Joachim Mogdans

Hydrodynamic stimuli and the fish lateral line.

Sensory systems need to distinguish biologically relevant stimuli from background noise. Here we investigate how the lateral-line mechanosensory system of the fish senses minute water motions in the vicinity while exposed to running water. We find that one class of receptor in the lateral line, the canal neuromasts, can respond to hydrodynamic stimuli even in the presence of unidirectional water flow, whereas superficial neuromasts, which predominate in still-water fish, cannot.

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°. 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°. 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. J. Morphol., 2008.

TRANSFORMATION OF PERIPHERAL INPUTS BY THE FIRST-ORDER LATERAL LINE BRAINSTEM NUCLEUS

Abstract Extracellular recording techniques were used to record the responses of medial nucleus cells and posterior lateral line nerve fibers in mottled sculpin, Cottus bairdi, and goldfish, Carassius auratus, to a 50-Hz dipole source (vibrating sphere). Responses were characterized in terms of (1) receptive fields that relate responsiveness (spike rate and phase-locking) to the location of the source along the length of the fish, (2) input-output functions that relate responsiveness to vibration amplitude for a fixed source location, and (3) peri-stimulus time histograms that relate responsiveness to time during a sustained period of vibration. Relative to posterior lateral line nerve fibers, medial nucleus cells in both species were similar in showing (1) lower spontaneous and evoked rates of spike activity, (2) greater degrees of adaptation, (3) greater heterogeneity in all response characteristics, and (4) evidence for inhibitory/excitatory interactions. Whereas receptive fields of nerve fibers in both species faithfully reflect both pressure gradient amplitudes (with rate changes) and directions (with phase-angle changes) in the stimulus field, receptive fields of medial nucleus were more difficult to relate to the stimulus field. Some, but not all, receptive fields could be modeled with excitatory center/inhibitory surround and inhibitory center/excitatory surround organizations.

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.

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.

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.

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.

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.

Flow Sensing in Air and Water

Aquatic animals of all major phyla have developed sensory systems to perceive water movements, so-called hydrodynamic sensory systems. These water movements, or hydrodynamic stimuli, arise from a variety of sources. Some sources of hydrodynamic stimuli are biotic, such as predators, prey, and conspecifics, some are abiotic, such as wind, gravity that induces currents, and others. We have only relatively recently begun to take a closer look at these hydrodynamic stimuli with regard to the question how they may have formed the hydrodynamic sensory systems of aquatic animals during evolution. Hydrodynamic stimuli are measured with several different techniques, some of which are invasive, meaning that a sensor is inserted into the flow, some are noninvasive, such as optical and acoustical techniques. The laser-based technique of particle image velocimetry (PIV) has proven especially helpful. It is an optical technique that measures flow velocities not only in a single point, but simultaneously in hundreds or thousands of points in a selected layer of the fluid, and with more advanced modifications of the technique, even in a limited volume. Furthermore, the laser-based technique of laser Doppler velocimetry has contributed much to our understanding. In this chapter, naturally occurring hydrodynamic stimuli measured with these and other techniques are discussed, along with the advantages and shortcomings of the different experimental approaches.

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.