Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii)

Weakly electric fishes are nocturnal and orientate in the absence of vision by using their electrical sense. This enables them not only to navigate but also to perceive and recognize objects in complete darkness. They create an electric field around their bodies by producing electric signals with specialized electric organs. Objects within this field alter the electric current at electroreceptor organs, which are distributed over almost the entire body surface. During active electrolocation, fishes detect, localize and analyse objects by monitoring their self-produced electric signals. We investigated the ability of the mormyrid Gnathonemus petersii to perceive objects three-dimensionally in space. Within a range of about 12 cm, G. petersii can perceive the distance of objects. Depth perception is independent of object size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters (maximal slope and maximal amplitude) of the electrical image which each object projects onto the fish's skin. During active electrolocation, electric fishes cannot only locate objects in space but in addition can determine the three-dimensional shape of an object. Up to certain limits, objects are spontaneously categorized according to their shapes, but not according to their sizes or the materials of which they are made.     

Non-visual environmental imaging and object detection through active electrolocation in weakly electric fish

Weakly electric fish orient at night by employing active electrolocation. South American and African species emit electric signals and perceive the consequences of these emissions with epidermal electroreceptors. Objects are detected by analyzing the electric images which they project onto the animal’s electroreceptive skin surface. Electric images depend on size, distance, shape, and material of objects and on the morphology of the electric organ and the fish’s body. It is proposed that the mormyrid Gnathonemus petersii possesses two electroreceptive “foveae” at its Schnauzenorgan and its nasal region, both of which resemble the visual fovea in the retina of many animals in design, function, and behavioral use. Behavioral experiments have shown that G. petersii can determine the resistive and capacitive components of an object’s complex impedance in order to identify prey items during foraging. In addition, fish can measure the distance and three-dimensional shape of objects. In order to determine object properties during active electrolocation, the fish have to determine at least four parameters of the local signal within an object’s electric image: peak amplitude, maximal slope, image width, and waveform distortions. A crucial parameter is the object distance, which is essential for unambiguous evaluation of object properties.     

Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii.

Weakly electric fish use active electrolocation for orientation at night. They emit electric signals (electric organ discharges) which generate an electrical field around their body. By sensing field distortions, fish can detect objects and analyze their properties. It is unclear, however, how accurately they can determine the distance of unknown objects. Four Gnathonemus petersii were trained in two-alternative forced-choice procedures to discriminate between two objects differing in their distances to a gate. The fish learned to pass through the gate behind which the corresponding object was farther away. Distance discrimination thresholds for different types of objects were determined. Locomotor and electromotor activity during distance measurement were monitored. Our results revealed that all individuals quickly learned to measure object distance irrespective of size, shape or electrical conductivity of the object material. However, the distances of hollow, water-filled cubes and spheres were consistently misjudged in comparison with solid or more angular objects, being perceived as farther away than they really were. As training continued, fish learned to compensate for these 'electrosensory illusions' and erroneous choices disappeared with time. Distance discrimination thresholds depended on object size and overall object distance. During distance measurement, the fish produced a fast regular rhythm of EOD discharges. A mechanisms for distance determination during active electrolocation is proposed.     

Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii

Weakly electric fish use active electrolocation for orientation at night. They emit electric signals (electric organ discharges) which generate an electrical field around their body. By sensing field distortions, fish can detect objects and analyze their properties. It is unclear, however, how accurately they can determine the distance of unknown objects. Four Gnathonemus petersii were trained in two-alternative forced-choice procedures to discriminate between two objects differing in their distances to a gate. The fish learned to pass through the gate behind which the corresponding object was farther away. Distance discrimination thresholds for different types of objects were determined. Locomotor and electromotor activity during distance measurement were monitored. Our results revealed that all individuals quickly learned to measure object distance irrespective of size, shape or electrical conductivity of the object material. However, the distances of hollow, water-filled cubes and spheres were consistently misjudged in comparison with solid or more angular objects, being perceived as farther away than they really were. As training continued, fish learned to compensate for these 'electrosensory illusions' and erroneous choices disappeared with time. Distance discrimination thresholds depended on object size and overall object distance. During distance measurement, the fish produced a fast regular rhythm of EOD discharges. A mechanisms for distance determination during active electrolocation is proposed.     

Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation

Weakly electric fish can detect nearby objects and analyse their electric properties during active electrolocation. Four individuals of the South American gymnotiform fish Eigenmannia sp., which emits a continuous wave-type electric signal, were tested for their ability to detect capacitive properties of objects and discriminate them from resistive properties. For individual fish, capacitive values of objects had to be greater than 0.22–1.7 nF (`lower threshold') and smaller than 120–680 nF (`upper threshold') in order to be detected. The capacitive values of natural objects fall well within this detection range. All fish trained could discriminate unequivocally between capacitive and resistive object properties. Thus, fish perceive capacitive properties as a separate object quality. The effects of different types of objects on the locally occurring electric signals which stimulate electroreceptors during electrolocation were examined. Purely resistive objects altered mainly local electric organ discharge (EOD) amplitude, but capacitive objects with values between about 0.5 and 600 nF changed the timing of certain EOD parameters (phase-shift) and EOD waveform. A mechanism for capacitance detection in wave-type electric fish based on time measurements is proposed and compared with the capacitance detection mechanism in mormyrid pulse-type fish, which is based on waveform measurements. Accepted: 31 July 1997     

Research on Location Characteristics and Algorithms based on Frequency Domain for a 2D Underwater Active Electrolocation Positioning System

Weakly electric fish has an ability to generate a low-frequency electric field actively to locate the surrounding object in complete darkness by sensing the change of the electric field.This ability is called active electrolocation.In this paper,we designed a two-dimensional (2D) experimental platform of underwater active electrolocation system by simulating weakly electric fish.On the platform,location characteristics based on frequency domain were investigated.Results indicated that surface shape of 3D location characteristic curves for the 2D underwater active electrolocation positioning system was convex upwards or concave down which was influenced by the material of probed objects and the frequency of the electric field excitation signal.Experiments also confirmed that the amplitude of the electric field excitation signal and the size of the probed object will only influence the amplitude corresponding to 3D location characteristic curves.Based on above location characteristics,we present three location algorithms including Cross Location Algorithm (CLA),Stochastic Location Algorithm (SLA) and Particle Swarm Optimization (PSO) location algorithm in frequency domain and achieved the task of the underwater positioning system.Our work may have reference value for underwater detection study.     

Biomimetic Sensors： Active Electrolocation of Weakly Electric Fish as a Model for Active Sensing in Technical Systems

Instead of vision, many nocturnal animals use alternative senses for navigation and object detection in their dark environment. For this purpose, weakly electric mormyrid fish employ active electrolocation, during which they discharge a specialized electric organ in their tail which discharges electrical pulses. Each discharge builds up an electrical field around the fish, which is sensed by cutaneous electroreceptor organs that are distributed over most of the body surface of the fish. Nearby objects distort this electrical field and cause a local alteration in current flow in those electroreceptors that are closest to the object. By constantly monitoring responses of its electroreceptor organs, a fish can detect, localize, and identify environmental objects.Inspired by the remarkable capabilities of weakly electric fish in detecting and recognizing objects, we designed technical sensor systems that can solve similar problems of remote object sensing. We applied the principles of active electrolocation to technical systems by building devices that produce electrical current pulses in a conducting medium (water or ionized gases) and simultaneously sense local current density. Depending on the specific task a sensor was designed for devices could (i) detect an object, (ii) localize it in space, (iii) determine its distance, and (iv) measure properties such as material properties, thickness, or material faults. Our systems proved to be relatively insensitive to environmental disturbances such as heat, pressure, or turbidity. They have a wide range of applications including material identification, quality control, non-contact distance measurements, medical applications and many more. Despite their astonishing capacities, our sensors still lag far behind what electric fish are able to achieve during active electrolocation. The understanding of the neural principles governing electric fish sensory physiology and the corresponding optimization of our sensors to solve certain technical tasks therefore remain ongoing goals of our research.     

Biomimetic Sensors: Active Electrolocation of Weakly Electric Fish as a Model for Active Sensing in Technical Systems

Instead of vision, many nocturnal animals use alternative senses for navigation and object detection in their dark environment. For this purpose, weakly electric mormyrid fish employ active electrolocation, during which they discharge a specialized electric organ in their tail which discharges electrical pulses. Each discharge builds up an electrical field around the fish, which is sensed by cutaneous electroreceptor organs that are distributed over most of the body surface of the fish. Nearby objects distort this electrical field and cause a local alteration in current flow in those electroreceptors that are closest to the object. By constantly monitoring responses of its electroreceptor organs, a fish can detect, localize, and identify environmental objects.Inspired by the remarkable capabilities of weakly electric fish in detecting and recognizing objects, we designed technical sensor systems that can solve similar problems of remote object sensing. We applied the principles of active electrolocation to technical systems by building devices that produce electrical current pulses in a conducting medium (water or ionized gases) and simultaneously sense local current density. Depending on the specific task a sensor was designed for devices could (i) detect an object, (ii) localize it in space, (iii) determine its distance, and (iv) measure properties such as material properties, thickness, or material faults. Our systems proved to be relatively insensitive to environmental disturbances such as heat, pressure, or turbidity. They have a wide range of applications including material identification, quality control, non-contact distance measurements, medical applications and many more. Despite their astonishing capacities, our sensors still lag far behind what electric fish are able to achieve during active electrolocation. The understanding of the neural principles governing electric fish sensory physiology and the corresponding optimization of our sensors to solve certain technical tasks therefore remain ongoing goals of our research.     

Modeling the electric image produced by objects with complex impedance in weakly electric fish

Weakly electric fish generate an electric field around their body by electric organ discharge (EOD). By measuring the modulation of the electric field produced by an object in the field these fish are able to accurately locate an object. Theoretical and experimental studies have focused on the amplitude modulations of EODs produced by resistive objects. However, little is known about the phase modulations produced by objects with complex impedance. The fish must be able to detect changes in object impedance to discriminate between food and nonfood objects. To investigate the features of electric images produced by objects with complex impedance, we developed a model that can be used to map the electric field around the fish body. The present model allows us to calculate the spatial distribution of the amplitude and phase shift in an electric image. This is the first study to investigate the changes in amplitude and phase shift of electric images induced by objects with complex impedance in wave-type fish. Using the model, we show that the amplitude of the electric image exhibits a sigmoidal change as the capacitance and resistance of an object are increased. Similarly, the phase shift exhibits a significant change within the object capacitance range of 0.1–100 nF. We also show that the spatial distribution of the amplitude and phase shifts of the electric image resembles a “Mexican hat” in shape for varying object distances and sizes. The spatial distribution of the phase shift and the amplitude was dependent on the object distance and size. Changes in the skin capacitance were associated with a tradeoff relationship between the magnitude of the amplitude and phase shift of the electric image. The specific range of skin capacitance (1–100 nF) allows the receptor afferents to extract object features that are relevant to electrolocation. These results provide a useful basis for the study of the neural mechanisms by which weakly electric fish recognize object features such as distance, size, and impedance.     

Imaging of objects through active electrolocation in Gnathonemus petersii.

The weakly electric fish Gnathonemus petersii detects, localizes, and analyzes objects during active electrolocation even in complete darkness. This enables these fish to lead a nocturnal life and find and identify their prey (small insect larvae) on the ground of their freshwater habitat. During active electrolocation, fish produce a series of brief electric signals, electric organ discharges (EOD), with an electric organ in their tail. Each EOD builds up a stable electric field around the fish, which is distorted only by nearby objects. Field distortions lead to changes of the transepidermal electric current flow at a region of the fish's electroreceptive skin surface called the 'electric image'. Within the electric image, locally perceived EODs can be either altered in amplitude or waveform by an object. Fish measure both parameters to assess object properties, such as the capacitive and resistive components of the object's complex impedance. the object's size and shape, and its distance from the fish. None of these object properties can be evaluated in isolation, but have to be inferred during parallel processing of electric image spatial and qualitative parameters. Two anterior skin regions of G. petersii appear to possess particular properties for special electrolocation tasks and we therefore refer to them as 'foveal' regions. Because of its high electroreceptor density, the electric field geometry around it, and its behavioral use, the 'nasal region' between the nares and the mouth at the head of the fish is suggested to be a fovea for long-range guidance and object detection. We propose that the 'Schnauzenorgan', a long and flexible chin appendix covered densely with electroreceptor organs, is a second electroreceptive fovea associated with a short-range (food) identification system. Together, these two electric foveae constitute an effective prey detection and identification system.     

Mind the gap: the minimal detectable separation distance between two objects during active electrolocation

In a food‐rewarded two‐alternative forced‐choice procedure, it was determined how well the weakly electric elephantnose fish Gnathonemus petersii can sense gaps between two objects, some of which were placed in front of complex backgrounds. The results show that at close distances, G. petersii is able to detect gaps between two small metal cubes (2 cm × 2 cm × 2 cm) down to a width of c. 1·5 mm. When larger objects (3 cm × 3 cm × 3 cm) were used, gaps with a width of 2–3 mm could still be detected. Discrimination performance was better (c. 1 mm gap size) when the objects were placed in front of a moving background consisting of plastic stripes or plant leaves, indicating that movement in the environment plays an important role for object identification. In addition, the smallest gap size that could be detected at increasing distances was determined. A linear relationship between object distance and gap size existed. Minimal detectable gap sizes increased from c. 1·5 mm at a distance of 1 cm, to 20 mm at a distance of 7 cm. Measurements and simulations of the electric stimuli occurring during gap detection revealed that the electric images of two close objects influence each other and superimpose. A large gap of 20 mm between two objects induced two clearly separated peaks in the electric image, while a 2 mm gap caused just a slight indentation in the image. Therefore, the fusion of electric images limits spatial resolution during active electrolocation. Relative movements either between the fish and the objects or between object and background might improve spatial resolution by accentuating the fine details of the electric images.     

Size does not matter: size-invariant echo-acoustic object classification

Echolocating bats can not only extract spatial information from the auditory analysis of their ultrasonic emissions, they can also discriminate, classify and identify the three-dimensional shape of objects reflecting their emissions. Effective object recognition requires the segregation of size and shape information. Previous studies have shown that, like in visual object recognition, bats can transfer an echo-acoustic object discrimination task to objects of different size and that they spontaneously classify scaled versions of virtual echo-acoustic objects according to trained virtual-object standards. The current study aims to bridge the gap between these previous findings using a different class of real objects and a classification—instead of a discrimination paradigm. Echolocating bats (Phyllostomus discolor) were trained to classify an object as either a sphere or an hour-glass shaped object. The bats spontaneously generalised this classification to objects of the same shape. The generalisation cannot be explained based on similarities of the power spectra or temporal structures of the echo-acoustic object images and thus require dedicated neural mechanisms dealing with size-invariant echo-acoustic object analysis. Control experiments with human listeners classifying the echo-acoustic images of the objects confirm the universal validity of auditory size invariance. The current data thus corroborate and extend previous psychophysical evidence for sonar auditory-object normalisation and suggest that the underlying auditory mechanisms following the initial neural extraction of the echo-acoustic images in echolocating bats may be very similar in bats and humans.     

Linking active sensing and spatial learning in weakly electric fish

Weakly electric fish can learn the spatial layout of their environment using only their short-range electric sense. During spatial learning, active sensing motions are used to memorize landmark locations so that they can serve as anchors for idiothetic-based navigation. A hindbrain feedback circuit selectively amplifies the electrosensory input arising from these motions. The ascending electrolocation pathway preferentially transmits this information to the pallial regions involved in spatial learning and navigation. Similarities in both behavioral patterns and hindbrain circuitry of gymnotiform and mormyrid fish, two families that independently evolved their electrosense, suggest that amplification and transmission of active sensing motion inputs are fundamental mechanisms for spatial memory acquisition.     

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.     

The effects of simple objects on the electric field of Apteronotus

How might electric fish determine, from patterns of transdermal voltage changes, the size, shape, location, and impedance of a nearby object? I have investigated this question by measuring and simulating electric images of spheres and ellipsoids near an Apteronotus leptorhynchus. Previous studies have shown that this fish's electric field magnitude, and perturbations of the field due to objects, are complicated nonliner functions of distance from the fish. These functions become much simpler when distance is measured from the axes of symmetry of the fish and the object, instead of their respective edges. My analysis suggests the following characteristics of high frequency electric sense and electric images. 1. The shape of electric images on the fish's body is relatively independent of a spherical object's radius, conductivity, and rostrocaudal location. 2. An image's relative width increases linearly with lateral distance, and might therefore unambiguously encode object distance. 3. Only objects with very large dielectric constants cause appreciable phase shifts, and the degree of shift depends strongly on water conductivity. 4. Several parameters, such as the range of electric sense, may depend on the rostrocaudal location of an object. Large objects may be detectable further from the head than the tail, and conversely, small objects may be detectable further from the tail than head. 5. Asymmetrical objects produce different electric images, correlated with their cross-sections, for different orientations and phases of the electric field. 6. The steep attenuation with distance of the field magnitude causes spatial distortions in electric images, somewhat analogous to the perspective distortion inherent in wide angle optical lenses.     

Orientation in the dark: brain circuits involved in the perception of electric signals in mormyrid electric fish.

Weakly electric fish produce electric signals with a specialised organ in their tail. In addition, they are electrosensitive and can perceive their self-generated signals (for electrolocation) and electric signals of other electric fishes (for electrocommunication). Mormyrids possess three types of peripheral electroreceptor organs, one used for electrocommunication and two types involved in electolocation. They are innervated by afferent fibres, which project to different zones in the electrosensory lateral line lobe (ELL) in the medulla. Brain circuits for electrolocation and electrocommunication are separated almost throughout the whole brain. Electrolocation pathways run from the ELL-cortex to the torus semicircularis of the midbrain and then via the valvula cerebelli towards the telencephalon. Pathways involved in electrocommunication run from the nucleus of the ELL to another part of the torus and from there through the isthmic granule nucleus to the valvula. In addition, a pathway via the preglomerular complex to the telencephalon might exist. In both the electrolocation and the electrocommunication circuits, prominent recurrent pathways are present.     

Fish perform spatial pattern recognition and abstraction by exclusive use of active electrolocation

The field generated by the electric organ of weakly electric fish varies with the electrical properties of nearby objects. Correspondingly, current fluxes in this field differentially stimulate the electroreceptors in the fish's skin. Thus, resistors are to conductors and insulators as gray is to black and white in optics. Additionally, the capacitances of plants and insect larvae contrast with those of water or stones, giving effects comparable to "coloration". Receptors arrayed over a large area of the skin act like a retina upon which the discharge projects "electric images". By further central processing, the fish also discriminate between objects according to their composition, size, or distance, a procedure termed "electrolocation", analogous to echolocation in bats. Here we demonstrate that G. petersii and S. macrurus can also recognize 3D orientations and configurations and extract and generalize spatial features solely with their electrical sense. We presented fish with virtual electrical "objects" formed from electrodes set flush in the inner surface of a Y maze with various patterns of external connectivity. With reward and aversion training, the fish could recognize similar electrode configurations and extract a feature, e.g., a vertical connectivity, present in various novel configurations. Previously, shape recognition has only been shown in electrolocating fish when they are in full mechanical contact with solid objects.     

Electrolocation of Capacitive Objects in Four Species of Pulse-type Weakly Electric Fish I. Discrimination Performance

The great variety of species-typical electric signals (electric organ discharges, EOD) emitted by weakly electric mormyrid fish might be the result of evolutionary pressures stemming from the two main functions of the electro-sensory-motor system: electrocommunication and electrolocation. Employing a conditioned discrimination task we tested four species of mormyrids, emitting EODs differing in waveform, for their ability to detect capacitive properties of objects during electrolocation. Each fish could discriminate capacitive objects within a certain range of capacitive values, which was species specific. The upper and lower limits (upper and lower thresholds) of this detectable range were determined for each fish. In fish species emitting long duration EODs composed of mainly low spectral frequencies both the lower and the upper thresholds were shifted to larger capacitive values compared to fish species emitting shorter EODs. The upper limit of the detectable range was much more variable between species than the lower limit, which was relatively low in all fish. We interpret this as an adaptation of mormyrids to detect small capacitive objects, for example food items. All mormyrids could discriminate between a resistive object and a capacitive object even if the complex impedances of the two objects were identical. This implies that the fish are highly sensitive to small waveform distortions of their self produced EODs.     

Modeling signal and background components of electrosensory scenes

Weakly electric fish are able to detect and localize prey based on microvolt-level perturbations in the fishs self-generated electric field. In natural environments, weak prey-related signals are embedded in much stronger electrosensory background noise. To better characterize the signal and background components associated with natural electrolocation tasks, we recorded transdermal voltage modulations in restrained Apteronotus albifrons in response to moving spheres, tail bends, and large nonconducting boundaries. Spherical objects give rise to ipsilateral images with center-surround structure and contralateral images that are weak and diffuse. Tail bends and laterally placed nonconducting boundaries induce relatively strong ipsilateral and contralateral modulations of opposite polarity. We present a computational model of electric field generation and electrosensory image formation that is able to reproduce the key features of these empirically measured signal and background components in a unified framework. The model comprises an array of point sources and sinks distributed along the midline of the fish, which can conform to arbitrary body bends. The model is computationally fast and can be used to estimate the spatiotemporal pattern of activation across the entire electroreceptor array of the fish during natural behaviors.     

Electric images of two low resistance objects in weakly electric fish

Electroreceptive fish detect nearby objects by processing the information contained in the pattern of electric currents through their skin. In weakly electric fish, these currents arise from a self-generated field (the electric organ discharge), depending on the electrical properties of the surrounding medium. The electric image can be defined as the pattern of transepidermal voltage distributed over the receptive surface. To understand electrolocation it is necessary to know how electric image of objects are generated. In pulse mormyrids, the electric organ is localized at the tail, far from the receptors and fires a short biphasic pulse. Consequently, if all the elements in the environment are resistive, the stimulus at every point on the skin has the same waveform. Then, any measure of the amplitude (for example, the peak to peak amplitude) could be the unique parameter of the stimulus at any point of the skin. We have developed a model to calculate the image, corroborating that images are spread over the whole sensory surface and have an opposite center-surround, "Mexican-hat" shape. As a consequence, the images of different objects superimpose. We show theoretically and by simulation that the image of a pair of objects is not the simple addition of the individual images of these objects.