Jacob Engelmann

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.

Electrifying love: electric fish use species-specific discharge for mate recognition

Mate choice is mediated by a range of sensory cues, and assortative mating based on these cues can drive reproductive isolation among diverging populations. A specific feature of mormyrid fish, the electric organ discharge (EOD), is used for electrolocation and intraspecific communication. We hypothesized that the EOD also facilitates assortative mating and ultimately promotes prezygotic reproductive isolation in African weakly electric fishes. Our behavioural experiments using live males as well as EOD playback demonstrated that female mate recognition is influenced by EOD signals and that females are attracted to EOD characteristics of conspecific males. The dual function of the EOD for both foraging and social communication (including mate recognition leading to assortative mating) underlines the importance of electric signal differentiation for the divergence of African weakly electric fishes. Thus, the EOD provides an intriguing mechanism promoting trophic divergence and reproductive isolation between two closely related Campylomormyrus species occurring in sympatry in the lower Congo rapids.

Object localization through the lateral line system of fish: theory and experiment

Fish acquire information about their aquatic environment by means of their mechanosensory lateral-line system. This system consists of superficial and canal neuromasts that sense perturbations in the water surrounding them. Based on a hydrodynamic model presented here, we propose a mechanism through which fish can localize the source of these perturbations. In doing so we include the curvature of the fish body, a realistic lateral line canal inter-pore distance for the lateral-line canals, and the surface boundary layer. Using our model to explore receptor behavior based on experimental data of responses to dipole stimuli we suggest that superficial and canal neuromasts employ the same mechanism, hence provide the same type of input to the central nervous system. The analytical predictions agree well with spiking responses recorded experimentally from primary lateral-line nerve fibers. From this, and taking into account the central organization of the lateral-line system, we present a simple biophysical model for determining the distance to a source.

3-Dimensional Scene Perception during Active Electrolocation in a Weakly Electric Pulse Fish.

Weakly electric fish use active electrolocation for object detection and orientation in their environment even in complete darkness. The African mormyrid Gnathonemus petersii can detect object parameters, such as material, size, shape, and distance. Here, we tested whether individuals of this species can learn to identify 3-dimensional objects independently of the training conditions and independently of the objects position in space (rotation-invariance; size-constancy). Individual G. petersii were trained in a two-alternative forced-choice procedure to electrically discriminate between a 3-dimensional object (S+) and several alternative objects (S−). Fish were then tested whether they could identify the S+ among novel objects and whether single components of S+ were sufficient for recognition. Size-constancy was investigated by presenting the S+ together with a larger version at different distances. Rotation-invariance was tested by rotating S+ and/or S− in 3D. Our results show that electrolocating G. petersii could (1) recognize an object independently of the S− used during training. When only single components of a complex S+ were offered, recognition of S+ was more or less affected depending on which part was used. (2) Object-size was detected independently of object distance, i.e. fish showed size-constancy. (3) The majority of the fishes tested recognized their S+ even if it was rotated in space, i.e. these fishes showed rotation-invariance. (4) Object recognition was restricted to the near field around the fish and failed when objects were moved more than about 4 cm away from the animals. Our results indicate that even in complete darkness our G. petersii were capable of complex 3-dimensional scene perception using active electrolocation.

Neural responses of goldfish lateral line afferents to vortex motions

SUMMARY The lateral line system of fish is sensitive to weak water motions. We recorded from posterior lateral line nerve afferents while stimulating goldfish, Carassius auratus, with unidirectional water flow and with a vortex ring. Posterior lateral line afferents of goldfish were either flow sensitive or flow insensitive. Both types of afferents responded to a vortex ring that passed the fish laterally with one to three reproducible patterns of neural activity, followed by activity patterns that were less reproducible. Using particle image velocimetry, we visualized and quantified the water motions in the vertical plane next to the surface of the fish while recording from lateral line afferents. Early response components correlated with the direction of water motions that occurred at the position of the neuromast recorded from. By contrast, neural activity that occurred after the vortex had passed the fish barely predicted the direction of water motions. These results are in agreement with the known directional sensitivity of hair cells and indicate that fish might be able to extract sensory information from complex stimuli like vortices by comparing the activity of a whole array of neuromasts. The stimulus used in this study is novel to lateral line research and resembles some of the hydrodynamic stimuli that fish might encounter in their natural environments. We expect that by combining naturalistic hydrodynamic stimuli and central nervous recordings, we will learn if and how hydrodynamic feature detection is accomplished by the lateral line system.

Active sensing in a mormyrid fish: electric images and peripheral modifications of the signal carrier give evidence of dual foveation.

SUMMARY Weakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation, nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance, can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response (novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions – the Schnauzenorgan and the nasal region – can be termed electric fovea but they serve separate functions during active electrolocation.

Functional Foveae in an Electrosensory System

Several species of Mormyrid weakly electric fish have a mobile chin protuberance that serves as a mobile antenna during prey detection, tracking behaviors, and foraging for food. It has been proposed that it constitutes a fovea of the electrosensory system. The distribution of the three types of receptor organs involved in active imaging of the local surroundings, prey detection, and passive electroreception, and their central projection to the electrosensory lobe (ELL), have been studied in Gnathonemus petersii. Density distributions were compared for different body regions. Primary afferent projections were labeled with biocytin or biotinylated dextrans. This showed that there is considerable central “over‐representation” of the mandibular and nasal regions of the sensory surface involved in electrolocation, at the expense of the other body regions investigated. This over‐representation is not a mere effect of the very high density of receptor organs in these areas, but is found to be due to central magnification. This magnification differs between the subclasses of electroreceptors, suggesting a functional segregation in the brain. We conclude that the chin protuberance and the nasal region are the regions of greatest sensitivity for the resistive, capacitive, and low‐frequency characteristics of the environment, and are probably most important in prey detection, whereas other regions of the skin with a lesser resolution and sensitivity to phase distortion of the EOD, in particular the trunk, are probably designed for imaging larger, inanimate features of the environment. Our data support the hypothesis that the chin appendage and nasal region are functionally distinct electrosensory foveae. J. Comp. Neurol. 511:342–359, 2008.

Photonic crystal light collectors in fish retina improve vision in turbid water.

Seeing in the Dark Elephantnose fish are known to use electrosensing to navigate their murky freshwater environment. However, unlike some other animals from dark environments, they have retained their eyes and some dependence on vision. While most vertebrate vision optimizes either photon catch (for increased light capture) or visual acuity, Kreysing et al. (p. 1700) show that the unique structures of the grouped retinae found in the eyes of this species matches rod and cone sensitivity, which allows for the simultaneous use of both types of photoreceptors over a large range of dim light intensities. Layering cones on top of rods allows the elephantnose fish to see low-contrast objects in a murky environment. Despite their diversity, vertebrate retinae are specialized to maximize either photon catch or visual acuity. Here, we describe a functional type that is optimized for neither purpose. In the retina of the elephantnose fish (Gnathonemus petersii), cone photoreceptors are grouped together within reflecting, photonic crystal–lined cups acting as macroreceptors, but rod photoreceptors are positioned behind these reflectors. This unusual arrangement matches rod and cone sensitivity for detecting color-mixed stimuli, whereas the photoreceptor grouping renders the fish insensitive to spatial noise; together, this enables more reliable flight reactions in the fish’s dim and turbid habitat as compared with fish lacking this retinal specialization.

Electric imaging through active electrolocation: implication for the analysis of complex scenes

The electric sense of mormyrids is often regarded as an adaptation to conditions unfavourable for vision and in these fish it has become the dominant sense for active orientation and communication tasks. With this sense, fish can detect and distinguish the electrical properties of the close environment, measure distance, perceive the 3-D shape of objects and discriminate objects according to distance or size and shape, irrespective of conductivity, thus showing a degree of abstraction regarding the interpretation of sensory stimuli. The physical properties of images projected on the sensory surface by the fish’s own discharge reveal a “Mexican hat” opposing centre-surround profile. It is likely that computation of the image amplitude to slope ratio is used to measure distance, while peak width and slope give measures of shape and contrast. Modelling has been used to explore how the images of multiple objects superimpose in a complex manner. While electric images are by nature distributed, or ‘blurred” behavioural strategies orienting sensory surfaces and the neural architecture of sensory processing networks both contribute to resolving potential ambiguities. Rostral amplification is produced by current funnelling in the head and chin appendage regions, where high density electroreceptor distributions constitute foveal regions. Central magnification of electroreceptive pathways from these regions particularly favours the detection of capacitive properties intrinsic to potential living prey. Swimming movements alter the amplitude and contrast of pre-receptor object-images but image modulation is normalised by central gain-control mechanisms that maintain excitatory and inhibitory balance, removing the contrast-ambiguity introduced by self-motion in much the same way that contrast gain-control is achieved in vision.

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.