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.     

Basal expansion of anal-fin rays: a new osteological character in weakly discharging electric fish (Mormyridae)

Bone expansion of anal-fin rays in mormyrid fish is introduced as a new osteological character to distinguish two mormyrid species, Brienomyrus brachyistius from Nigeria and Brienomyrus kingsleyae from Gabon. This character is sexually dimorphic and species-specific, affecting the bases of anal-fin rays in adult males only. Between the two species, it differed in degree, the number of rays involved, and the number of the first ray affected. These differences together with differences in conventional meristic and morphometric characters further support ongoing revisions of Brienomyrus taxonomy.     

Spectral sensitivity of the weakly discharging electric fish Gnathonemus petersi using its electric organ discharges as the response measure

The spectral sensitivity of the weakly electric mormyrid fish Gnathonemus petersi was investigated under dark- and light-adapted conditions using a transient change (startle) in its electric organ discharge (EOD) rate as response measure. The startle was resistant to habituation and graded with light intensity. Under both lighting conditions, the fish responded optimally to a monochromatic light of 525 nm. A porphyropsin pigment (520–540₂) appears to mediate spectral sensitivity over most of the visible spectrum. However, G. petersi responded more strongly to 625- and 675-nm lights (dark- and light-adapted fish) and a 725-nm light (light-adapted fish only) than predicted by the presence of a single rod pigment. These data suggest that at least one additional visual pigment (most likely of cone cells) maximally absorbing long wavelength light (600 nm or longer) is present. The spectral sensitivity data are consistent with the sensitivity hypothesis in that heightened sensitivity to long wavelength light is predicted for fish living in blackwater habitats which are characterized typically by low light levels and transmission of predominantly long wavelengths. Histology of the retina showed photoreceptors grouped into bundles and ensheathed by pigment epithelial cells. Our results demonstrated a functional visual sense in a species of fish much better known and studied for its electrosensory and electromotor abilities.     

The function of agonistic display behaviours in Gnathonemus petersii

In pairs of interacting Gnathonemus petersii , a mormyrid electric fish, dominant individuals were larger (longer body). Pairs of interacting fish of similar body size emitted more parallel displays at the onset of an interaction. Over the course of 10 min interactions, head butting increased and parallel display decreased. This decrease occurred primarily in pairs that contained a prior resident and intruder, as compared with two intruders. The patterns of electric organ discharge during parallel display, and the possible sensory modalities mediating this behaviour are discussed.     

Central connections of the olfactory bulb in the weakly electric fish,Gnathonemus petersii

Summary We have investigated the central connections of the classical olfactory system in the weakly electric fish Gnathonemus petersii using HRP and cobalt labelling techniques. The olfactory bulb projects bilaterally via the medial and lateral olfactory tracts to restricted areas of the telencephalon, namely to its rostromedial, lateral and posterior medial parts. The most extensive telencephalic target is the posterior terminal field, which arcs around the lateral forebrain bundle at levels posterior to the anterior commissure. Projections to the contralateral hemisphere cross in the ventral telencephalon rostral to the anterior commissure and via the posterior dorsal part of the anterior commissure; endings are also present within the anterior commissure. Bilateral projections to the preoptic area, to the nucleus posterior tuberis and to an area in the thalamus are apparent. In all cases, contralateral projections are less extensive than those on the side ipsilateral to the injected bulb. A projection via the medial olfactory tract can be followed to the contralateral bulb. Following injections into the olfactory bulb, retrogradely labelled neurons are found in the contralateral bulb and in six telencephalic areas; they are also present in the periventricular diencephalon and in an area lateral to the nucleus posterior tuberis. The present results support the suggestion that a reduction in olfactory input to the telencephalon occurs together with increased telencephalic differentiation in actinopterygian fishes.     

Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii

Weakly electric fish use active electrolocation for orientation at night. They emit electric signals (electric organ discharges) which generate an electrical field around their body. By sensing field distortions, fish can detect objects and analyze their properties. It is unclear, however, how accurately they can determine the distance of unknown objects. Four Gnathonemus petersii were trained in two-alternative forced-choice procedures to discriminate between two objects differing in their distances to a gate. The fish learned to pass through the gate behind which the corresponding object was farther away. Distance discrimination thresholds for different types of objects were determined. Locomotor and electromotor activity during distance measurement were monitored. Our results revealed that all individuals quickly learned to measure object distance irrespective of size, shape or electrical conductivity of the object material. However, the distances of hollow, water-filled cubes and spheres were consistently misjudged in comparison with solid or more angular objects, being perceived as farther away than they really were. As training continued, fish learned to compensate for these 'electrosensory illusions' and erroneous choices disappeared with time. Distance discrimination thresholds depended on object size and overall object distance. During distance measurement, the fish produced a fast regular rhythm of EOD discharges. A mechanisms for distance determination during active electrolocation is proposed.     

Discrimination of objects through electrolocation in the weakly electric fish,Gnathonemus petersii

Summary Three weakly electric fish (Gnathonemus petersii) were force-choice trained in a two-alternative procedure to discriminate between objects differing in their electrical characteristics. The objects were carbon dipoles in plexiglass tubing (length 2.5 cm, diameter 0.6 cm). Their electrical characteristics could be changed by varying the impedance of an external circuit to which they were connected (Fig. 1). In one (the capacitance dipole) the resistance was very low(< 3 ) and the capcitance variable. In the other (the resistance dipole) the resistance was variable and the capacitance low (<50 pF).Capacitances from several hundred pF (lower thresholds, Fig. 2) to several hundred nF (upper thresholds, Fig. 3) could be discriminated from both insulators and good conductors. In all cases the reward-negative stimulus was the capacitance dipole, which was avoided by all fish spontaneously. Thresholds were defined at 70% correct choices.The fish were then tested for their ability to discriminate between one object with a given capacitance and another with resistances varying from 3 to 200 k. The capacitance dipole continued to be the negative stimulus throughout. All 3 fish avoided it in at least 80% of the trials at each stimulus combination (Fig. 4). This result suggests that Gnathonemus perceives the capacitance and the resistance of objects differentially.The effect of the dipole-objects as well as some natural objects on the local EOD was recorded differentially very close to the fish's skin (Fig. 5). The amplitude of the local EODs was affected by all types of objects as they approached the skin. However, the waveform was changed only by capacitance dipoles and some natural objects (Figs. 6 and 7). It appears that the fish perceive not only intensity changes in the local EOD but wave-form deformations as well and can thus distinguish objects of different complex impedances.Abbreviations EOD electric organ discharge - f _max maximal spectral frequency - GP Gnathonemus petersii - LFS local filtered signal - PMA probing motor act - S+ positive stimulus - S negative stimulus     

Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii.

Weakly electric fish use active electrolocation for orientation at night. They emit electric signals (electric organ discharges) which generate an electrical field around their body. By sensing field distortions, fish can detect objects and analyze their properties. It is unclear, however, how accurately they can determine the distance of unknown objects. Four Gnathonemus petersii were trained in two-alternative forced-choice procedures to discriminate between two objects differing in their distances to a gate. The fish learned to pass through the gate behind which the corresponding object was farther away. Distance discrimination thresholds for different types of objects were determined. Locomotor and electromotor activity during distance measurement were monitored. Our results revealed that all individuals quickly learned to measure object distance irrespective of size, shape or electrical conductivity of the object material. However, the distances of hollow, water-filled cubes and spheres were consistently misjudged in comparison with solid or more angular objects, being perceived as farther away than they really were. As training continued, fish learned to compensate for these 'electrosensory illusions' and erroneous choices disappeared with time. Distance discrimination thresholds depended on object size and overall object distance. During distance measurement, the fish produced a fast regular rhythm of EOD discharges. A mechanisms for distance determination during active electrolocation is proposed.     

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

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

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     

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).     

A well defined spinocerebellar system in the weakly electric teleost fish Gnathonemus petersii. A tracing and immuno-histochemical study.

Long ascending fiber systems were investigated in the spinal cord of a teleost fish, Gnathonemus petersii. Concomitant results of Fink-Heimer degeneration tracing as well as CaBP28K immunohistochemical labelling demonstrate the existence of a well defined direct pathway from the very lowest spinal level to the caudal lobe of the cerebellum. HRP retrograde labelling shows that this pathway originates in a cellular column located in the most ventral part of the lateral column next to the lateral extremity of the ventral horn. From each spinal segment, the large axons of these cells gather and form a strip shaped tract at the periphery of the lateral column immediately dorsal to the cell column from which they originate. The spinal course of these fibers is ipsilateral; they give off a large number of collaterals to the lateral reticular nucleus. Bypassing the trigeminal motor nucleus, the lateral column tract courses dorsally to the paratrigeminal command associated nucleus between the lateral lemniscus and the nucleus preeminentialis and with a ventro-dorsally oriented large loop, turns in the caudal direction and penetrates into the cerebellar caudal lobe. Running caudally in the dorsal granular layer of the caudal lobe, it shifts more and more medially and crosses the midline whilst decussating with the contralateral tract on the dorsal margin of the molecular layer of the caudal lobe. Finally, the tract splits off and terminates throughout the granular layer of the caudal lobe. The main characteristics of this pathway are similar to those of the ventral spinocerebellar tract of higher vertebrates; it conveys information from all spinal levels directly to the contralateral cerebellum. However, it does not seem to receive direct synaptic input from the periphery, since projection of the dorsal root fibers appears to be limited to the dorsal ipsilateral half of the spinal cord. The appearance of such a pathway in a teleost fish is probably related to the existence of a well developed proprioceptive system in this species.     

Electroreceptor model of weakly electric fish Gnathonemus petersii: II. Cellular origin of inverse waveform tuning.

In part I (. Biophys. J. 75:1712-1726), we presented a cellular model of the A- and B-electroreceptors of the weakly electric fish Gnathonemus petersii. The model made clear the cellular origin of the differences in the response functions of A- and B-receptors, which sensitively code the intensity of the fish's own electric organ discharge (EOD) and the variations in the EOD waveform, respectively. The main purpose of the present paper is to clarify the cellular origin of the inverse waveform tuning of the B-receptors by using the receptor model. Inverse waveform tuning means that B-receptors respond more sensitively to the 180 degrees inverted EOD than to undistorted or less distorted EODs. We investigated how the A- and B-receptor models respond to EODs with various waveforms, which are the phase-shifted EODs, whose shift angle is varied from -1 degrees to -180 degrees, and single-period sine wave stimuli of various frequencies. We show that the tuning properties of the B-receptors arise mainly from the combination of two attributes: 1) The waveform of the stimuli (Bstim) effectively sensed by the B-receptor cells. This consists of a first smaller and a second larger positive peak, even though in the original phase-shifted EOD stimuli, the amplitudes of the two positive peaks are reversed. 2) The effective time constant of dynamical response of the receptor cells. It is on the order of the duration of a single EOD pulse. We also calculated the response properties of the A- and B-receptor models when stimulated with natural EODs distorted by various capacitive and resistive objects. Furthermore, we investigated the effect of EOD amplitude on the receptor responses to capacitive and resistive objects. The models presented can systematically reproduce the experimentally observed response properties of natural A- and B-receptor cells. The mechanism producing these properties can be reasonably explained by the variation in the stimulus waveforms effectively sensed by the A- and B-receptor cells and by time constants.     

Ionic currents that contribute to a sexually dimorphic communication signal in weakly electric fish

Weakly electric fish produce a communication signal, the electric organ discharge, that is species specific, and in many species, sexually dimorphic. Because the neural circuit that controls the electric organ discharge is relatively simple, it is an excellent model in which to study both the biophysical mechanisms underlying a rhythmic behavior and the neuroendocrine control of a sexually dimorphic behavior. By studying the effects of ion channel blockers on neurons in the medullary pacemaker nucleus, I pharmacologically characterized three ionic currents that influence the pacemaker rhythm, and thus electric organ discharge frequency, in the gymnotiform fish, Apteronotus leptorhynchus. These currents included a tetrodotoxin-sensitive sodium current; a potassium current that was sensitive to 4-aminopyridine; and a calcium current that was sensitive to nickel and cadmium, but resistant to specific blockers of L-, N-, P-, and Q-type calcium currents. The pharmacological profiles of the ionic currents in the pacemaker nucleus are similar to those of ionic currents involved in pacemaking in other neuronal oscillators. Because these ionic currents dramatically influence pacemaker firing frequency, which is directly related to electric organ discharge frequency, these ionic currents are likely targets of steroid hormone action in producing sexual dimorphisms in electric organ discharge frequency. Additional studies are needed to determine how these ionic currents interact to generate the electric organ discharge rhythm and to investigate the possibility that sexual dimorphism in the electric organ discharge results from the actions of gonadal steroids on these ionic currents. Accepted: 3 June 1999     

Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii)

Weakly electric fishes are nocturnal and orientate in the absence of vision by using their electrical sense. This enables them not only to navigate but also to perceive and recognize objects in complete darkness. They create an electric field around their bodies by producing electric signals with specialized electric organs. Objects within this field alter the electric current at electroreceptor organs, which are distributed over almost the entire body surface. During active electrolocation, fishes detect, localize and analyse objects by monitoring their self-produced electric signals. We investigated the ability of the mormyrid Gnathonemus petersii to perceive objects three-dimensionally in space. Within a range of about 12 cm, G. petersii can perceive the distance of objects. Depth perception is independent of object size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters (maximal slope and maximal amplitude) of the electrical image which each object projects onto the fish's skin. During active electrolocation, electric fishes cannot only locate objects in space but in addition can determine the three-dimensional shape of an object. Up to certain limits, objects are spontaneously categorized according to their shapes, but not according to their sizes or the materials of which they are made.     

Differential responses of two types of electroreceptive afferents to signal distortions may permit capacitance measurement in a weakly electric fish,Gnathonemus petersii

Summary Gnathonemus petersii discriminates between ohmic and capacitive objects. To investigate the sensory basis of this discrimination we recorded from primary afférents that innervate either A or B mormyromast sensory cells. Modified and natural electric organ discharges were used as stimuli. In both A and B fibres frequencies below the peak-power frequency (3.8 to 4.5 kHz) of the electric organ discharge caused minimal first-spike latencies and a maximum number of spikes. A fibres did not discriminate phase-shifted stimuli, whereas B fibres responded significantly with a decrease in first-spike latency if the phase shift was only — 1°. In both A and B fibres an amplitude increase caused a decrease in spike latency and an increase in spike number; an amplitude decrease had the reverse effect. If stimulated with quasi-natural electric organ discharges distorted by capacitive objects, the responses of A fibres decreased with increasing signal distortion. In contrast, the responses of B fibres increased until amplitude effects began to dominate. Gnathonemus may use the physiological differences between A and B fibres to detect and discriminate between capacitive and purely ohmic objects.Abbreviations ELL electrosensory lateral line lobe - EOD electric organ discharge - LFS local filtered signal - p-p peak-to-peak     

Spatial aspects of electrolocation in the mormyrid fish, Gnathonemus petersii

The range of electrolocation in the weakly electric fish, Gnathonemus petersii, was determined for plastic and aluminium cubes. A characteristic change in the fish's EOD activity, and abrupt change to more uniform EOD intervals (regularization), was used as the criterion for object detection. The average response distances extending laterally from the fish's longitudinal axis were significantly different (p less than 0.05) for the aluminium cube (5.4 cm) and the plastic cube (7.0 cm).     

Electroreceptor model of the weakly electric fish Gnathonemus petersii. I. The model and the origin of differences between A- and B-receptors.

We present an electroreceptor model of the A- and B-receptors of the weakly electric fish Gnathonemus petersii. The model consists of a sensory cell, whose membrane is separated into an apical and basal portions by support cells, and an afferent fiber. The apical membrane of the cell contains only leak channels, while the basal membrane contains voltage-sensitive Ca2+ channels, voltage-sensitive and Ca2+-activated K+ channels, and leak channels. The afferent fiber is described with the modified Hodgkin-Huxley equation, in which the voltage-sensitive gate of the K+ channels is a dynamic variable. In our model we suggest that the electroreceptors detect and process the information provided by an electric organ discharge (EOD) as follows: the current caused by an EOD stimulus depolarizes the basal membrane to a greatly depolarized state. Then the release of transmitter excites the afferent fiber to oscillate after a certain time interval. Due to the resistance-capacitance structure of the cells, they not only perceive the EOD intensity, but also sense the variation of the EOD waveform, which can be strongly distorted by the capacitive component of an object. Because of the different morphologies of A- and B-cells, as well as the different conductance of leak ion channels in the apical membrane and the different capacitance of A- and B-cells, A-receptors mainly respond to the EOD intensity, while B-receptors are sensitive to the variation of EOD waveform.     

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.     

Serotonergic activation of 5HT1A and 5HT2 receptors modulates sexually dimorphic communication signals in the weakly electric fish Apteronotus leptorhynchus

Serotonin modulates agonistic and reproductive behavior across vertebrate species. 5HT_1A and 5HT_1B receptors mediate many serotonergic effects on social behavior, but other receptors, including 5HT₂ receptors, may also contribute. We investigated serotonergic regulation of electrocommunication signals in the weakly electric fish Apteronotus leptorhynchus. During social interactions, these fish modulate their electric organ discharges (EODs) to produce signals known as chirps. Males chirp more than females and produce two chirp types. Males produce high-frequency chirps as courtship signals; whereas both sexes produce low-frequency chirps during same-sex interactions. Serotonergic innervation of the prepacemaker nucleus, which controls chirping, is more robust in females than males. Serotonin inhibits chirping and may contribute to sexual dimorphism and individual variation in chirping. We elicited chirps with EOD playbacks and pharmacologically manipulated serotonin receptors to determine which receptors regulated chirping. We also asked whether serotonin receptor activation generally modulated chirping or more specifically targeted particular chirp types. Agonists and antagonists of 5HT_1B/1D receptors (CP-94253 and GR-125743) did not affect chirping. The 5HT_1A receptor agonist 8OH-DPAT specifically increased production of high-frequency chirps. The 5HT₂ receptor agonist DOI decreased chirping. Receptor antagonists (WAY-100635 and MDL-11939) opposed the effects of their corresponding agonists. These results suggest that serotonergic inhibition of chirping may be mediated by 5HT₂ receptors, but that serotonergic activation of 5HT_1A receptors specifically increases the production of high-frequency chirps. The enhancement of chirping by 5HT_1A receptors may result from interactions with cortisol and/or arginine vasotocin, which similarly enhance chirping and are influenced by 5HT_1A activity in other systems.