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     

Electric organ activation in Gymnotus carapo: Spinal origin and peripheral mechanisms

A new technique of multiple-air-gap recording was developed to study the EO activation process in Gymnotus carapo. Using this technique, the spatiotemporal pattern of electromotive force generation was investigated in normal and spinal-lesioned animals.Our data indicate that the EOD may be considered as the result of the sequential activation of 3 defined portions of the EO: the abdominal portion (included in the rostral 25% of the fish body), the central portion (comprising the intermediate 50% of the fish body) and the tail portion (the caudal 25% of the fish body). The EOD generated at each portion is characterized by: 1) timing respect to the pacemaker nucleus discharge, 2) speed of progression within the region, 3) waveform, and 4) magnitude.Spinal sections demonstrated that EMNs serving relatively small portions of the EO are widely distributed (convergence) and that surgical exclusion of relatively small portions of the spinal cord diminishes the amplitude of the EOD along an extended portion of the EO (divergence).Abbreviations EMF electromotive force - EMN electromotor-neurons - EO electric organ - EOD electric organ discharge - PMNFP pacemaker nucleus field potential - PEN posterior electromotor nerve - PNA peripheral neural activity     

Spatial distribution of the medullary command signal within the electric organ of Gymnotus carapo

The pacemaker nucleus of Gymnotus carapo contains two types of neurons: pacemaker cells which set up the frequency of the electric organ discharge (EOD) and relay cells which convey the command signal to the spinal cord. Direct activation of a single relay cell provides enough excitation to discharge a pool of spinal electromotor neurons and electrocytes, generating a small EOD (unit EOD). Different relay cells generate unit EODs of variable size and waveform, indicating the involvement of different groups of electrocytes. A special technique of EOD recording (multiple air-gap) was combined with intracellular stimulation of relay cells to study the spatial distribution within the electric organ (EO) of the command signal arising from different relay cells. Three types of relay cells could be identified: type I commanding the rostral 10% of the EO, type II which distribute their command all along the EO and type III driving the caudal 30%. Waveform analysis of unit EODs indicates that doubly innervated electrocytes which are the most relevant for attaining the specific EOD waveform, receive a favored command from the pacemaker nucleus.Abbreviations CV conduction velocity - EMF electromotive force - EMN electromotor neuron - EO electric organ - EOD electric organ discharge - PN pacemaker nucleus - uEOD unit electric organ discharge     

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     

Spinal mechanisms of electric organ discharge synchronization in Gymnotus carapo

Summary The duration of the electric organ discharge (EOD) in Gymnotus carapo is brief and independent of fish size. Spinal mechanisms involved in electrocyte synchronization were explored by recording spontaneous action potentials of single fibers from the electromotor bulbospinal tract (EBST). Using the field potential of the medullary electromotor nucleus (MEN) as a temporal reference we calculated the orthodromic conduction velocity (CV) of these fibers (range: 10.7–91 m/s).The CVs (in m/s) of fibers recorded at the same level of the spinal cord were significantly different in small and large fish; this difference disappeared when CV were expressed as percentage of body length/ms. Plotting these values against conduction distance (also in %) showed that low CV fibers predominate in the rostral cord while only fast fibers are found at distal levels. Moreover, antidromic stimulation of the distal cord was only effective on high CV fibers. The orthodromic CVs in the distal portion of the recorded fibers were calculated by collision experiments; no significant differences were found between proximal and distal portions.The spatial distribution of CV values within the EBST is proposed to play the main role in synchronizing the electromotoneurons' activity along the spinal cord.Abbreviations EOD electric organ discharge - EO electric organ - EBST electromotor bulbospinal tract - MEN medullary electromotor nucleus - CV conduction velocity - EMN electromotoneuron     

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     

Electric organ morphology of Sternopygus macrurus,a wave-type,weakly electric fish with a sexually dimorphic EOD

In several species of electric fish with a sex difference in their pulse-type electric organ discharge (EOD), the action potential-generating cells of the electric organ (electrocytes) of males are larger and more invaginated compared to females. Androgen treatment of females and juveniles produces a longer-duration EOD pulse that mimics the mature male EOD, with a concurrent increase in electrocyte size and/or membrane infolding. In Sternopygus macrurus, which generates a wave-type EOD, androgen also increases EOD pulse duration. To investigate possible morphological correlates of hormone-dependent changes in EOD in Sternopygus, we examined electric organs from both fish collected in the field, and untreated and androgen-treated specimens in the laboratory. The electrocytes are cigar shaped, with prominent papillae on the posterior, innervated end. Electrocytes of field-caught specimens were significantly larger in all parameters than were electrocytes of specimens maintained in the laboratory. EOD pulse duration and frequency were highly correlated, and were significantly different between the sexes in sexually mature fish. Nevertheless, no sex difference in electrocyte morphology was observed, nor did any parameters of electrocyte morphology correlate with EOD pulse duration or frequency. Further, whereas androgen treatment significantly lowered EOD frequency and broadened EOD pulse duration, there was no difference in electrocyte morphology between hormone-treated and control groups. Thus, in contrast to results from studies on both mormyrid and gymnotiform pulse fish, electrocyte morphology is not correlated with EOD waveform characteristics in the gymnotiform wave-type fish Sternopygus. The data, therefore, suggest that sex differences in EOD are dependent on changes in active electrical properties of electrocyte membranes. © 1992 John Wiley & Sons, Inc.     

From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish,Eigenmannia

Summary During their jamming avoidance response (JAR), weakly electric fish of the genusEigenmannia shift their electric organ discharge (EOD) frequency away from a similar EOD frequency of a neighboring fish. The behavioral rules and neural substrates for stimulus recognition and motor control of the JAR have been extensively studied (see review by Heiligenberg 1986). The diencephalic nucleus electrosensorius (nE) links sensory processing within the torus semicircularis and optic tectum with the mesencephalic prepacemaker nucleus which, in turn, modulates the medullary pacemaker nucleus and hence the EOD frequency. Two separate areas within the nE responsible for JAR-related EOD frequency rises and frequency falls, respectively, were identified by iontophoresis of the excitatory amino acid L-glutamate. Bilateral lesion of the areas causing EOD frequency rises resulted in elimination of JAR-related frequency rises above a baseline frequency obtained in the absence of a jamming stimulus. Similarly, bilateral lesion of the areas causing frequency falls resulted in a loss of JAR-related frequency falls below the baseline frequency. Whether these areas are also responsible for non-JAR-related frequency shifts is not known. The strength of response and spatial extent of the areas causing frequency shifts varied among fish and also varied in individual fish, reflecting the strength of JAR-related frequency shifts and the balance of activities in frequency-rise and frequency-fall areas. Local application of bicuculline-methiodide or GABA demonstrated a tonic inhibitory input to each area and suggests a reciprocal inhibitory interaction between the two ipsilateral areas, possibly accounting for much of the individual plasticity.The nE thus is a site for neuronal transformation from distributed, topographically organized processing within the laminated structures of the torus and tectum to discrete cell clusters which control antagonistic motor responses.Abbreviations EOD electric organ discharge - JAR jamming avoidance response - Df difference frequency between jamming signal and the fish's own EOD - nE nucleus electrosensorius - PPn prepacemaker nucleus     

Commissural neurons of the electrosensory lateral line lobe of Apteronotus leptorhynchus: morphological and physiological characteristics

Extracellular injections of horseradish peroxidase were used to label commissural cells connecting the electrosensory lateral line lobes of the weakly electric fish Apteronotus leptorhynchus. Multiple commissural pathways exist; a caudal commissure is made up of ovoid cell axons, and polymorphic cells' axons project via a rostral commissure. Intracellular recording and labeling showed that ovoid cells discharge spontaneously at high rates, fire at preferred phases to the electric organ discharge, and respond to increased receptor afferent input with short latency partially adapting excitation. Ovoid cell axons ramify extensively in the rostro-caudal direction but are otherwise restricted to a single ELL subdivision. Polymorphic cells are also spontaneously active, but their firing is unrelated to the electric organ discharge waveform. They respond to increased receptor afferent activity with reduced firing frequency and response latency is long. Electrical stimulation of the commissural axons alters the behavior of pyramidal cells in the contralateral ELL. Basilar pyramidal cells are hyperpolarized and nonbasilar pyramidal cells are depolarized by this type of stimulation. The physiological results indicate that the ovoid cells participate in common mode rejection mechanisms and also suggest that the ELLs may function in a differential mode in which spatially restricted electrosensory stimuli can evoke heightened responses.Abbreviations ccELL caudal commissure of the ELL - CE contralaterally excited - DML dorsal molecular layer - ELL electrosensory lateral line lobe - EOD electric organ discharge - HRP horseradish peroxidase - IE ipsilaterally excited - MTI mouth-tail inverted - MTN mouth-tail normal - rcELL rostral commissure of the ELL - TRI transverse inverted - TRN transverse normal     

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     

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     

Waveform generation in Rhamphichthys rostratus (L.) (Teleostei,Gymnotiformes)

Rhamphichthys rostratus (L.) emits brief pulses (2 ms) repeated very regularly at 50 Hz. The electric organ shows a heterogeneous distribution of the electrocyte tubes and the occurrence of three electrocyte types (caudally innervated, rostrally innervated and marginallycaudally innervated). In the sub-opercular region the electric organ consists of a pair of tubes containing only caudally innervated electrocytes. At the abdominal region the EO consists of three pairs of tubes. Each pair contains one of the described electrocyte types. The number of electrocyte tubes increases toward the tail to reach nine or ten pairs in the most caudal segments. In the intermediate region most tubes contain doubly innervated electrocytes except the ventral pair that contains caudally innervated electrocytes. The caudal 25% contains exclusively caudally innervated electrocytes. The electric organ discharge consists of five wave components (V1 to V5). Electrophysiological data are consistent with the hypothesis that V1 results from the activity of the rostral faces of rostrally innervated electrocytes. V2 results from the activities of rostral faces of marginally-caudally innervated electrocytes while V3 results from the activities of caudal faces of most electrocytes. Curarization experiments demonstrated that V4 and V5 result from action potential invasion and are not directly elicited by neural activity.Abbreviations AEN1 anterior electromotor nerve 1 - AEN2 anterior electromotor nerve 2 - BMB boraxic methylene blue - CIE caudally innervated electrocytes - EMF electromotive force - EO electric organ - EOD electric organ discharge - I current amplitude - MCIE marginally-caudally innervated electrocytes - MT medial tubes - PEN posterior electromotor nerve - R _n internal impedance - RIE rostrally innervated electrocytes - Rl load resistor - SAT short abdominal tubes - V voltage amplitude     

Production of aggressive electrocommunication signals to progressively realistic social stimuli in male Apteronotus leptorhynchus

Brown ghost knife fish, Apteronotus leptorhynchus, produce a continuous electric organ discharge (EOD) that they use for communication. While interacting aggressively, males also emit brief EOD modulations termed chirps. The simplicity of this behaior and its underlying neural circuitry has made it an important model system in neuroethology. Chirping is typically assayed by confining a fish in a tube (‘chirp chamber’) and presenting it with sine wave electrical stimuli that partially mimic EODs of other fish. We presented male fish with progressively more realistic social stimuli to examine whether some of the stimulus complexities during dyadic interaction influence the production of chirps. In a chirp chamber, fish chirped less to a recording of an EOD containing chirps than to a recording of an EOD alone and to sine wave stimuli. Free‐swimming fish chirped more to stimulus fish than to sine wave stimuli presented through electrodes. Fish chirped more when interacting directly than when interacting across a perforated barrier. Together, these studies demonstrate that the presence of chirps, electric field complexity, and/or non‐electric social stimuli are important in eliciting chirp production in brown ghosts.     

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fish Paramormyrops kingsleyae

Communication signals serve crucial survival and reproductive functions. In Gabon, the widely distributed mormyrid fish Paramormyrops kingsleyae emits an electric organ discharge (EOD) signal with a dual role in communication and electrolocation that exhibits remarkable variation: populations of P. kingsleyae have either biphasic or triphasic EODs, a feature that characterizes interspecific signal diversity among the Paramormyrops genus. We quantified variation in EODs of 327 P. kingsleyae from nine populations and compared it to genetic variation estimated from microsatellite loci. We found no correlation between electric signal and genetic distances, suggesting that EOD divergence cannot be explained by drift alone. An alternative hypothesis is that EOD differences are used for mate discrimination, which would require P. kingsleyae be capable of differentiating between divergent EOD waveforms. Using a habituation-dishabituation assay, we found that P. kingsleyae can discriminate between biphasic and triphasic EOD types. Nonetheless, patterns of genetic and electric organ morphology divergence provide evidence for hybridization between these signal types. Although reproductive isolation with respect to signal type is incomplete, our results suggest that EOD variation in P. kingsleyae could be a cue for assortative mating.     

The development of the Jamming Avoidance Response (JAR) in Eigenmannia: An innate behavior indeed

Summary In its Jamming Avoidance Response (JAR), the gymnotiform electric fish Eigenmannia shifts its electric organ discharge (EOD) frequency away from similar interfering frequencies. Continual behavioral measurements were carried out in 164 juvenile fish until a correct JAR emerged. Sixty-four of these fish were raised in complete isolation, the remainder in a community of their siblings. A correct JAR emerged in fish of 1.2–1.6 cm in body length, corresponding to a developmental age of 24–32 days. In 6 of 164 fish, the emergence of a correct JAR followed an interim appearance of an incorrect JAR, which involved frequency shifts in the direction opposite to those of a correct JAR. The fish raised in isolation developed the same forms of behavior and showed the same sequence in their appearance as did socially raised fish. This indicates that the JAR and its developmental schedule are innate. The appearance of an incorrect JAR suggests initial errors or incompleteness in the wiring of central nervous connections. A correct JAR ultimately emerged even if a stimulus regimen was offered that rewarded frequency shifts in the direction opposite to those of a correct JAR. This indicates that the development of the JAR is immune to experimental alterations of sensory experience.Abbreviations Df frequency difference between a jamming stimulus and fish's EOD - ELL electrosensory lateral line lobe - EO electric organ - EOD electric organ discharge - JAR Jamming Avoidance Response - nE nucleus electrosensorius - nE subnucleus of nE, causing drop of EOD frequency - nE subnucleus of nE, causing rise of EOD frequency - Pn pacemaker nucleus - PPn prepacemaker nucleus     

Hormone-induced and maturational changes in electric organ discharges and electroreceptor tuning in the weakly electric fishApteronotus

Summary Plasticity in the frequency of the electric organ discharge (EOD) and electroreceptor tuning of weakly electric fish was studied in the genusApteronotus. Both hormone-induced and maturational changes in EOD frequency and electroreceptor tuning were examined.Apteronotus is different from all other steroid-responsive weakly electric fish in that estradiol-17, rather than androgens, induces discharge frequency decreases. This result can account for the reversed discharge frequency dimorphism found inApteronotus in which, counter to all other known sexually dimorphic electric fish, females have lower discharge frequencies than males. Studies of electroreceptor tuning inApteronotus indicate that electroreceptors are closely tuned to the frequency of the EOD. This finding was noted not only in adult animals, but also in juvenile animals shortly after the onset of their EODs. Tuning plasticity inApteronotus, as in other species studied, is associated with altered EOD frequencies and was noted in both maturational EOD changes and in estrogen-induced changes. Thus, tuning plasticity appears to be a general phenomenon which occurs concurrent with a variety of EOD changes.     

Electric organ discharges of the gymnotiform fishes: III. Brachyhypopomus

We measured and mapped the electric fields produced by three species of neotropical electric fish of the genus Brachyhypopomus (Gymnotiformes, Rham phichthyoidea, Hypopomidae), formerly Hypopomus. These species produce biphasic pulsed discharges from myogenic electric organs. Spatio-temporal false-color maps of the electric organ discharges measured on the skin show that the electric field is not a simple dipole in Brachyhypopomus. Instead, the dipole center moves rostro-caudally during the 1st phase (P1) of the electric organ discharge, and is stationary during the 2nd phase (P2). Except at the head and tip of tail, electric field lines rotate in the lateral and dorso-ventral planes. Rostro-caudal differences in field amplitude, field lines, and spatial stability suggest that different parts of the electric organ have undergone selection for different functions; the rostral portions seem specialized for electrosensory processing, whereas the caudal portions show adaptations for d.c. signal balancing and mate attraction as well. Computer animations of the electric field images described in this paper are available on web sites http://www.bbb.caltech.edu/ElectricFish or http://www.fiu.edu/∼stoddard/electricfish.html. Accepted: 22 September 1998     

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.