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     

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.     

Pyramidal-cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs

Recordings within the posterior eminentia granularis of the weakly electric fish, Apteronotus leptorhynchus, revealed multiple types of proprioceptive units responsive to changes in the position of the animal's trunk and tail. Intracellular labelling showed that the proprioceptor recordings were made from axons that ramify extensively within the EGp. The location of the somata giving rise to these axons is presently unknown. Electroreceptor afferent responses to electric organ discharge amplitude modulations caused by movement of the animal's tail were compared to responses caused by electronically generated AMs of similar amplitude and time course. These did not differ. Electrosensory lateral line lobe pyramidal cells responded significantly less to electric organ discharge amplitude modulations caused by changing the animal's posture as compared to electronically produced AMs, suggesting that central mechanisms attenuate pyramidal cell responses to reafferent electrosensory inputs. Experiments in which the pattern of reafferent input associated with changes in posture was altered revealed that the pyramidal cells learn, over a time course of several minutes, to reject new patterns of input. Both proprioceptive input and descending electrosensory input to the posterior eminentia granularis are involved in generating the observed plastic changes in pyramidal cell responsiveness.Abbreviations AM amplitude modulation - EGp posterior eminentia granularis - ELL electrosensory lateral line lobe - EOD electric organ discharge - HRP horseradish peroxidase - LTD long-term depression - LTP long-term potentiation     

Species recognition in mormyrid weakly electric fish

We investigated group cohesion in four species of African weakly electric fish (Brienomyrus niger, Gnathonemus petersii, Marcusenius cyprinoides and Pollimyrus isidori). The attraction among members of the same and different species served as the criterion for species recognition. To identify possible mechanisms underlying this ability, conspecifics were allowed to interact through a wide-meshed plastic screen with either a pair of confined conspecifics or a pair from a related species. Members of each of the four test species were optimally attracted to their own kind, but also responded selectively to the presence of the other species. These interspecific interactions ranged from attraction to avoidance. The difference in the fish's preference to aggregate in inter- and intraspecific interactions pointed to species-specific social cues that facilitate group cohesion in mormyrid fish. Since all four species respond to each other's electric organ discharge with changes in their own discharge rate, species recognition cannot be merely a function of electroreceptor characteristics but must involve the integration of electroreceptive and other sensory cues.     

The responses of peripheral and central mechanosensory lateral line units of weakly electric fish to moving objects

Mechanosensory lateral line afferents of weakly electric fish (Eigenmannia) responded to an object which moved parallel to the long axis of the fish with phases of increased spike activity separated by phases of below spontaneous activity. Responses increased with object speed but finally may show saturation. At increasingly greater distances the responses decayed as a power function of distance. For different object velocities the exponents (mean±SD) describing this response falloff were -0.71±0.4 (20 cm/s object velocity) and-1.9±1.25 (10 cm/s). Opposite directions of object movement may cause an inversion of the main features of the response histograms. In terms of peak spike rate or total number of spikes elicited, however, primary lateral line afferents were not directionally sensitive.Central (midbrain) lateral line units of weakly electric fish (Apteronotus) showed a jittery response if an object moved by. In midbrain mechanosensory lateral line, ampullary, and tuberous units the response to a rostral-tocaudal object movement may be different from that elicited by a caudal-to-rostral object motion. Central units of Apteronotus may receive input from two or more sensory modalities. Units may be lateral line-tuberous or lateral line-ampullary. Multimodal lateral line units were OR units, i.e., the units were reliably driven by a unimodal stimulus of either modality. The receptive fields of central units demonstrate a weak somatotopic organization of lateral line input: anterior body areas project to rostral midbrain, posterior body areas project to caudal midbrain.Abbreviation EOD electric organ discharge     

Peripheral electrosensory imaging by weakly electric fish

Different species have developed different solutions to the problem of constructing a representation of the environment from sensory images projected onto sensory surfaces. Comprehension of how these images are formed is an essential first step in understanding the representation of external reality by a given sensory system. Modeling of the electrical sensory images of objects began with the discovery of electroreception and continues to provide general insights into the mechanisms of imaging. Progress in electric image research has made it possible to establish the physical basis of electric imaging, as well as methods to accurately predict the electric images of objects alone and as a part of a natural electric scene. In this review, we show the following. (1) The internal low resistance of the fish’s body shapes the image in two different ways: by funneling the current generated by the electric organ to the sensory surface, it increases the fields rostrally, thus enhancing the perturbation produced by nearby objects; and by increasing the projected image. (2) The electric fish’s self-generated currents are modified by capacitive objects in a distinctive manner. These modulations can be detected by different receptor types, yielding the possibility of “electric color.” (3) The effects of different objects in a scene interact with each other, generating an image that is different from the simple addition of the images of individual objects, thus causing strong contextual effects.     

Communication in the weakly electric fish Sternopygus macrurus

Summary A classical conditioning paradigm was used to test the ability of Sternopygus macrurus to detect EOD-like stimuli (sine waves) of different frequencies. The behavioral tuning curves were quite close in shape to tuning curves based on single-unit recordings of T units, although the sensitivity at all frequencies was much greater. The behavioral curves showed notches of greatly reduced sensitivity when the test frequency was equal to, or twice the EOD frequency. The EOD of each of the fish was eliminated by lesioning the medullary pacemaker nucleus, and the fish were retested. The resulting tuning curves were nearly the same in shape as those of the EOD-intact individuals, but the PMN-lesioned fish showed an overall reduction of sensitivity of 30 dB. The EOD appears to enhance sensitivity by placing the summed stimulus (test stimulus + fish's EOD) at an amplitude where T units are maximally sensitive to small temporal modulations in the fish's own EOD. Peripheral tuning appears to limit the ability of males to detect the EOD of females, since these are, on average, an octave higher in frequency than the male EOD, while the peak sensitivity of the male occurs 5–10 Hz above its own EOD frequency.Abbreviations EOD electric organ discharge - PMN pacemaker nucleus - BF best frequency - DF difference frequency     

Communication in the weakly electric fish Sternopygus macrurus

There is a sexual dimorphism in the frequency of the quasi-sinusoidal electric organ discharge (EOD) of Sternopygus macrurus, with males, on average, an octave lower. EODs are detected by tuberous electroreceptor organs, which exhibit V-shaped frequency tuning with maximal sensitivity near the fish's own EOD frequency. This would seem to limit the ability of a fish to detect the EODs of opposite-sex conspecifics. However, electroreceptor tuning has always been based on single-frequency stimulation, while actual EOD detection involves the addition of a conspecific EOD to the fish's own. In the present study, recordings were made from single electroreceptive units while the fish were stimulated with pairs of sine waves: one (S1) representing the fish's own EOD added to a second (S2) representing a conspecific EOD. T unit response was easily predicted by assuming that the electroreceptor acts as a linear filter in series with a threshold-sensitive spike initiator. P unit response was more complex, and unexpectedly high sensitivity was found for frequencies of S2 well displaced from the fish's EOD frequency. For both P and T units, detection thresholds for S2 were much lower when added to S1, than when presented alone.     

Spatial acuity and prey detection in weakly electric fish

It is well-known that weakly electric fish can exhibit extreme temporal acuity at the behavioral level, discriminating time intervals in the submicrosecond range. However, relatively little is known about the spatial acuity of the electrosense. Here we use a recently developed model of the electric field generated by Apteronotus leptorhynchus to study spatial acuity and small signal extraction. We show that the quality of sensory information available on the lateral body surface is highest for objects close to the fish's midbody, suggesting that spatial acuity should be highest at this location. Overall, however, this information is relatively blurry and the electrosense exhibits relatively poor acuity. Despite this apparent limitation, weakly electric fish are able to extract the minute signals generated by small prey, even in the presence of large background signals. In fact, we show that the fish's poor spatial acuity may actually enhance prey detection under some conditions. This occurs because the electric image produced by a spatially dense background is relatively “blurred” or spatially uniform. Hence, the small spatially localized prey signal “pops out” when fish motion is simulated. This shows explicitly how the back-and-forth swimming, characteristic of these fish, can be used to generate motion cues that, as in other animals, assist in the extraction of sensory information when signal-to-noise ratios are low. Our study also reveals the importance of the structure of complex electrosensory backgrounds. Whereas large-object spacing is favorable for discriminating the individual elements of a scene, small spacing can increase the fish's ability to resolve a single target object against this background.     

Model of P- and T-electroreceptors of weakly electric fish.

To clarify the microscopic mechanisms by which P- and T-receptors encode amplitude modulation and zero crossing time of jamming signals, we present a model of P- and T-receptors based on their physiological and anatomical properties. The model consists of a receptor cell, supporting cells, and an afferent nerve fiber. The basal membrane of the receptor cell includes voltage-sensitive Ca2+ channels, Ca(2+)-activated K+ channels, and leak channels of Na+, K+, and Cl-. The driving force of potential change under stimulation is generated by the voltage-sensitive Ca2+ channels, and the suppressing force of the change is generated by Ca(2+)-activated K+ channels. It has been shown that in T-receptor cells the driving force is much stronger than the suppressing force, whereas in P-receptor cells the driving force is comparable with the suppressing force. The difference in various kinds of response properties between P- and T-receptors have been consistently explained based on the difference in the relative strengths of the driving and suppressing forces between P- and T-receptor cells. The response properties considered are encoding function, probability of firing of afferent nerve, pattern of damped oscillation, shape of tuning curves, values of the optimum frequency, and response latency.     

The anal fin complex in a weakly discharging electric fish, Gnathonemus petersii(Mormyridae)

An examination of the permanent bony structures of the anal fin complex in the mormyrid fish, Gnathonemus petersii , revealed two new structural sexual dimorphisms: longer proximal pterygiophores and wider anal fin rays in males than in females. Both structures are thought to facilitate the male's courtship‐associated anal fin reflex. Adult male mormyrid fishes are characterized by a dorsally directed indentation of the posterior body wall (anal fin indentation). The expression of this indentation in males, presumably driven by anal fin musculature, was correlated with the fish's gonadal state: large indentations were associated with high gonado‐somatic indices and small indentations with low indices.     

Development of the gigantocerebellum of the weakly electric fish Pollimyrus

The morphogenesis of the "hypertrophied" mormyrid cerebellum was investigated in Pollimyrus (Pisces). Two adults and 36 larvae and young fish raised in captivity were used. Two Gnathonemus petersii adults were taken for comparison. The ontogenetic development of the various cerebellar structures was analysed in inverse chronological order with the aid of serial sagittal and frontal brain sections. Special attention was given to the trilobed corpus cerebelli (C1, C2, C3), the lobi transitorii et caudales, the valvula, the crista cerebelli, the eminentia granularis and the lobus lineae lateralis. 1. The cerebellar structures are of bilateral origin; they develop from the cerebellar and acoustico-lateral "anlage" of the rhombencephalon behind the rhombomesencephalic fissure, either through budding or individualisation and appear between the 4th and 11th day after spawning. The midline fusion of the symmetrical structures is accomplished somewhat later, between the 8th and 23rd days. 2. The cerebellar structures acquire their definitive spatial organisation within 38 days, except for the valvula whose development takes much longer. Recognisable from the 11th day, the valvula upon which ridges are visible from the beginning continues to grow after the 38th day beyond the mesencephalic ventricle, finally overlying the telencephalon frontally and the different rhombencephalic structures caudally. This development, which includes a large antero-lateral folding of the valvula, takes 240 days. 3. Cytological differentiation is just as complex as the general development of the cerebellar structures. Cortical stratification first begins on the 8th to the 11th day in the corpus cerebelli and in the valvula from day 21 to 23 onwards. This differentiation is characterised throughout almost the entire cerebellum by a downward migration of the superficial undifferentiated cells which then constitute the granular layer. In the valvula, the majority of the undifferentiated cells leave the ridges to form a continuous granular layer at the base of the ridges. 4. A differentiation gradient was observed on the antero-posterior axis. 5. In spite of its complexity, the mormyrid cerebellum develops much more rapidly than the cerebellum of the trout.