opposite, object diameter was between 0.1 and 4 cm and the distance between object and fish varied between 1 and 6 cm. Fibers exhibited monophasic responses characterized by a transient increase in discharge rate, biphasic responses consisting of an increase followed by a decrease in discharge rate or vice versa, or triphasic responses characterized by a rate increase followed by a decrease and again an increase or by the inverse pattern. In two-thirds of the fibers response patterns depended on object motion direction. Of these, about 60% responded to a reversal of motion direction with an inversion of the response pattern. Our results differ from previous data obtained from posterior lateral line nerve fibers in the relative proportions of the observed response patterns, and by a much smaller proportion of fibers that exhibited a direction-dependent response. These differences can be explained by the fact that the spatial orientations of the neuromasts on the head are more heterogenuous than on the trunk.     

The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.Abbreviation EOD electric organ discharge     

Responses of midbrain lateral line units of the goldfish, Carassius auratus, to constant-amplitude and amplitude-modulated water wave stimuli

 Responses of mechanosensory lateral line units to constant-amplitude hydrodynamic stimuli and to sinusoidally amplitude-modulated water movements were recorded from the goldfish (Carassius auratus) torus semicircularis. Responses were classified by the number of spikes evoked in the unit's dynamic range and by the degree of phase locking to the carrier- and amplitude-modulation frequency of the stimulus. Most midbrain units showed phasic responses to constant-amplitude hydrodynamic stimuli. For different units peri-stimulus time histograms varied widely. Based on iso-displacement curves, midbrain units prefered either low frequencies (≤33 Hz), mid frequencies (50–100 Hz), or high frequencies (≥200 Hz). The distribution of the coefficient of synchronization to constant-amplitude stimuli showed that most units were only weakly phase locked. Midbrain units of the goldfish responded to amplitude-modulated water motions in a phasic/tonic or tonic fashion. Units highly phase locked to the amplitude modulation frequency, provided that modulation depth was at least 36%. Units tuned to one particular amplitude modulation frequency were not found. Accepted: 10 July 1999     

Responses to dipole stimuli of anterior lateral line nerve fibres in goldfish, <Emphasis Type="Italic">Carassius auratus</Emphasis>, under still and running water conditions

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

The responses of central octavolateralis cells to moving sources

Mechanosensory lateral line units recorded from the medulla (medial octavolateralis nucleus) and midbrain (torus semicircularis) of the bottom dwelling catfish Ancistrus sp. responded to water movements caused by an object that passed the fish laterally. In terms of peak spike rate or total number of spikes elicited responses increased with object speed and sometimes showed saturation (Figs. 7, 14). At sequentially greater distances the responses of most medullary lateral line units decayed with object distance (Fig. 11). Units tuned to a certain object speed or distance were not found. The signed directionality index of most lateral line units was between –50 and +50, i.e. these units were not or only slightly sensitive to the direction of object motion (Figs. 10, 17). However, some units were highly directionally sensitive in that the main features of the response histograms and/or peak spike rates clearly depended on the direction of object movement (e.g. Fig. 9C, D and Fig. 16). Midbrain lateral line units of Ancistrus may receive input from more than one sensory modality. All bimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. Units which receive bimodal input may show an extended speed range (e.g. Fig. 18).Abbreviations MON medial octavolateralis nucleus - MSR mean spike rate - PSR peak spike rate - p-p peak-to-peak - SDI signed directionality index     

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. Accepted: 2 June 1999     

Coding of lateral line stimuli in the goldfish midbrain in still and running water

We investigated in goldfish, Carassius auratus, how running water affects the responses of toral lateral line units to a stationary vibrating sphere or to a non-vibrating sphere that moves along the side of the fish. Experiments were conducted in the presence of running water (hydrodynamic noise) to further explore the sensory capabilities of the lateral line with special focus on the morphological sub-modalities. Previous recordings from lateral line nerve fibres in various fish species and the first nucleus of the ascending lateral line pathway in goldfish revealed flow-sensitive and flow-insensitive units. These physiological differences represent, at least in part, the differences in morphology of the lateral line, superficial and canal neuromasts. Following up on these findings we recorded flow-sensitive and flow-insensitive units in the Torus semicircularis of goldfish. In still water, both types of units responded to a vibrating or moving sphere. In running water, neural responses were weaker when the sphere was moved with the flow but were comparable or slightly stronger when the sphere was moved against the flow. In running water, responses of flow-sensitive fibres to the vibrating sphere were masked. In contrast, the responses of units insensitive to water flow were not masked. Our data confirm previous findings but also indicate differences when compared to previous reports. We discuss these differences with respect to lateral line morphology, sub-modalities and convergence of different channels of information at higher brain stations.     

The evolution of the amphibian lateral line system and its bearing on amphibian phylogeny

In modern amphibians that are aquatic the lateral line system is organized, by order, as follows: caecilians have electroreceptive ampullary organs and single rows of mechanoreceptive neuromast organs; generalized anurans have single rows of neuromasts that divide in a transverse plane to form secondary neuromasts or stitches, they do not have ampullary organs; generalized urodeles have ampullary organs, transverse stitches, and double or triple rows of neuromasts. Fossil evidence indicates that early amphibians had both ampullary organs and single rows of neuromasts embedded in bone. With time, receptors became epidermal in all three orders. Modern caecilians have retained the primitive receptor arrangement. I propose that the common ancestor of anurans and urodeles had transverse stitches, and that this character allies these two groups. Subsequent to the anuranurodele split, anurans lost their ampullary organs, perhaps concomitant with developing specializations for herbivory. Urodeles developed orthogonal neuromast couplets und triplets. In modern anurans und urodeles, transverse stitches are correlated with pond dwelling, while ampullary organs are correlated with carnivory, suggesting that the anuran-urodele ancestor(s) was a (were) pond-dwelling carnivore(s).     

Variations of glycogen: II. Following deafferentation of Knollenorgan sensory cells,a lateral line electroreceptor of mormyrid fish

The effect of deafferentation on glycogen metabolism was studied in the sensory cells of mormyrid Knollenorgan electroreceptors. Glycogen was visualized in the sensory cells after fixation in a solution containing potassium ferricyanide and osmium tetroxide. The density variations of glycogen were evaluated by a morphometric method. Sectioning of the afferent nerve results in a cessation of the spontaneous receptor cells activity after 48 h and the glycogen content of these cells increases three fold in the first 5 days after nerve transection. From day 5 on, the glycogen concentration diminishes progressively until day 13. After the sensory cells had become completely deformed, the quantification of glycogen particles was no longer possible and the degeneration of the sensory cells was complete within 20 days after nerve section. These results show that (1) the afferent nerve fibre is indispensable for the anatomo-functional maintenance of the sensory cells and (2) the nerve has only an indirect influence on glycogen variations within the sensory cells.     

Development of the lateral line canal system through a bone remodeling process in zebrafish

The lateral line system of teleost fish is composed of mechanosensory receptors (neuromasts), comprising superficial receptors and others embedded in canals running under the skin. Canal diameter and size of the canal neuromasts are correlated with increasing body size, thus providing a very simple system to investigate mechanisms underlying the coordination between organ growth and body size. Here, we examine the development of the trunk lateral line canal system in zebrafish. We demonstrated that trunk canals originate from scales through a bone remodeling process, which we suggest is essential for the normal growth of canals and canal neuromasts. Moreover, we found that lateral line cells are required for the formation of canals, suggesting the existence of mutual interactions between the sensory system and surrounding connective tissues.     

Variations of glycogen: I. Following stimulation of Knollenorgan sensory cells,a lateral line electroreceptor of mormyrid fish

The metabolism of glycogen was studied in sensory cells of the mormyrid fish, Gnathonemus petersii. Knollenorgans, specific cutaneous electroreceptor organs of the lateral line system, have a spontancous electrical activity and their resting discharge in the absence of stimulation is about 0.04 kHz. Various types of stimulation can produce an increase in frequency; the highest frequency (1.30 kHz) is obtained by moving the Knollenorgan above water level. Glycogen was visualized in ultrathin sections after fixation in a solution of potassium ferricyanide and osmium tetroxide. The density of glycogen particles was determined morphometrically in sensory cells before stimulation, after high-frequency activity, and after reimmersion in water. An increase in the electrical activity of the Knollenorgan resulted in a decrease of the glycogen content of sensory cells. The glycogen store was replenished to about 85% of control within 40 min after stimulation and subsequent reimmersion. The results demonstrate that glycogen in the sensory cells of the Knollenorgan represents an energy source which can be catabolized during high electrical activity and replenished during rest.     

Responses of the PAS-positive pars intermedia cells in the cichlid fish Sarotherodon mossambicus to ambient calcium and background adaptation

Summary The function of the PAS-positive pars intermedia cells in fish has been connected with control of background adaptation and of plasma calcium levels. Since background reflectivity and illumination influence calcium metabolism in S. mossambicus, we have tested the hypothesis that the effects of background reflectivity on the PAS-positive cells are mediated by changes in plasma calcium. However, total plasma calcium does not correlate with the activity of the PAS-positive cells as estimated by morphometrical criteria. Transfer of S. mossambicus to a white background leads to a drop in plasma calcium, and a marked reduction of the activity of the PAS-positive cells. Adaptation to low-calcium freshwater, on a neutral background, has the same effect on plasma calcium but has no effect on the PAS-positive cells. The characteristic structural features of highly active PAS-positive cells in fish from a black background are not due to the slight hypocalcemia that occurs in these fish, since addition of calcium to the water in concentrations that fully prevent the drop in plasma calcium does not suppress the PAS-positive cells. These findings make it very unlikely that these cells produce a hypercalcemie factor in S. mossambicus.     

Metamorphosis-related changes in the lateral line system of lampreys, <Emphasis Type="Italic">Petromyzon marinus</Emphasis>

Lamprey metamorphosis leads to considerable changes in morphology and behavior. We have recently reported that larval lampreys possess a functional lateral line system. Here we investigated metamorphic morphological changes in the lateral line system using light and electron microscopy. Functional modifications were studied by recording the trunk lateral line nerve activity of larvae and adults while stimulating neuromasts with approximately sinusoidal water motion. We found a general re-patterning of neuromasts on the head and trunk including an increase in numbers, redistribution within the pit lines, and shifts of the pit lines relative to external features. The trunk lateral line nerve response was qualitatively similar in adults and larvae. Both showed two neuronal populations responding to opposite directions of water flow. Magnitude of the response increased monotonically with stimulus amplitude. At low frequencies, the response lag relative to the stimulus maximum was approximately 220°, and the gain depended approximately linearly on frequency, confirming that superficial neuromasts are velocity detectors. Changes in phase lag with increasing stimulus frequency were steeper in larvae, suggesting slower afferent conductance. The response gain with frequency was smaller for adults, suggesting a narrower frequency discrimination range and decreased sensitivity. These changes may be adaptations for the active lifestyle of adult lampreys.     

Dermal morphogenesis controls lateral line patterning during postembryonic development of teleost fish

The lateral line system displays highly divergent patterns in adult teleost fish. The mechanisms underlying this variability are poorly understood. Here, we demonstrate that the lateral line mechanoreceptor, the neuromast, gives rise to a series of accessory neuromasts by a serial budding process during postembryonic development in zebrafish. We also show that accessory neuromast formation is highly correlated to the development of underlying dermal structures such as bones and scales. Abnormalities in opercular bone morphogenesis, in endothelin 1-knockdown embryos, are accompanied by stereotypic errors in neuromast budding and positioning, further demonstrating the tight correlation between the patterning of neuromasts and of the underlying dermal bones. In medaka, where scales form between peridermis and opercular bones, the lateral line displays a scale-specific pattern which is never observed in zebrafish. These results strongly suggest a control of postembryonic neuromast patterns by underlying dermal structures. This dermal control may explain some aspects of the evolution of lateral line patterns.     

The development of lateral line placodes: Taking a broader view

The lateral line system of anamniote vertebrates enables the detection of local water movement and weak bioelectric fields. Ancestrally, it comprises neuromasts – small sense organs containing mechanosensory hair cells – distributed in characteristic lines over the head and trunk, flanked on the head by fields of electroreceptive ampullary organs, innervated by afferent neurons projecting respectively to the medial and dorsal octavolateral nuclei in the hindbrain. Given the independent loss of the electrosensory system in multiple lineages, the development and evolution of the mechanosensory and electrosensory components of the lateral line must be dissociable. Nevertheless, the entire system arises from a series of cranial lateral line placodes, which exhibit two modes of sensory organ formation: elongation to form sensory ridges that fragment (with neuromasts differentiating in the center of the ridge, and ampullary organs on the flanks), or migration as collectives of cells, depositing sense organs in their wake. Intensive study of the migrating posterior lateral line placode in zebrafish has yielded a wealth of information concerning the molecular control of migration and neuromast formation in this migrating placode, in this cypriniform teleost species. However, our mechanistic understanding of neuromast and ampullary organ formation by elongating lateral line placodes, and even of other zebrafish lateral line placodes, is sparse or non-existent. Here, we attempt to highlight the diversity of lateral line development and the limits of the current research focus on the zebrafish posterior lateral line placode. We hope this will stimulate a broader approach to this fascinating sensory system.     

Brainstem lateral line responses to sinusoidal wave stimuli in the goldfish, Carassius auratus

Extracellular recordings were made from single lateral line units in the medial octavolateralis nucleus in the brainstem of goldfish, Carassius auratus. Units were defined as receiving lateral line input if they responded to the water motions generated by a stationary, sinusoidally oscillating sphere and/or a moving sphere but not to airborne sound and vibrations. Units which responded to airborne sound or vibrations were assumed to receive input from the inner ear and were not further investigated. Responses of lateral line units were quantified in terms of the number of evoked spikes and the degree of phase-locking to a 50 Hz vibrating sphere presented at various stationary locations along the side of the fish. Receptive fields were characterized based on spike rate, degree of phase-locking and average phase angle as a function of sphere location. Four groups of units were distinguished: 1, units with receptive fields comparable to those of primary afferents; 2, units with receptive fields which consisted of one excitatory and one inhibitory area; 3, units with receptive fields which consisted of more than two excitatory and/or inhibitory areas; 4, units with receptive fields which consisted of a single excitatory or a single inhibitory area. The receptive fields of most units were characterized by adjacent excitatory and inhibitory areas. This organization is reminiscent of excitatory-inhibitory receptive field organizations in other vertebrate sensory systems.     

Ontogeny and phylogeny of the trunk lateral line system in cichlid fishes

An examination of the ontogeny of the lateral line trunk canal and the diversity of adult trunk canal patterns among cichlids indicates that bidirectional canal formation is a general ontogenetic pattern in the Cichlidae with the exception of Cichla and those few species with a complete trunk canal pattern. In addition to the tubed scales which make up the trunk canal, some lateral line scales have pits containing superficial neuromasts. These are recognized as components of the lateral line system of the trunk in adult cichlids for the first time. Eight trunk canal patterns that are variations on a simple disjunct pattern are defined among the 17 cichlid genera examined. Using bidirectional canal formation as a developmental model, these patterns can be placed along an ontogenetic spectrum. This suggests that heterochrony (alterations in the timing of development) is an important mechanism of evolutionary change in the lateral line system of the trunk in cichlid fishes.