Sensory ecology of the fish lateral-line system: Morphological and physiological adaptations for the perception of hydrodynamic stimuli.

Fishes are able to detect and perceive the hydrodynamic and physical environment they inhabit and process this sensory information to guide the resultant behaviour through their mechanosensory lateral-line system. This sensory system consists of up to several thousand neuromasts distributed across the entire body of the animal. Using the lateral-line system, fishes perceive water movements of both biotic and abiotic origin. The anatomy of the lateral-line system varies greatly between and within species. It is still a matter of debate as to how different lateral-line anatomies reflect adaptations to the hydrodynamic conditions to which fishes are exposed. While there are many accounts of lateral-line system adaptations for the detection of hydrodynamic signals in distinct behavioural contexts and environments for specific fish species, there is only limited knowledge on how the environment influences intra and interspecific variations in lateral-line morphology. Fishes live in a wide range of habitats with highly diverse hydrodynamic conditions, from pools and lakes and slowly moving deep-sea currents to turbulent and fast running rivers and rough coastal surf regions. Perhaps surprisingly, detailed characterisations of the hydrodynamic properties of natural water bodies are rare. In particular, little is known about the spatio-temporal patterns of the small-scale water motions that are most relevant for many fish behaviours, making it difficult to relate environmental stimuli to sensory system morphology and function. Humans use bodies of water extensively for recreational, industrial and domestic purposes and in doing so often alter the aquatic environment, such as through the release of toxicants, the blocking of rivers by dams and acoustic noise emerging from boats and construction sites. Although the effects of anthropogenic interferences are often not well understood or quantified, it seems obvious that they change not only water quality and appearance but also, they alter hydrodynamic conditions and thus the types of hydrodynamic stimuli acting on fishes. To date, little is known about how anthropogenic influences on the aquatic environment affect the morphology and function of sensory systems in general and the lateral-line system in particular. This review starts out by briefly describing naturally occurring hydrodynamic stimuli and the morphology and neurobiology of the fish lateral-line system. In the main part, adaptations of the fish lateral-line system for the detection and analysis of water movements during various behaviours are presented. Finally, anthropogenic influences on the aquatic environment and potential effects on the fish lateral-line system are discussed.

Adaptive responses of peripheral lateral line nerve fibres to sinusoidal wave stimuli.

Sensory adaptation is characterized by a reduction in the firing frequency of neurons to prolonged stimulation, also called spike frequency adaptation. This has been documented for sensory neurons of the visual, olfactory, electrosensory, and auditory system both in response to constant-amplitude and to sinusoidal stimuli, but has thus far not been described systematically for the lateral line system. We recorded neuronal activity from primary afferent nerve fibres in the lateral line in goldfish in response to sinusoidal wave stimuli. Depending on stimulus characteristics, afferent fibre responses exhibited a distinct onset followed by a decline in firing rate to an apparent steady-state level, i.e., they exhibited adaptation. The degree of adaptation, measured as the percent decrease in firing rate between onset and steady-state, increased with stimulus amplitude and frequency and with increasing steepness of the rising flank of the stimulus. This may in part be due to the velocity and/or acceleration sensitivity of the lateral line receptors. The time course of the response decline, i.e., the time course of adaptation was best-fit by a power function. This is consistent with the previous studies on spike frequency adaptation in sensory afferents of weakly electric fish.

Smart Mechanical Dipole: a device for the measurement of sphere motion in behavioral and neurophysiological experiments.

Fluid motion and pressure fields induced by vibrating spheres are frequently used to investigate the function of biological mechanosensory systems and artificial sensors. The calibration of the sphere motion amplitude (displacement, velocity, acceleration), time course and vibration direction often demands expensive equipment. To mitigate this requirement, we have developed a high-quality, low-cost device that we term a 'Smart Mechanical Dipole'. It provides real-time measurement of sphere acceleration along three axes and can be used to obtain an accurate stimulation trace. We applied digital filtering to equalize the frequency response of the vibrating sphere, which also reduced unwanted amplitude and frequency changes in the hydrodynamic signal. In addition, we show that the angular orientation of the rod to which the sphere was attached, i.e. axial versus transverse, but not the immersion depth of the sphere affected sphere vibration behavior.

The lateral line receptor array of cyprinids from different habitats.

The lateral line system of teleost fishes consists of an array of superficial and canal neuromasts (CN). Number and distribution of neuromasts and the morphology of the lateral line canals vary across species. We investigated the morphology of the lateral line system in four diurnal European cyprinids, the limnophilic bitterling (Rhodeus sericeus), the indifferent gudgeon (Gobio gobio), and ide (Leuciscus idus), and the rheophilic minnow (Phoxinus phoxinus). All fish had lateral line canals on head and trunk. The total number of both, CN and superficial neuromasts (SN), was comparable in minnow and ide but was greater than in gudgeon and bitterling. The ratio of SNs to CNs for the head was comparable in minnow and bitterling but was greater in gudgeon and ide. The SN-to-CN ratio for the trunk was greatest in bitterling. Polarization of hair cells in CNs was in the direction of the canal. Polarization of hair cells in SNs depended on body area. In cephalic SNs, hair cell polarization was dorso-ventral or rostro-caudal. In trunk SNs, it was rostro-caudal on lateral line scales and dorso-ventral on other trunk scales. On the caudal fin, hair cell polarization was rostro-caudal. The data show that, in the four species studied here, number, distribution, and orientation of CNs and SNs cannot be unequivocally related to habitat.

Coping with flow: behavior, neurophysiology and modeling of the fish lateral line system.

With the mechanosensory lateral line fish perceive water motions relative to their body surface and local pressure gradients. The lateral line plays an important role in many fish behaviors including the detection and localization of dipole sources and the tracking of prey fish. The sensory units of the lateral line are the neuromasts which are distributed across the surface of the animal. Water motions are received and transduced into neuronal signals by the neuromasts. These signals are conveyed by afferent nerve fibers to the fish brain and processed by lateral line neurons in parts of the brainstem, cerebellum, midbrain, and forebrain. In the cerebellum, midbrain, and forebrain, lateral line information is integrated with sensory information from other modalities. The present review introduces the peripheral morphology of the lateral line, and describes our understanding of lateral line physiology and behavior. It focuses on recent studies that have investigated: how fish behave in unsteady flow; what kind of sensory information is provided by flow; and how fish use and process this information. Finally, it reports new theoretical and biomimetic approaches to understand lateral line function.

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.

The oscar, Astronotus ocellatus, detects and discriminates dipole stimuli with the lateral line system.

We studied the role of the lateral line system for detection and discrimination of dipole stimuli in the oscar, Astronotus ocellatus (Family Cichlidae), and determined detection thresholds in still water and frequency discrimination capabilities in still and turbulent water. Average detection threshold of six animals for a 100-Hz dipole stimulus was 0.0059 µm peak-to-peak water displacement at the surface of the fish. After inactivation of the neuromast receptor organs of the lateral line system with the antibiotic streptomycin, dipole detection was reduced, but recovered within 2-4 weeks. This suggests that the oscar relied strongly on hydrodynamic information received by the lateral line system. Five oscars learned to discriminate a 100-Hz stimulus from 70 Hz and lower frequencies. When turbulence was introduced into the experimental tank, fish were still able to discriminate 100 Hz from frequencies 70 Hz and lower indicating that frequency discrimination mediated by the lateral line system was not reduced in turbulent water.

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 50 Hz 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.

Goldfish and oscars have comparable responsiveness to dipole stimuli.

The relative roles of the fish lateral line and inner ear for the perception of hydrodynamic stimuli are poorly investigated. Here, we studied responsiveness to a 100 Hz vibrating sphere (dipole stimulus) of goldfish and oscars, two species that differ in peripheral lateral line morphology, inner ear morphology, mechanical linkage between inner ear and swim bladder, and inner ear sensitivity. We measured unconditioned dipole-evoked changes in breathing activity in still water and in the presence of a 5-cm s(-1) background flow. In still water, individuals from both species responded to sound pressure levels (SPLs) between 92 and 109 dB SPL re 1 microPa(RMS). Responsiveness was not affected by background flow or by temporary inactivation of the lateral line. The data suggest that fish with different lateral line and inner ear morphologies have similar sensitivities to vibrating sphere stimuli and can detect and respond to dipole sources equally well in still water and in moderate background flows. Moreover, behavioral responses were not dependent on a functional lateral line, suggesting that in this type of experiment, the inner ear is the dominant sense organ for the perception of hydrodynamic stimuli.

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.

Organization of the superficial neuromast system in goldfish, Carassius auratus.

Distribution, morphology, and orientation of superficial neuromasts and polarization of the hair cells within superficial neuromasts of the goldfish (Carassius auratus) were examined using fluorescence labeling and scanning electron microscopy. On each body side, goldfish have 1,800-2,000 superficial neuromasts distributed across the head, trunk and tail fin. Each superficial neuromast had about 14-32 hair cells that were arranged in the sensory epithelium with the axis of best sensitivity aligned perpendicular to the long axis of the neuromast. Hair cell polarization was rostro-caudal in most superficial neuromasts on trunk scales (with the exception of those on the lateral line scales), or on the tail fin. On lateral line scales, the most frequent hair cell polarization was dorso-ventral in 45% and rostro-caudal in 20% of the superficial neuromasts. On individual trunk scales, superficial neuromasts were organized in rows which in most scales showed similar orientations with angle deviations smaller than 45 degrees . In about 16% of all trunk scales, groups of superficial neuromasts in the dorsal and ventral half of the scale were oriented orthogonal to each other. On the head, most superficial neuromasts were arranged in rows or groups of similar orientation with angle deviations smaller than 45 degrees . Neighboring groups of superficial neuromasts could differ with respect to their orientation. The most frequent hair cell polarization was dorso-ventral in front of the eyes and on the ventral mandible and rostro-caudal below the eye and on the operculum.

Responses to dipole stimuli of anterior lateral line nerve fibres in goldfish, Carassius auratus, 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.

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.

Brainstem lateral line responses to sinusoidal wave stimuli in still and running water.

The fish lateral line consists of superficial and canal neuromasts. In still water, afferent fibers from both types of neuromast respond equally well to a sinusoidally vibrating sphere. In running water, responses to a vibrating sphere of fibers innervating superficial neuromasts are masked. In contrast, responses of fibers innervating canal neuromasts are barely altered. It is not known whether this functional subdivision of the peripheral lateral line is maintained in the brain. We studied the effect of running water on the responses to a 50 Hz vibrating sphere of single units in the medial octavolateralis nucleus (MON) in goldfish Carassius auratus. The MON is the first site of central processing of lateral line information. Three types of units were distinguished. Type I units (N=27) were flow-sensitive; their ongoing discharge rates either increased or decreased in running water, and as a consequence, responses of these units to the vibrating sphere were masked in running water. Type II units (N=7) were not flow-sensitive; their ongoing discharge rates were comparable in still and running water, so their responses to the vibrating sphere were not masked in running water. Type III units (N=7) were also not flow-sensitive, but their responses to the vibrating sphere were nevertheless masked in running water. Although interactions between the superficial and canal neuromast system cannot be ruled out, our data indicate that the functional subdivision of the lateral line periphery is maintained to a large degree at the level of the medial octavolateralis nucleus.

Responses of diencephalic neurons to sensory stimulation in the goldfish, Carassius auratus.

We studied the responses to sensory stimulation in two diencephalic areas, the central posterior nucleus of the dorsal thalamus (CP) and the anterior tuberal nucleus of the hypothalamus (TA). In both the CP and the TA, units sensitive to acoustic (500-Hz sound), hydrodynamic (25-Hz dipole stimulus), and visual (640-nm light flash) stimuli were found. In the CP, most units were unimodal and responded exclusively to visual stimulation. In contrast, in the TA, most units responded to more than one modality. The data suggest that the CP is primarily involved in the unimodal processing of sensory information, whereas the TA may be involved in multisensory integration.

Response properties of diencephalic neurons to visual, acoustic and hydrodynamic stimulation in the goldfish, Carassius auratus.

We studied the responses to sensory stimulation of three diencephalic areas, the central posterior nucleus of the dorsal thalamus, the anterior tuberal nucleus of the hypothalamus, and the preglomerular complex. Units sensitive to acoustic (500 Hz tone burst), hydrodynamic (25 Hz dipole stimulus) and visual (640 nm light flash) stimuli were found in both the central posterior and anterior tuberal nucleus. In contrast, unit responses or large robust evoked potentials confined to the preglomerular complex were not found. In the central posterior nucleus, most units were unimodal. Many units responded exclusively to visual stimulation and exhibited a variety of temporal response patterns to light stimuli. In the anterior tuberal nucleus of the hypothalamus, most units responded to more than one modality and showed a stronger response decrement to stimulus repetitions than units in the central posterior nucleus. Our data suggest that units in the central posterior nucleus are primarily involved in the unimodal processing of sensory information whereas units in the anterior tuberal nucleus of the hypothalamus may be involved in multisensory integration.