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.     

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.     

A new method for the simulation of electric fields,generated by electric fish,and their distorsions by objects

Among the many species of fishes endowed with electric organs Mormyriformes and Gymnotoidei are known to emit and receive electric signals for the purposes of intraspecific communication and recognition of objects. Models which have been proposed for this electro-sensory system generally assume steady-state conditions. On the other hand, the very character of the signals itself and the idea that the cerebellum might be working as a clock point to the importance of the signal dynamics. Therefore a new approach to the simulation of electric fields is described in the paper. The basic idea is to superpose the fields of point charges in a way that the sum is in accordance with the fish's electric field. The same technique could be used to simulate the influence of objects on the electric field. Following a suggestion of Dr. E. Kasper I used a simpler but equal effective approach for object simulation consisting in the use of a dipole instead of point charges. The model described is easily applied to diverse situations and allows one to estimate the influence of various parameters (size, shape, and position) on the “electric image” of an object. Furthermore, the well-known behaviour of tailbending and its consequences in object recognition can be simulated. The results underline the importance of signal dynamics for species with pulse-type discharges.     

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.     

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.     

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.     

Marine electric fields and fish orientation

1. Two methods for short-span measurements of DC electric fields in the sea are described. 2. The results indicate a difference between local electric fields (up to 150 muV/m) caused by bottom structures and regional electric fields (up to 60 muV/m) due to electromagnetic processes. 3. The possible relevance of these phenomena to electro-sensitive fishes is discussed.     

Behavioral responses of weakly electric fish to complex impedances

Summary Members of the family of African electric fish, Mormyridae, exhibit a novelty response, consisting of an acceleration in the rate of electric organ discharges (EODs), when faced with changes in feedback arising from their EODs. In this study, the novelty responses of three different species of mormyrids to shunts with different electrical characteristics were noted. The three species differed in the frequency contents of their EODs: two species had relatively high spectral frequencies in their EODs (>10 kHz), while the third species had only lower spectral frequencies (< 10 kHz). Primarily resistive shunts elicited novelty response accelerations in all three species, and the magnitudes of these responses, when normalized to the responses obtained for a shunt with no introduced resistance, were comparable for all three species. For primarily capacitive shunts, however, the magnitudes of the normalized responses were different for the three species: the two species with high spectral frequencies in their EODs showed larger normalized responses than the third species which had only low EOD spectral frequencies.The differences in species responses for capacitive shunts, and the similarities in species responses for resistive shunts, suggest that electric fish detect the complex impedance of objects in their near field environment: a circuit model consisting of a fish emitting discharges into the surrounding water, which can be shunted by a variable complex impedance, conforms well to the data. Thus, electrolocation is a frequency dependent sensory process, and this frequency dependency should be considered in any speculation about the adaptive value of different EOD waveforms.Abbreviation EOD electric organ discharge     

60-Hz electric and magnetic fields generated by a distribution network

From a mobile unit, 60-Hz electric and magnetic fields generated by Hydro-Québec's distribution network were measured. Nine runs, representative of various human environments, were investigated. Typical values were 32 V/m and 0.16 microT. The electrical distribution networks investigated were major contributors to the electric and magnetic environments.     

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.     

Theoretical analysis of pre-receptor image conditioning in weakly electric fish

Electroreceptive fish detect nearby objects by processing the information contained in the pattern of electric currents through the skin. The distribution of local transepidermal voltage or current density on the sensory surface of the fish's skin is the electric image of the surrounding environment. This article reports a model study of the quantitative effect of the conductance of the internal tissues and the skin on electric image generation in Gnathonemus petersii (Günther 1862). Using realistic modelling, we calculated the electric image of a metal object on a simulated fish having different combinations of internal tissues and skin conductances. An object perturbs an electric field as if it were a distribution of electric sources. The equivalent distribution of electric sources is referred to as an object's imprimence. The high conductivity of the fish body lowers the load resistance of a given object's imprimence, increasing the electric image. It also funnels the current generated by the electric organ in such a way that the field and the imprimence of objects in the vicinity of the rostral electric fovea are enhanced. Regarding skin conductance, our results show that the actual value is in the optimal range for transcutaneous voltage modulation by nearby objects. This result suggests that "voltage" is the answer to the long-standing question as to whether current or voltage is the effective stimulus for electroreceptors. Our analysis shows that the fish body should be conceived as an object that interacts with nearby objects, conditioning the electric image. The concept of imprimence can be extended to other sensory systems, facilitating the identification of features common to different perceptual systems.     

Neural correlates of novelty detection in pulse-type weakly electric fish

Evoked potentials (EPs) and single unit recordings from various electrosensory-processing regions of several pulse-type gymnotiform species were made to investigate neural activity patterns that could be associated with novelty detection. Whereas the electrosensory afferents and cells in the ELL exhibited only minor changes in response size as stimuli were presented less frequently (novel stimuli), most units studied in the torus semicircularis (TS) showed very strong, increased responsiveness to stimuli presented less frequently relative to stimuli presented persistently (at every EOD event. The responses of the TS were graded with respect to stimulus frequency. The discrimination between novel and persistent stimuli by the TS occurred with stimuli presented transversely or longitudinally with respect to the fish's long axis, and regardless of the timing of the stimulus with respect to the fish's pacemaker-related signal (PS). When electrosensory novelties were presented persistently the responses of the TS rapidly habituated. This may indicate that activity in this region of the TS is novelty related. This novelty-related activity in the TS can be correlated with certain aspects of the fish's behavior, i.e., EOD interval length during a behavioral novelty response. However, TS activity may continue to indicate the occurrence of electrosensory novelties after the behavior has habituated. It is suggested that the novelty-related activity of the TS of these fish is necessary, but not sufficient, for the production of electrosensory novelty-induced behavioral responses. Lesions of the region of the TS containing the rapidly-habituating neurons abolished the electrosensory novelty response, but not that resulting from visual and auditory stimulation.     

Distance and shape: perception of the 3-dimensional world by weakly electric fish.

Weakly electric fish orient at night in complete darkness by employing their active electrolocation system. They emit short 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. This process corresponds to similar processes during vision, where visual images are cast onto the retinas of eyes. Behavioral experiments have shown that electric fish can measure the distance of objects during active electrolocation, thus possessing three-dimensional depth perception of their surroundings. The fundamental mechanism for distance determination differs from stereopsis used during vision by two-eyed animals, but resembles some supplementary mechanisms for distance deduction in humans. Weakly electric fish can also perceive the three-dimensional shape of objects. The fish can learn to identify certain objects and discriminate them from all other objects. In addition, they spontaneously categorize objects according to their shapes and not according to object size or material properties. There is good evidence that some fundamental types of perceptional invariances during visual object recognition in humans are also found in electric fish during active electrolocation. These include size invariance (maybe including size constancy), rotational invariance, and translational invariance. The mechanisms of shape detection during electrolocation are still unknown, and their discoveries require additional experiments.