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     

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     

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     

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.     

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.     

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.     

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).     

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.     

The effects of captivity on the electric organ discharge and plasma hormone levels in Gnathonemus petersii (Mormyriformes)

1. Experiment 1 employed a repeated measures design to examine the effects of captivity on sex differences in the electric organ discharge (EOD) of Gnathonemus petersii, newly imported from Africa, and maintained individually or in groups.
2. On the day of import, males exhibited longer durations of phases 2 and 3 of the EOD and lower peak power spectral frequencies (PPSFs) than females.
3. After 14 days in captivity in the laboratory, the sex differences were eliminated. After 37 days of captivity, all sex differences were still abolished, or even reversed depending on housing conditions. Males exhibited the most dramatic changes in EODs and females appeared to have higher testosterone (T) levels than males.
4. Experiment 2 was designed to investigate the effects of captivity on both behavior and endocrine status in 58 newly imported males. In this independent group design, EOD data and blood were collected from subjects over 15 days.
5. Decreases in phase 3 of the EOD and increases in PPSFs progressed over the 15 day experimental period, becoming statistically significant by days 10 and 15, respectively. Regardless of housing conditions, both T and 11-keto T dramatically decreased to near non-detectable levels by Day 5 in the laboratory.
6. Captivity causes rapid and profound changes in the endocrine system which result in dramatic changes in steroid-sensitive EODs. These findings directly link captivity, hormones, and behavior, and show why feral animals brought into captivity usually do not exhibit sexual behavior.

     

Auditory sensitivity and psychophysical tuning curves in the elephant nose fish,Gnathonemus petersii

Summary Hearing sensitivity and psychophysical tuning curves were determined for the mormyridGnathonemus petersii. Pure tone hearing thresholds were determined from 100 Hz to 2,500 Hz, with best sensitivity being about –31 dB (re: 1 dyne/ cm²) from 300 Hz to 1,000 Hz. In order to determine frequency tuning of the auditory system, psychophysical tuning curves (PTC's) were measured with the masker presented simultaneously with, or just ahead of, the 500 Hz test signal. The sound level for different frequencies needed to just mask the test tone were determined from 100 to 800 Hz. Maximum masking occurred in both forward and simultaneous conditions when the masker and the test tone were at the same frequency. As the masker was moved in frequency from 500 Hz, higher sound levels of maskers were needed to afford masking of the test tone. The data were similar in simultaneous and forward masking, with theQ _{10 dB}, a measure of sharpness of tuning, being about 5 in both cases. Data were compared for other species for which behavioral thresholds and PTC's are available.Gnathonemus hears about as wide a range of frequencies as the goldfish,Carassius auratus, although the PTC's for the two species are strikingly different. The PTC's forGnathonemus resemble those determined in a forward-masking paradigm for the clown knife fish,Notopterus chitala, even thoughGnathonemus has a wider hearing bandwidth.Abbreviations AM amplitude modulated - EOD electric organ discharge - PTC psychophysical tuning curve     

Sensory nerve endings of highly mobile structures in two marine teleost fishes

Summary With the use of a whole mount silver impregnation technique, sensory nerve endings were located in the connective tissue at the base of the modified pectoral fin ray in the gurnard,Aspitrigla cuculus, and within the perichondrium of the barbel in the goatfish,Mullus surmuletus. The location of these endings and their planar receptory fields in such highly mobile structures, suggests that the sensory endings are proprioceptive in nature and that they are associated in monitoring the positional state of the modified pectoral fin ray and barbel, respectively, during voluntary movement. This investigation addresses itself to the general problem of proprioception in teleost fishes and provides histological evidence for the presence of proprioceptive nerve endings.     

Cytochemistry and distribution of polysaccharides in an electroreceptor: the tuberous organ of Gnathonemus petersii (Mormyrids).

The polysaccharides were studied in an electroreceptor organ, the tuberous organ of Gnathonemus petersii (Mormyridae). Histochemical methods (P.A.S., alcian blue, toluidine blue and iron colloidal reactions) allowed us to demonstrate the existence of glycogen in the sensory cytoplasm, and P.A.S. positive polysaccharides in the sensory cavity. The polysaccharides were shown to be amylase proof; they display an acidity due to the existence of sulphated radicals. The histochemical study was completed by a cytochemical analysis: a treatment with thiocarbohydrazide (TCH) according to the Thiery's method. This method allowed us to estimate the glycogen concentration, its localization, and relationship with cellular organites within the sensory cytoplasm, as well as to differentiate the highly glycogenous type II cells of the platform from the other accessory cells (Derbin and Szabo, 1968). After a treatment for 20 hours with TCH, silver stained grains were visible on the polysaccharide filaments of the sensory chamber, between the microvilli and the vacuoles of the epidermal cells lining to the sensory cavity. Silver grains coated the outer surface of the microvilli. Such polysaccharides were not identical to the filamentous polysaccharides of the cavity. In order to determine the cytochemical localization of the polysaccharide acid groups, sections were stained with iron salts. The colloidal iron constitutes a deposit opaque to electrons and located both on the filamentous polysaccharides of the sensory cavity and in the vacuoles of the epidermal cells, indicating that only these filamentous polysaccharides display acid radicals.     

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     

Convergence of electrotonic club endings,GABA- and serotoninergic terminals on second order neurons of the electrosensory pathway in mormyrid fish,Gnathonemus petersii and Brienomyrus niger (Teleostei)

Summary Previous electrophysiological data indicate that the afferent electrosensory impulses conveyed towards the mesencephalon are blocked in the rhombencephalic electrosensory lateral line nucleus (nELL) by the concomitantly occurring EOD (electric organ discharge) command-associated (corollary) discharge. Electron-microscopic observations and anterograde labeling with horseradish peroxidase show that the primary electrosensory fibers terminate with club endings on the adendritic soma of the nELL cells and form gap junctions with the postsynaptic membrane. The remaining part of the soma and the initial segment membrane of nELL cells are covered with a large number of boutons showing chemical synaptic profiles. The GABA-ergic (gamma-aminobutyric-acid) nature of the majority of the boutons is revealed immunocytochemically by anti-GABA and anti-glutamic acid decarboxylase (anti-GAD) antisera, as seen in the light microscope. Electron-microscopic examination confirms the GABAergic nature of most of the bouton-like terminals, whereas club endings show negative immunoreactivity. In addition, serotonin-immunoreactive fibers and boutons are found in the same nucleus, between and next to the nELL cells. It is suggested that the GABAergic endings are the morphological basis for the inhibition that occurs in the nELL and that is mediated by the corollary discharge.     

Adenosine triphosphatases in electroreceptor organs (ampullary organs and mormyromasts) of Gnathonemus petersii Mormyridae

Summary Cytochemical techniques were used for the light and electron microscopical localization of ATPase in the ampullary organ and the mormyromast, both cutaneous electroreceptors inGnathonemus petersii (Mormyridae).At the light microscope level, two different techniques gave the same results, namely that high concentrations of the enzyme are present in the mormyromast and certain epidermal cells and weak concentrations in the ampullary organ.The enzyme was localized at the ultrastructural level using the lead capture method. It was found in the cytoplasm of type III accessory cells of the ampullary organ, in the apical cytoplasm of SC1 sensory cells and the accessory cells surrounding them and on the membrane of the SC2 sensory cells of the mormyromast. The ATPase of these various cells was inhibited byp-chloromercuribenzoate.The enzyme in the mormyromast SC1 and their accessory cells was not dependent on Mg²⁺ ions. However, that in the type III accessory cells of the ampullary organ and in the SC2 of the mormyromast was strictly dependent on Mg²⁺. In addition, there was a Ca²⁺-dependent ATPase in the microvilli of the SC2 of certain mormyromasts.     

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.