Sensory cues for the gradual frequency fall responses of the gymnotiform electric fish, Rhamphichthys rostratus

The sensory cues for a less known form of frequency shifting behavior, gradual frequency falls, of electric organ discharges (EODs) in a pulse-type gymnotiform electric fish, Rhamphichthys rostratus, were identified. We found that the gradual frequency fall occurs independently of more commonly observed momentary phase shifting behavior, and is due to perturbation of sensory feedback of the fish's own EODs by EODs of neighboring fish. The following components were identified as essential features in the signal mixture of the fish's own and the neighbor's EOD pulses: (1) the neighbor's pulses must be placed within a few millisecond of the fish's own pulses, (2) the neighbor's pulses, presented singly at low frequencies (0.2–4 Hz), were sufficient, (3) the frequency of individual pulse presentation must be below 4 Hz, (4) amplitude modulation of the sensory feedback of the fish's own pulses induced by such insertions of the neighbor's pulses must contain a high frequency component: sinusoidal amplitude modulation of the fish's own EOD feedback at these low frequencies does not induce gradual frequency falls. Differential stimulation across body surfaces, which is required for the jamming avoidance response (JAR) of wave-type gymnotiform electric fish, was not necessary for this behavior. We propose a cascade of high-pass and low-pass frequency filters within the amplitude processing pathway in the central nervous system as the mechanism of the gradual frequency fall response.Abbreviations EOD electric organ discharge - f frequency of EOD or pacemaker command signal - JAR jamming avoidance response - S ₁ stimulus mimicking fish's own EOD - f ₁ frequency of S₁ - S ₂ stimulus mimicking neighbor's EOD - f ₂ frequency of S₂     

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.     

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.     

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 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.     

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.     

Differential distribution of ampullary and tuberous processing in the torus semicircularis of Eigenmannia

Summary Gymnotiform electric fish sense low-and high frequency electric signals with ampullary and tuberous electroreceptors, respectively. We employed intracellular recording and labeling methods to investigate ampullary and tuberous information processing in laminae 1–5 of the dorsal torus semicircularis of Eigenmannia. Ampullary afferents arborized extensively in laminae 1–3 and, in some cases, lamina 7. Unlike tuberous afferents to the torus, ampullary afferents had numerous varicosities along their finest-diameter branches. Neurons that were primarily ampullary were found in lamina 3. Neurons primarily excited by tuberous stimuli were found in lamina 5 and, more rarely, in lamina 4. Cells that had dendrites in lamina 1–3 and 5 could be recruited by both ampullary and tuberous stimuli. These bimodal cells were found in lamina 4. During courtship, Eigenmannia produces interruptions of its electric organ discharges. These interruptions stimulate ampullary and tuberous receptors. The integration of ampullary and tuberous information may be important in the processing of these communication signals.Abbreviations JAR jamming avoidance response - EOD electric organ discharge - S1 sinusoidal signal mimicking fish's EOD - S2 jamming signal - Df frequency difference (S2-S1) or between a neighbor's EODs and fish's own EODs - CNS central nervous system     

Primary afferent fibers conduct impulses in both directions under physiological stimulus conditions

Summary In electric fish of the family Mormyridae some primary afferent fibers conduct impulses not only from electroreceptors to the brain but also from the brain to the receptors. The efferent impulses may be elicited by electrical stimulation which is within the physiological range, i.e., by stimulation which is similar in amplitude and duration to the stimulation that is caused by the fish's own electric organ discharge. Afferent and efferent impulses in the same afferent fiber were identified by: simultaneously recording from a fiber at two different points, at the receptor and at the nerve trunk (Figs. 2C-H; 3B-D); by cutting the afferent fiber between the brain and the recording site as well as between the recording site and the periphery; and by intra-axonal recording from the afferent fiber near its entry into the brain (Fig. 4). The efferent impulses result from the central integration of a corollary discharge of the electric organ motor command with excitatory and inhibitory input from several different receptors near the one from which afferent impulses originate (Fig. 4). The centrally originating impulse may be capable of modifying the effect of signals originating in the periphery.Abbreviations ELLL electrosensory lateral line lobe - EOCD electric organ corollary discharge - EOD electric organ discharge - epsp excitatory postsynaptic potential - NPLL posterior lateral line nerve     

Group cohesion in juvenile weakly electric fish Mormyrus rume proboscirostris

The current study demonstrated that juvenile Mormyrus rume proboscirostris , an African freshwater weakly electric fish, used their active electrosense in group cohesion. Data also indicated that sight and mechano-reception could play a synergistic role in controlling this behaviour. The developmental change from a larval monophasic electric organ discharge to the adult biphasic waveform was accompanied by a reversal of the fish's social spacing. Light was aversive to social spacing in the younger fish (aged 49 and 65 days), but facilitated aggregation in the older fish (245 days).     

Electrosensory phase sensitivity in the weakly electric fish Eigenmannia in the detection of signals similar to its own

The electric organ discharge (EOD) of the South American knifefish Eigenmannia sp. is a permanently present wave signal of usually constant amplitude and frequency (similar to a sine wave). A fish perceives discharges of other fish as a modulation of its own. At frequency identity (F = 0 Hz) the phase difference between a fish's own electric discharge and that of another fish affects the superimposed waveform. It was unclear whether or not the electrosensory stimulus-intensity threshold as behaviourally determined depends on the phase difference between a fish's own EOD and a sine-wave stimulus (at F = 0 Hz). Also the strength of the jamming avoidance response (JAR), a discharge frequency shift away from a stimulus that is sufficiently close to the EOD frequency, as a function of phase difference was studied. Sine-wave stimuli were both frequency-clamped and phase-locked to a fish's discharge frequency (F = 0 Hz). In food-rewarded fish, the electrosensory stimulus-intensity threshold depended significantly on the phase difference between a fish's discharge and the stimulus. Stimulus-intensity thresholds were low (down to 3 V/cm, peak-to-peak) when the superimposed complex wave changed such that the shift in zero-crossings times relative to the original EOD was large but amplitude change minimal; stimulus-intensity thresholds were high (up to 16.9 V/cm, peak-to-peak) when the shift in zero-crossings times was small but amplitude change maximal. Similar results were obtained for the non-conditioned JAR: at constant supra-threshold stimulus intensities and F = 0 Hz, the phase difference significantly affected the strength of the JAR, although variability between individuals was higher than that observed in the conditioned experiments.Abbreviations ACP active phase coupling - EOD electric organ discharge - JAR jamming avoidance response - F frequency (fish) — frequency (stimulus) [Hz] - p-p peak-to-peak     

Active electric imaging: body-object interplay and object's "electric texture"

This article deals with the role of fish's body and object's geometry on determining the image spatial shape in pulse Gymnotiforms. This problem was explored by measuring local electric fields along a line on the skin in the presence and absence of objects. We depicted object's electric images at different regions of the electrosensory mosaic, paying particular attention to the perioral region where a fovea has been described. When sensory surface curvature increases relative to the object's curvature, the image details depending on object's shape are blurred and finally disappear. The remaining effect of the object on the stimulus profile depends on the strength of its global polarization. This depends on the length of the object's axis aligned with the field, in turn depending on fish body geometry. Thus, fish's body and self-generated electric field geometries are embodied in this "global effect" of the object. The presence of edges or local changes in impedance at the nearest surface of closely located objects adds peaks to the image profiles ("local effect" or "object's electric texture"). It is concluded that two cues for object recognition may be used by active electroreceptive animals: global effects (informing on object's dimension along the field lines, conductance, and position) and local effects (informing on object's surface). Since the field has fish's centered coordinates, and electrosensory fovea is used for exploration of surfaces, fish fine movements are essential to perform electric perception. We conclude that fish may explore adjacent objects combining active movements and electrogenesis to represent them using electrosensory information.     

Differential production of chirping behavior evoked by electrical stimulation of the weakly electric fish, Apteronotus leptorhynchus

Aperonotus leptorhynchus (Gymnotiformes) produces wave-like electric organ discharges distinguished by a high degree of constancy. Transient frequency and amplitude modulations of these discharges occur both spontaneously and during social interactions, which can be mimicked by external electrical stimulation. The so-called chirps can be divided into four different types. Independent of the type of chirp produced under spontaneous conditions, the fish generate only significant numbers of type-2 chirps under evoked conditions. The rate of production of chirps of this type is largely determined by the frequency relative to the fish's frequency and signal intensity. Frequencies of + 10 Hz of the fish's own discharge frequency most effectively elicit chirps. Type-2 chirps can also be evoked through stimulation at or near the higher harmonic frequencies of the fish's frequency, but the chirp rate decreases with increasing number of the higher harmonic component. Over a certain range, the rate of production of type-2 chirps increases with increasing stimulus intensity. At very high intensities the generation of type-2 chirps is accompanied by the production of a novel type of electrical signal ("abrupt frequency rise") characterized by a frequency increase of approximately 20 Hz and high repetition rates of roughly 10 s(-1). We hypothesize that the different types of electric modulations subserve different behavioral functions.     

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.     

Electrosensory modulation of escape responses

Once initiated, rapid escape responses of teleost fishes are thought to be completed without additional sensory modification. This suggests that the motor program for a particular response is selected for by the constellation of sensory cues existing at the time of the releasing stimulus. This paper presents initial evidence that a highly specialized, phylogenetically recent electrosensory system is integrated with a primitive motor system and allows an animal to continuously monitor its environment for producing accurate escape behaviors.Behavioral testing for directed startle responses in a Y-maze demonstrates that when presented immediately before an acoustic startle stimulus, electric fish (Eigenmannia virescens), direct their response away from the cue (a transient shorting of their electric field). Thus, electrosensory cues as brief as 100 ms provide directional information to the escape motor network.In electric fish that are curarized to facilitate intracellular recording, the normal electric organ discharge is attenuated. When an electronically generated replacement field of the same frequency and amplitude as the fish's normal signal is shorted, a fast-rising, 7 ms latency post-synaptic potential is evoked from the Mauthner cell. Similar PSPs are generated by turning the replacement stimulus on and off. In some recordings, removing the S1 replacement field elicits a rebound of other afferent activity to the Mauthner cell; replacing the field suppresses this activity.Abbreviations EHP extrinsic hyperpolarizing potential - EOD electric organ discharge - JAR jaming avoidance response - LED light emitting diode - PSP postsynaptic potential     

Behavioral evidence of a latency code for stimulus intensity in mormyrid electric fish

Mormryid electric fish (Gnathonemus petersii) respond to novel stimuli with an increase in the rate of the electric organ discharge (EOD). These novelty responses were used to measure the fish's ability to detect small changes in the amplitude and latency of an electrosensory stimulus. Responses were evoked in curarized fish in which the EOD was blocked but in which the EOD motor command continued to be emitted. An artificial EOD was provided to the fish at latencies of 2.4 to 14.4 ms following the EOD motor command.Novelty responses were evoked in response to transient changes in artificial EOD amplitude as small as 1% of baseline amplitude, and in latency as small as 0.1 ms. Changes in latency were effective only at baseline delays of less than 12.4 ms.The sensitivity to small changes in latency supports the hypothesis that latency is used as a code for stimulus intensity in the active electrolocation system of mormyrid fish. The results also indicate that a corollary discharge signal associated with the EOD motor command is used to measure latency.Abbreviations EOD electric organ discharge - ELL electrosensory lateral line lobe - epsp excitatory post synaptic potential     

Coding conspecific identity and motion in the electric sense

Interactions among animals can result in complex sensory signals containing a variety of socially relevant information, including the number, identity, and relative motion of conspecifics. How the spatiotemporal properties of such evolving naturalistic signals are encoded is a key question in sensory neuroscience. Here, we present results from experiments and modeling that address this issue in the context of the electric sense, which combines the spatial aspects of vision and touch, with the temporal aspects of audition. Wave-type electric fish, such as the brown ghost knifefish, Apteronotus leptorhynchus, used in this study, are uniquely identified by the frequency of their electric organ discharge (EOD). Multiple beat frequencies arise from the superposition of the EODs of each fish. We record the natural electrical signals near the skin of a "receiving" fish that are produced by stationary and freely swimming conspecifics. Using spectral analysis, we find that the primary beats, and the secondary beats between them ("beats of beats"), can be greatly influenced by fish swimming; the resulting motion produces low-frequency envelopes that broaden all the beat peaks and reshape the "noise floor". We assess the consequences of this motion on sensory coding using a model electroreceptor. We show that the primary and secondary beats are encoded in the afferent spike train, but that motion acts to degrade this encoding. We also simulate the response of a realistic population of receptors, and find that it can encode the motion envelope well, primarily due to the receptors with lower firing rates. We discuss the implications of our results for the identification of conspecifics through specific beat frequencies and its possible hindrance by active swimming.     

Emergence of temporal-pattern sensitive neurons in the midbrain of weakly electric fish Gymnarchus niloticus.

Sensitivity of neurons in the torus semicircularis of a weakly electric fish, Gymnarchus niloticus, to two stimulus parameters that are critical for its behavior the jamming avoidance response was examined. The first parameter is the sign of frequency difference between discharge frequencies of fish's own electric organ and that of a neighbor's. The second parameter is the spatial orientation of neighbor's electric field. Whereas neuronal ambiguity of frequency coding for different orientations of neighbor's electric field is predicted, unambiguous JAR occurs at the behavioral level. Most neurons in the torus semicircularis showed sensitivity to the sign of frequency difference. Although a small number of neurons showed preference to a consistent sign of the frequency difference, the coding of the sign of frequency differences was found to be ambiguous with a highly variable pattern of responses for different orientations in most of neurons.     

Social spacing in the mormyrid fish Gnathonemus petersii (Pisces): A multisensory approach

The sensory basis of group cohesion in the weak-electric fish Gnathonemus petersii was investigated in a circular tank with groups of four fish each, interacting through a wide-meshed plastic screen with intact or operated conspecifics, or with other stimulus objects. We confined these stimuli to one or two peripheral holding compartments. The response measures were obtained from the free swimming fish and included (1) the time the fish spent together as a group, (2) the time they spent in front of the holding compartments, (3) the circular distribution of the fish's positions, and (4) the mean nearest neighbour distances. Under empty compartment conditions, four different groups were tested, consisting of either (1) intact, electrically active fish, or (2) electrically ‘silent’ fish (with their electric organ surgically rendered inoperative), or (3) blind, or (4) ‘silent’ and blind animals. The loss of either sensory modality, vision or feedback from electric organ discharge, led to changes of comparable size, decreasing the time spent as a group and increasing the mean nearest neighbour distance. In fish lacking both modalities, group cohesion was further impaired. With stimuli present in one or both holding compartments, the strength of social attraction depended on the nature of the stimulus: the more intact stimulus conspecifics were present, the more densely did the fish group in front of the stimulus compartment. ‘Wired-in’ electric organ discharges (simulating waveform and intensity) and electrically ‘silent’ fish were equally attractive, but only half as attractive as intact fish. Blind free swimming fish aggregated with intact and also with ‘silent’ conspecifics. Under dim light conditions, group cohesion was predominantly, though not exclusively, affected by electrosensory feedback from the electric organ discharge and visual input. Mechanical and olfactory cues may also be involved.     

Insight into the mechanisms of neuronal processing from electric fish

Weakly electric fish use their electric fields to locate objects and communicate with each other. Their electric discharges vary with species, gender, and social status. This variation is mediated by steroid and peptide hormones that influence ion currents through changes in gene expression or phosphorylation state. Understanding how electric fish decode the perturbations of their electric fields that result from interactions with the discharges of other fish or prey is illuminating general mechanisms of neuronal processing. Their central sensory circuits are specialized to process amplitude modulated signals, to detect microsecond variations in spike timing, and are dynamically reconfigured depending on the stimulus parameters.