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.     

Behavioral detection of electric signal waveform distortion in the weakly electric fish,Gnathonemus petersii

The novelty response of weakly electric mormyrids is a transient acceleration of the rate of electric organ discharges (EOD) elicited by a change in stimulus input. In this study, we used it as a tool to test whether Gnathonemus petersii can perceive minute waveform distortions of its EOD that are caused by capacitive objects, as would occur during electrolocation. Four predictions of a hypothesis concerning the mechanism of capacitance detection were tested and confirmed: (1) G. petersii exhibited a strong novelty response to computer-generated (synthetic) electric stimuli that mimic both the waveform and frequency shifts of the EOD caused by natural capacitive objects (Fig. 3). (2) Similar responses were elicited by synthetic stimuli in which only the waveform distortion due to phase shifting the EOD frequency components was present (Fig. 4). (3) Novelty responses could reliably be evoked by a constant amplitude phase shifted EOD that effects the entire body of the fish evenly, i.e., a phase difference across the body surface was lacking (Figs. 3, 4). (4) Local presentation of a phase-shifted EOD mimic that stimulated only a small number of electroreceptor organs at a single location was also effective in eliciting a behavioral response (Fig. 5).Our results indicate that waveform distortions due to phase shifts alone, i.e. independent of amplitude or frequency cues, are sufficient for the detection of capacitive, animate objects. Mormyrids perceive even minute waveform changes of their own EODs by centrally comparing the input of the two types of receptor cells within a single mormyromast electroreceptor organ. Thus, no comparison of differentially affected body regions is necessary. This shows that G. petersii indeed uses a unique mechanism for signal analysis, which is different from the one employed by gymnotiform wavefish.Abbreviations EOD electric organ discharge - p-p-amplitude peak-to-peak amplitude     

Short-range Navigation of the Weakly Electric Fish,Gnathonemus petersii L. (Mormyridae,Teleostei), in Novel and Familiar Environments

We investigated the electrolocation performance of the weakly electric fish, Gnathonemus petersii, in novel and familiar environments. By selectively interfering with the fish's sensory input, we determined the sensory channels necessary for navigation and orientation. The fish's task was to locate a circular aperture (diameter: 64 mm) in a wall dividing a 200–1 aquarium into two equal compartments. To assess the fish's performance, we measured (1) the time it took the fish to locate the aperture, (2) the height at which it contacted the divider, (3) its electric organ discharge rate, and (4) the frequency of divider crossings. In the first experiment (novel environment), 50 naive G. petersii assigned to five groups of 10 fish each (intact, blind, electrically “silent,” blind and “silent,” and shamoperated animals) were tested with the aperture presented randomly in one of three positions (aperture center: 7.6, 17.7, 27.8 cm from the bottom). In a novel environment, G. petersii depend on active electrolocation. Despite the changing aperture position, over the 15 trials, fish with a functioning electric organ found the aperture, whereas those without one did not. The electric organ discharge rate was inversely correlated with the amount of time spent searching for the aperture. In a second experiment (familiar environment) 20 intact fish learned the position of a fixed aperture. When we subsequently denervated the electric organ in 10 of these animals, their performance did not differ significantly from that of their conspecifics. Thus, once the fish were familiar with the aperture's position, they no longer depended on active electrolocation. We interpret and discuss this behavior as evidence for a “central expectation” and discuss its possible role in electronavigation.     

Phase and amplitude maps of the electric organ discharge of the weakly electric fish,Apteronotus leptorhynchus

Summary The electric organ discharge (EOD) potential was mapped on the skin and midplane of several Apteronotus leptorhynchus. The frequency components of the EOD on the surface of the fish have extremely stable amplitude and phase. However, the waveform varies considerably with different positions on the body surface. Peaks and zero crossings of the potential propagate along the fish's body, and there is no point where the potential is always zero. The EOD differs significantly from a sinusoid over at least one third of the body and tail. A qualitative comparison between fish showed that each individual had a unique spatiotemporal pattern of the EOD potential on its body.The potential waveforms have been assembled into high temporal and spatial resolution maps which show the dynamics of the EOD. Animation sequences and Macintosh software are available by anonymous ftp (mordor.cns.caltech.edu; cd/pub/ElectricFish).We interpret the EOD maps in terms of ramifications on electric organ control and electroreception. The electrocytes comprising the electric organ do not all fire in unison, indicating that the command pathway is not synchronized overall. The maps suggest that electroreceptors in different regions fulfill different computational roles in electroreception. Receptor mechanisms may exist to make use of the phase information or harmonic content of the EOD, so that both spatial and temporal patterns could contribute information useful for electrolocation and communication.Abbreviations EOD electric organ discharge - EO electric organ - CV coefficient of variance     

Dim light vision – Morphological and functional adaptations of the eye of the mormyrid fish, Gnathonemus petersii

The African weakly electric fish Gnathonemus petersii is well known for its electrosensory capabilities. These animals can detect and distinguish objects through active electrolocation in complete darkness. Because of their nocturnal lifestyle, a low contribution of vision for orientation and object detection has been expected. However, as we show in this review, the retina of G. petersii is highly specialized with hundreds of rods and tens of cones grouped together in bundles in a complex way, ensheathed by a tapetum lucidum. The structure of the bundles goes beyond what would be expected if only photon catch was supposed to be increased. During daytime, the structure of these “macro-receptors” changes dramatically depending on retinomotor movements. During the day, the rods and cones are located in different compartments of the bundle, separated by a narrow canal in the form of a “bottle neck”. Investigations on cell structure and neurochemistry in the retina indicate a general organization that is simpler in terms of bipolar and ganglion cell diversity than in tetrachromatic species such as goldfish, yet similar in terms of neurochemical differentiation of amacrine cells. In both respects, the inner retina of the elephantnose fish bears the greatest similarity to catfish and some deep-sea fish retinae. Neuronal circuits and bundle structure give hints of possible adaptations for contrast and/or movement detection. Behavioral experiments suggest that, in contrast to the vision specialists Lepomis gibbosus, pattern detection of G. petersii is not affected by higher spatial frequencies. A pattern of low spatial frequencies, however, was equally well detected by G. petersii and L. gibbosus. Optomotor response experiments indicate that motion vision is important for Gnathonemus, narrowing down the search for the functional specialization of the Gnathonemus retina and providing a starting point for work on multisensory integration in these fish.     

Waveform tuning of electroreceptor cells in the weakly electric fish, Gnathonemus petersii

Electroreceptive afferents from A- and B-electroreceptor cells of mormyromasts and Knollenorgans were tested for their sensitivity to different stimulus waveforms in the weakly electric fish Gnathonemus petersii. Both A- and B-mormyromast cells had their lowest sensitivity to a waveform similar to the self-generated electric organ discharge (EOD) (around 0° phase-shift). Highest sensitivities, i.e. lowest response thresholds, in both A- and B-cells were measured at phase shifts of +135°. Thus, both cell types were inversely waveform tuned. The sensitivity of B-cells increased sharply with increasing waveform distortions. Their tuning curves had a sharp minimum of sensitivity at +7° phase shift. A-cells had a much broader waveform tuning with a plateau level of low sensitivity from +24° to −15°. Across a 360° cycle of phase-shifts, the range of thresholds was 16 dB for individual B-cells and 4.5 dB for individual A-cells. Knollenorgan afferents were tuned to 0° phase-shifted EODs and had a dynamic range of 12 dB. Lowest sensitivities were measured at a phase shift of +165°. Experiments with computer-generated stimuli revealed that the strong sensitivity of mormyromast B-cells of EOD waveform distortions cannot be attributed to any of the seven waveform parameters tested. In addition, EOD stimuli must have the correct duration for B-cells to respond to waveform distortions. Thus, waveform tuning appears to be based on the specific combination of several waveform parameters that occur only with natural EODs. Accepted: 28 April 1997     

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.     

Adenosine triphosphatases in electroreceptor organs (ampullary organs and mormyromasts) of Gnathonemus petersii Mormyridae

Summary Cytochemical techniques were used for the light and electron microscopical localization of ATPase in the ampullary organ and the mormyromast, both cutaneous electroreceptors inGnathonemus petersii (Mormyridae).At the light microscope level, two different techniques gave the same results, namely that high concentrations of the enzyme are present in the mormyromast and certain epidermal cells and weak concentrations in the ampullary organ.The enzyme was localized at the ultrastructural level using the lead capture method. It was found in the cytoplasm of type III accessory cells of the ampullary organ, in the apical cytoplasm of SC1 sensory cells and the accessory cells surrounding them and on the membrane of the SC2 sensory cells of the mormyromast. The ATPase of these various cells was inhibited byp-chloromercuribenzoate.The enzyme in the mormyromast SC1 and their accessory cells was not dependent on Mg²⁺ ions. However, that in the type III accessory cells of the ampullary organ and in the SC2 of the mormyromast was strictly dependent on Mg²⁺. In addition, there was a Ca²⁺-dependent ATPase in the microvilli of the SC2 of certain mormyromasts.     

The electric image in weakly electric fish: I. A data-based model of waveform generation inGymnotus carapo

Understanding how electrosensory images are generated and perceived in actively electrolocating fish requires the study of the characteristics of fish bodies as electric sources. This paper presents a model ofGymnotus carapo based on measurements of the electromotive force generated by the electric organ and the impedance of the passive tissues. A good agreement between simulated and experimentally recorded transcutaneous currents was obtained. Passive structures participate in the transformation of the electromotive force pattern into transcutaneous current profiles. These spatial filtering properties of the fish's body were investigated using the model. The shape of the transcutaneous current profiles depends on tissue resistance and on the geometry and size of the fish. Skin impedance was mainly resistive. The effect of skin resistance on the spatial filtering properties of the fish's body was theoretically analyzed.The model results show that generators in the abdominal and central regions produce most of the currents through the head. This suggests that the electric organ discharge (EOD), generated in the abdominal and central regions is critical for active electrolocation. In addition, the well-synchronized EOD components generated all along the fish produce large potentials in the far field. These components are probably involved in long-distance electrocommunication.Preliminary results of this work were published as a symposium abstract.     

Special cutaneous receptor organs of fish. 3. The ampullary organs of Eigenmannia

Ampullary receptor organs of the South American weakly electric gymnotid fish Eigenmannia virescens consist of a pore at the surface of the skin, a canal through the epidermis, and the expanded basal end of the canal in the corium. The cavity of the organ contains a jelly that is filled with fine fibers. The canal wall consists of three to six layers of flattened cells that appear to be derived from the adjacent skin. Along the lumen of the organ the cells are joined by tight junctions. Usually there are four spherical receptor cells in the base of the organ. They are innervated by single neural terminals. These organs are compared to tuberous receptor organs found in the same species, and the functional significance of the fine structure observed in these cells is discussed.     

Trained Weakly-electric Fishes Pollimyrus isidori and Gnathonemus petersii (Mormyridae,Teleostei) Discriminate between Waveforms of Electric Pulse Discharges

Fish of the family Mormyridae emit weak, pulse-like electric organ discharges (EODs). The discharge rhythm is variable, but the waveform of the EOD is constant for each fish, with species- and individual characteristics. The ability of Pollimyrus isidori and Gnathonemus petersii (Mormyridae) to discriminate between different EOD waveforms was tested using a differential conditioning procedure. Fish were first trained to respond to a reference signal in swimming to a dish to receive a bloodworm (food reward). The reference signal consisted of a 10-Hz train of the digitally recorded EOD of a conspecific. Second, an alternative signal (10-Hz train of a different EOD, either from another species, or from a conspecific of the other sex) was associated with air bubbles as punishment. The two signals were played at successive trials in random order. On each trial the latency was measured between the onset of the signal and the response. 7 out of the 8 P. isidori tested and both of the two G. petersii tested associated the reference EOD with food. Among these, five P. isidori and two G. petersii responded differentially (p < 0.01) to EODs of different species. P. isidori similarly discriminated between conspecific EODs of different sexes. The quantity of different alternative EODs which could be tested was limited when fish eventually habituated to the punishment. Even when the amplitude of the EODs was randomly changed at each trial, two out of two G. petersii differentiated between EODs of the two species, and three out of three P. isidori tested differentiated between EODs within their own species. Response latencies to the rewarded signal during the basic training and during discrimination (when it had to be distinguished from the S-) were similar. G. petersii showed differential responses for S+ and S- also in the rhythm of discharge exhibited during playback, after five EOD pulses for one fish, and after a single pulse for the other. Mormyrids may therefore distinguish between conspecifics and members of other species, and even between individual conspecifics, by their EOD waveform.     

An internal current source yields immunity of electrosensory information processing to unusually strong jamming in electric fish

Summary The electric organ of a fish represents an internal current source, and the largely isopotential nature of the body interior warrants that the current associated with the fish's electric organ discharges (EODs) recruits all electroreceptors on the fish's body surface evenly. Currents associated with the EODs of a neighbor, however, will not penetrate all portions of the fish's body surface equally and will barely affect regions where the neighbor's current flows tangentially to the skin surface. The computational mechanisms of the jamming avoidance response (JAR) in Eigenmannia exploit the uneven effects of a neighbor's EOD current to calculate the correct frequency difference between the two interfering EOD signals even if the amplitude of a neighbor's signal surpasses that of the fish's own signal by orders of magnitude. The particular geometry of the fish's own EOD current thus yields some immunity against the potentially confusing effects of unusually strong interfering EOD currents of neighbors.Abbreviations DF frequency difference - ELL electrosensory lateral line lobe - EOD electric organ discharge - JAR jamming avoidance response     

Electric Imaging through Evolution,a Modeling Study of Commonalities and Differences

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.     

The electric organ discharges of the gymnotiform fishes: I. Apteronotus leptorhynchus

We present high temporal and spatial resolution maps in 3-dimensions of the electric field vector generated by the weakly electric fish, Apteronotus leptorhynchus. The waveforms and harmonic composition of the electric organ discharge (EOD) are variable around the fish but highly stable over long times at any position. We examine the role of harmonics on the temporal and spatial characteristics of the EOD, such as the slew rate and rostral-to-caudal propagation. We also explore the radial symmetry of the fish's field. There are major differences in the direction of the electric field vector at the head and caudal body. In the caudal part of the fish, the electric field vector rotates during the EOD cycle. However, rostral of the pectoral fin, the field magnitude and sign oscillate while maintaining relatively constant orientation. We discuss possible functional ramifications of these electric field patterns to electrolocation, communication, and electrogenesis.Abbreviations EOD electric organ discharge - EO electric organ - RMS root mean square - ADC analog-to-digital converter     

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.     

Active electrolocation of polarized objects by a pulse-discharging electric fish, <Emphasis Type="Italic">Gnathonemus </Emphasis><Emphasis Type="Italic">petersii</Emphasis>

Weakly electric fish react to resistance and capacitance of objects that locally amplify and distort their self-generated Electric Organ Discharge (EOD) received by their skin receptors. The successive-layer structure of tissues gives certain biological materials a kind of electrical anisotropy. A polarized object, for instance, will conduct current differently in one versus the other direction. This diode-like electric anisotropy should make a significant difference to a Mormyrid who emits a directional, biphasic EOD and whose receptors are sensitive to EOD amplitude and distortion changes. The ability of Gnathonemus petersii (Mormyridae) to discriminate polarity was investigated on a virtual object by manipulating changes in a circuit comprised of diodes combined in various ways. The “novelty response,” an increase in the discharge rate in response to perceived changes, was used to assess the fish’s sensitivity. Indeed, G. petersii detects polarized objects and discriminates between polarity directions. However, the diode-like anisotropy entails a voltage threshold. Because voltage decreases with distance, and the EOD comprises opposite phases of different amplitudes, the active spaces of detection and discrimination are different and depend on the object orientation. Electric polarity thus extends the “palette” of dielectric properties used by this fish to evaluate object quality, direction, and distance.     

Zur Signalverarbeitung im elektrischen Empfangsorgan des schwachelektrischen Fisches Gnathonemus petersii (Mormyriformes,Teleostei)

Zusammenfassung Wenn der schwachelektrische Fisch Gnathonemus petersii mit Hilfe seines elektrischen Organs eine Änderung seiner Umgebung bemerkt, reagiert er durch Erhöhung seiner Sendefrequenz. Diese Reaktion erfolgt dann, wenn eine gewisse Anzahl N von Elektrorezeptoren überschwellig gereizt wird, wobei es auf die relative Lage der gereizten Rezeptoren zueinander innerhalb der untersuchten Gebiete nicht ankommt und es auf die Zahl N keinen Einfluß hat, ob die Rezeptoren schwach oder stark überschwellig gereizt werden (s. Abb. 5). Bei der Detektion sind wahrscheinlich die sog. Knollenorgane, ein bestimmter Typ von Elektrorezeptoren, maßgeblich beteiligt. In einem Dressurexperiment wird geprüft, ob Gnathonemus außer der Information über die Zahl der gereizten Elektrorezeptoren auch die Information über ihre Lage nutzt: Gnathonemus kann zwei in der örtlichen Verteilung auf der Fischoberfläche verschiedene Signale weitgehend unabhängig von deren Amplitude unterscheiden.

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Signal processing in the receptor system of the weakly electric fish Gnathonemus petersii (Mormyriformes, teleostei, pisces)

Summary The weakly electric fish Gnathonemus petersii increases the discharge frequency of its electric organ if it detects a change in its environment. This reaction appears if a number N of electroreceptors is stimulated above the threshold. The number N is not dependent upon the relative position of the stimulated receptors (within the investigated area) nor upon the degree to which the stimulus is raised above the threshold (see Fig. 5). Probably one class of electroreceptors, the so-called Knollenorgane, play a decisive role in detection. By means of a training experiment it was determined that Gnathonemus is able to distinguish between two signals which differ in their spatial distribution on the surface of the fish. This ability is largely independent of the magnitude of the signals.

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Der Verfasser dankt dem Bundesministerium der Verteidigung für die Bereitstellung der Mittel für diese Untersuchungen.     

Cutaneous electrical oscillation in a weakly electric fish, Gymnarchus niloticus

An African electric fish, Gymnarchus niloticus. ceases its electric organ discharge for a prolonged time in response to external electrical signals. During the cessation of electric organ discharges from the electric organ, a weak sinusoidal signal (approximately 0.1 mV cm(-1)) near the fish's previous discharge frequency was recorded near the body. The oscillatory potentials at all points on the body surface were synchronized and had a complex spatial distribution. The source of the potential was determined to be within the dermal tissue. Electroreceptive central neurons that responded to a moving target near the fish with normal electric organ discharges also responded to the same target when the electric organ discharge was interrupted and the potential from the skin existed. This result suggests that the fish may be able to electrolocate objects without the discharge from the electric organ.     

Untersuchungen zur circadianen Rhythmik der elektrischen und motorischen Aktivität von Gnathonemus petersii (Mormyridae,Pisces)

Investigations on the diurnal rhythm of the motoric and electric activity were performed with the electric fish Gnathonemus petersii. A group of 11 conspecifics as well as single fishes showed an increased electric and motoric activity at night, especially at the beginning and end of the dark phase and also during feeding. These normal diurnal rhythms were changed for at least 3 days by the aggressive behaviour of two fishes who were set together for the first time. During this time an order of precedence was established.