Lateral Line Units Research Articles

Representation of bulk water flow in the goldfish (Carassius auratus) midbrain.

With the mechanosensory lateral line system, fish and semi-aquatic amphibians detect water movements and pressure gradients. Hydrodynamic information picked up by the lateral line receptors is relayed via peripheral nerves to the lateral line brainstem and from there to the midbrain torus semicircularis. Most prior electrophysiological studies of the lateral line were done under still-water conditions, even though natural environments encountered by fish include bulk-flow. Flow velocity and direction sensing are likely important to fish as they navigate variable, turbulent environments, but to date, only few studies have gathered information on the processing of bulk water flow by midbrain units. Here, we recorded from lateral line units in the torus semicircularis while presenting various bulk flow velocities in anterior-to-posterior and posterior-to-anterior flow directions. We studied (1) the temporal spike patterns of mechanosensory midbrain units, (2) the processing of bulk water flow velocity by these units, and (3) the processing of bulk water flow direction. We found that midbrain mechanosensory units alter their discharge rate during bulk water flow - some units responded to flow by increasing their discharge rate but did not vary this rate significantly with flow velocity, while others exhibited increasing discharge rates with increasing flow velocity. Units directly coding for flow direction were not found.

Responses of medullary lateral line units of the rudd, Scardinius erythrophthalmus, and the nase, Chondrostoma nasus, to vortex streets.

Fish use their mechanosensory lateral line amongst others for the detection of vortices shed by an upstream object and/or for the detection of vortices caused by the tail fin movements of another fish. Thus, vortices are one type of hydrodynamic stimuli to which fish are exposed in their natural environment. We investigated the responses of medullary lateral line units of common rudd, Scardinius erythrophthalmus, and common nase, Chondrostoma nasus (Cyprinidae), to water flow (9.5-13.3 cm-1) that contained vortices (a Kármán vortex street) shed by an upstream cylinder (diameter 2cm). The distance between the cylinder and the tip of the fish's snout varied between 8 and 24cm. 21 out of 42 units (S. erythrophthalmus), respectively, 9 out of 39 units (Chondrostoma nasus) responded to the vortices shed by the cylinder. Up to a cylinder distance of 24cm, interburst intervals revealed the vortex shedding frequency, i.e., burst frequency was similar to or identical with the vortex shedding frequency.

Medullary lateral line units of rudd, Scardinius erythrophthalmus, are sensitive to Kármán vortex streets.

We investigated the responses of medullary lateral line units of the rudd, Scardinius erythrophthalmus, to bulk water flow (7cms(-1)) and to water flow that contained vortices shed by an upstream half cylinder (diameter 1, 2, and 3cm). Thirty-five percent of the medullary units either increased or decreased their discharge rate with the increasing cylinder diameter. In some units, the spike patterns revealed the vortex shedding frequency, i.e., in these units the amplitude of spike train frequency spectra was similar or identical to the vortex shedding frequency.

Anterior lateral line nerve encoding to tones and play back vocalisations in free swimming oyster toadfish, Opsanus tau

In the underwater environment, sound propagates both as a pressure wave and as particle motion, with particle motion dominating close to the source. At the receptor level, the fish ear and the neuromast hair cells act as displacement detectors, and both are potentially stimulated by the particle motion component of sound. The encoding of the anterior lateral line nerve to acoustic stimuli in freely behaving oyster toadfish, Opsanus tau, was examined. Nerve sensitivity and directional responses were determined using spike rate and vector strength analysis, a measure of phase-locking of spike times to the stimulus waveform. All units showed greatest sensitivity to 100 Hz stimulus. While sensitivity was independent of stimuli orientation, the neuron's ability to phase-lock was correlated with stimuli origin. Two different types of units were classified, type 1 (tonic), and type 2 (phasic). The type 1 fibres were further classified into two sub-types based on their frequency response (type 1-1 and type 1-2), which was hypothesised to be related to canal (type 1-1) and superficial (type 1-2) neuromast innervation. Lateral line units also exhibited sensitivity and phase locking to boatwhistle vocalisations, with greatest spike rates exhibited at the onset of the call. These results provide direct evidence that oyster toadfish can use their lateral line to detect behaviourally relevant acoustic stimuli, which could provide a sensory pathway to aid in sound source localisation.

Toral lateral line units of goldfish, Carassius auratus, are sensitive to the position and vibration direction of a vibrating sphere

We recorded the responses of lateral line units in the midbrain torus semicircularis of goldfish, Carassius auratus, to a 50-Hz vibrating sphere and determined the unit's spatial receptive fields for various distances between fish and sphere and for different directions of sphere vibration. All but one unit responded to the vibrating sphere with an increase in discharge rate. Only a proportion (25%) of the units exhibited phase-locked responses. Receptive fields were narrow or broad and contained one, two or more areas of increased discharge rate. The data show that the receptive fields of toral lateral line units are in many respects similar to those of brainstem units but differ from those of afferent nerve fibres. The responses of primary afferents represent the pressure gradient pattern generated by a vibrating sphere and provide information about sphere location and vibration direction. Across the array of lateral line neuromasts, the fish brain in principle can derive this information. Nevertheless, toral units tuned to a distinct sphere location or sensitive to a distinct sphere vibration direction were not found. Therefore, it is conceivable that the torus semicircularis uses a population code to determine spatial location and vibration direction of a vibrating sphere.

Two-dimensional receptive fields of midbrain lateral line units in the goldfish, Carassius auratus

We determined the receptive fields of midbrain lateral line units in goldfish, Carassius auratus, with a 50Hz vibrating sphere placed at various azimuths and elevations alongside the fish and studied how responses were affected by different directions of sphere vibration. The receptive fields of toral lateral line units, in contrast to those of primary afferent nerve fibers, did not represent the pressure gradient pattern generated by a vibrating sphere. Thus, unlike primary afferents, single toral lateral line units did not code for source location in their spatial discharge patterns. The two-dimensional receptive fields were round, horizontally or vertically stretched, or complex. While some toral lateral line units were sensitive to the direction of sphere vibration others were not.

Responses of brainstem lateral line units to different stimulus source locations and vibration directions

We recorded responses of lateral line units in the medial octavolateralis nucleus in the brainstem of goldfish, Carassius auratus, to a 50Hz vibrating sphere and studied how responses were affected by placing the sphere at various locations alongside the fish and by different directions of vibration. In most units (88%), stimulation with the sphere from one or more spatial locations caused an increase and/or decrease in discharge rate. In few units (10%), discharge rate was increased by stimulation from one location and decreased by stimulation from an adjacent location in space. In a minority of the units (2%), changing sphere location did not affect discharge rates but caused a change in phase coupling. Units sensitive to a distinct sphere vibration direction were not found. The data also show that the responses of most brainstem units differ from those of primary afferent nerve fibers. Whereas primary afferents represent the pressure gradient pattern generated by the sphere and thus encode location and vibration direction of a vibrating sphere, most brainstem units do not. This information may be represented in the brainstem by a population code or in higher centers of the ascending lateral line pathway.

Responses of Medullary Lateral Line Units of the Goldfish,Carassius auratus, to Amplitude-Modulated Sinusoidal Wave Stimuli

This paper describes the responses of brainstem lateral line units in goldfish,Carassius auratus, to constant-amplitude and to amplitude-modulated sinusoidal water motions. If stimulated with constant-amplitude sinusoidal water motions, units responded with phasic (50%) or with sustained (50%) increases in dicharge rate. Based on isodisplacement curves, units preferred low (33 Hz, 12.5%), mid (50 Hz, 10% and 100 Hz, 30%) or high (200 Hz, 47.5%) frequencies. In most units, responses were weakly phase locked to the carrier frequency. However, at a carrier frequency of 50 Hz or 100 Hz, a substantial proportion of the units exhibited strong phase locking. If stimulated with amplitude-modulated water motions, units responded with a burst of discharge to each modulation cycle, that is, units phase locked to the amplitude modulation frequency. Response properties of brainstem units were in many respects comparable to those of midbrain units, suggesting that they emerge first in the lateral line brainstem.

Lateral line units in the amphibian brain could integrate wave curvatures

Aquatic predators like Xenopus laevis exploit mechano-sensory lateral lines to localise prey on the water surface by its wave emissions. In terms of distance, hypothetically, the source of a concentric wave could be centrally represented based on wave curvatures: for Xenopus, we present a first sample of 98 extracellularly recorded brainstem and midbrain responses to waves with curvatures ranging from 22.2-11.1 m(-1). At the frog, concurrently, wave amplitudes and their spectral composition were kept stable. Notably, 61% of 98 units displayed curvature-dependent spike rates, suggesting that wave curvatures could support an extraction of source distances in the amphibian brain.

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.

Effects of Running Water on Lateral Line Responses to Moving Objects

We investigated in goldfish, Carassius auratus, and trout, Oncorhynchus mykiss, how running water affects the responses of afferent fibers in the posterior lateral line nerve and of lateral line units in the brainstem medial octavolateralis nucleus to an object that is moved from anterior to posterior or opposite along the side of the fish. In still water, nerve fibers in both species responded to the moving object with alternating periods of increased and decreased firing rate. Most fibers in goldfish but none in trout discharged bursts of spikes in response to the object’s wake. Responses of brainstem units were more variable and less distinct than nerve fiber responses. Bursting activity in response to the object’s wake was found in only one brainstem unit. In running water, responses of goldfish nerve fibers were weaker than in still water. This effect was independent of object motion direction. Responses of trout fibers were weaker when the object was moved with the flow but were slightly stronger when the object was moved against the flow. In general, running water affected the responses of goldfish nerve fibers more strongly than the responses of trout fibers. Compared to still water, brainstem units in both species responded more weakly when the object was moved with the flow. When the object was moved against the flow, brainstem responses were on average comparable to those in still water. Measurements of changes in pressure and water velocity caused by the moving object indicate that the observed effects can largely be explained by peripheral hydrodynamic effects. However, physiological differences between goldfish and trout units indicate that the lateral line systems in these two species are adapted to different hydrodynamic conditions.

RESPONSES OF PRIMARY AND SECONDARY LATERAL LINE UNITS TO DIPOLE STIMULI APPLIED UNDER STILL AND RUNNING WATER CONDITIONS

RESPONSES OF PRIMARY AND SECONDARY LATERAL LINE UNITS TO DIPOLE STIMULI APPLIED UNDER STILL AND RUNNING WATER CONDITIONS

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.

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.

Sensitivity of central units in the goldfish, Carassius auratus, to transient hydrodynamic stimuli.

This study describes the discharges of central units in the medulla of the goldfish, Carassius auratus, to hydrodynamic stimuli received by the lateral line. We stimulated the animal with a small object moving in the water and recorded activity of 85 medullary lateral line units in response to different motion directions and to various object distances, velocities, accelerations and sizes. All but one unit increased discharge rate when the moving object passed the fish laterally. Five response types were distinguished based on temporal patterns of unit responses. Ten units were recorded which encoded motion direction by different temporal discharge patterns. In general, discharge rates decreased when object distance was increased and when object speed was decreased. When object size was decreased, discharge rates decreased systematically in one group of units, but they were comparable for all but the smallest object tested in a second group of units. Units responded about equally well whether an object was moved at a constant velocity or was accelerated when it passed the fish. The data indicate that medullary lateral line units in the goldfish can encode motion direction but are not tuned to other aspects of an object moving in the water. The functional properties of units in the medulla of goldfish are similar to those reported for medullary units in the catfish Ancistrus sp., suggesting that the central mechanisms for processing complex hydrodynamic stimuli may be quite similar in fish species that occupy habitats with different hydrodynamic conditions.

Sensitivity of Central Units in the Goldfish, <i>Carassius auratus, </i>to Transient Hydrodynamic Stimuli (Part 2 of 2)

This study describes the discharges of central units in the medulla of the goldfish, <i>Carassius auratus, </i>to hydrodynamic stimuli received by the lateral line. We stimulated the animal with a small object moving in the water and recorded activity of 85 medullary lateral line units in response to different motion directions and to various object distances, velocities, accelerations and sizes. All but one unit increased discharge rate when the moving object passed the fish laterally. Five response types were distinguished based on temporal patterns of unit responses. Ten units were recorded which encoded motion direction by different temporal discharge patterns. In general, discharge rates decreased when object distance was increased and when object speed was decreased. When object size was decreased, discharge rates decreased systematically in one group of units, but they were comparable for all but the smallest object tested in a second group of units. Units responded about equally well whether an object was moved at a constant velocity or was accelerated when it passed the fish. The data indicate that medullary lateral line units in the goldfish can encode motion direction but are not tuned to other aspects of an object moving in the water. The functional properties of units in the medulla of goldfish are similar to those reported for medullary units in the catfish <i>Ancistrus sp., </i>suggesting that the central mechanisms for processing complex hydrodynamic stimuli may be quite similar in fish species that occupy habitats with different hydrodynamic conditions.

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).

Integration of hydrodynamic information in the hindbrain of fishes

Fishes detect weak water movements generated by a predator or by prey with the aid of the mechanosensory lateral line. In this study, we investigated the way information received by the lateral line is processed by neurons in the hindbrain of two fish species, the bottom dwelling catfish, Ancistrussp., and the goldfish, Carassius auratus. We stimulated the lateral line with a small object moving in the water and recorded the responses of single units in the medulla. Medullary lateral line units increased their discharge rate when the moving object passed the fish. At least three different response types could be distinguished on the basis of response patterns. In some units, the response pattern differed for different motion directions, indicating that these units were sensitive for the direction of object motion. In general, discharge rates decreased both when object speed decreased or when object distance increased. The results suggest that in the hindbrain of fishes different neuron populations may be ...

Form and Function Relationships in Lateral Line Systems: Comparative Data from Six Species of Antarctic Notothenioid Fish

The structure and physiology of the anterior lateral line canal systems were studied in six species of fish belonging to two different families within the suborder of antarctic fish Notothenioidei. Many of the canals within the species belonging to the genus Trematomus are relatively straight sided tubes with diameters around 0.4 mm. Some of the canals in Trematomus, and most of the canals in the icefishes (family Channichthyidae) are more complex. Relatively small pores lead into large tubules, the walls of which appear partially membranous, and the canals not much more than constrictions between adjacent tubules. Dissostichus mawsoni, a large species, has canals with distinctive wide and narrow sections, 1.8 mm and 0.48 mm, respectively. Despite these morphological differences the frequency response characteristics of anterior lateral line units are remarkably similar in all six species. In the case of D. mawsoni, this functional similarity results from narrow sections of the canals, which provide the viscous resistance to flow that preserves the mechanical filtering properties of the canal despite the huge size difference between D. mawsoni and the other species. It is argued that the most appropriate way to view canals is as high pass filters which attenuate lower frequencies, and that this effect is best illustrated by comparing the frequency response characteristics of superficial and canal neuromasts using a sinusoidal stimulus that has a constant peak-to-peak velocity. The functional contribution of canals is to attenuate low frequencies and improve the signal-to-noise ratio for biologically important signals in the presence of low frequency noise produced, for example, by the animal's own movements.

Response Properties of Lateral Line and Auditory Units in the Medulla Oblongata of the Rainbow Trout (Oncorhynchus Mykiss)

ABSTRACT The objective of this study was to investigate the response properties of second-order lateral line and auditory neurones in the medulla oblongata of the rainbow trout. The frequency response of 20 medullary units was measured by recording single-unit spike activity in response to a mechanical stimulus provided by an oscillating membrane or by a small vibrating sphere. These 20 units were categorized, according to their frequency response properties, into two classes. Ten units responded to relatively low frequencies (&amp;lt;50Hz) and showed a maximum in the frequency response between 70 and 120Hz. The other units responded to higher frequencies, showing a maximum in the frequency response above 150Hz. Significant differences between these two classes were also observed with respect to recording site, latency and sensitivity. It is concluded that these two classes of medullary units are lateral line units and auditory units, respectively. In the medulla, the input from the two mechanosensory systems appears to be mainly processed separately. The majority of mechanically sensitive units (95%) showed a sustained, phase-locked response; 25% displayed a transient response component, mostly in addition to a sustained response component. All units were spontaneously active, with a mean firing rate of 27spikes s−1. Two units responded to a visual stimulus. No topographical representation of lateral line receptive fields was found in the caudal part of the medulla. The response characteristics of primary afferents reported in the literature differ from those of the medullary units of this study, so we conclude that the latter are higher-order units. Medullary lateral line units stimulated by the vibrating sphere appeared to be less sensitive than units stimulated by the vibrating membrane. The sensitivity of the units and the size of their receptive fields indicate that lateral line input converges in the medial nucleus.