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.     

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     

Variations of glycogen: II. Following deafferentation of Knollenorgan sensory cells,a lateral line electroreceptor of mormyrid fish

The effect of deafferentation on glycogen metabolism was studied in the sensory cells of mormyrid Knollenorgan electroreceptors. Glycogen was visualized in the sensory cells after fixation in a solution containing potassium ferricyanide and osmium tetroxide. The density variations of glycogen were evaluated by a morphometric method. Sectioning of the afferent nerve results in a cessation of the spontaneous receptor cells activity after 48 h and the glycogen content of these cells increases three fold in the first 5 days after nerve transection. From day 5 on, the glycogen concentration diminishes progressively until day 13. After the sensory cells had become completely deformed, the quantification of glycogen particles was no longer possible and the degeneration of the sensory cells was complete within 20 days after nerve section. These results show that (1) the afferent nerve fibre is indispensable for the anatomo-functional maintenance of the sensory cells and (2) the nerve has only an indirect influence on glycogen variations within the sensory cells.     

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     

Variations of glycogen: I. Following stimulation of Knollenorgan sensory cells,a lateral line electroreceptor of mormyrid fish

The metabolism of glycogen was studied in sensory cells of the mormyrid fish, Gnathonemus petersii. Knollenorgans, specific cutaneous electroreceptor organs of the lateral line system, have a spontancous electrical activity and their resting discharge in the absence of stimulation is about 0.04 kHz. Various types of stimulation can produce an increase in frequency; the highest frequency (1.30 kHz) is obtained by moving the Knollenorgan above water level. Glycogen was visualized in ultrathin sections after fixation in a solution of potassium ferricyanide and osmium tetroxide. The density of glycogen particles was determined morphometrically in sensory cells before stimulation, after high-frequency activity, and after reimmersion in water. An increase in the electrical activity of the Knollenorgan resulted in a decrease of the glycogen content of sensory cells. The glycogen store was replenished to about 85% of control within 40 min after stimulation and subsequent reimmersion. The results demonstrate that glycogen in the sensory cells of the Knollenorgan represents an energy source which can be catabolized during high electrical activity and replenished during rest.     

The African wave-type electric fish,Gymnarchus niloticus,lacks corollary discharge mechanisms for electrosensory gating

Gymnarchus niloticus, a wave-type African electric fish, performs its jamming avoidance response by relying solely upon afferent signals and does not use corollary discharges from the pacemaker nucleus in the medulla which generates the rhythmicity of electric organ discharges. This is in sharp contrast to the mode of sensory processing found in closely related African pulse-type electric fishes where afferent signals are gated by corollary discharges from the pacemaker for the distinction of exafferent and reafferent stimuli. Does Gymnarchus still possess a corollary discharge mechanism for other behavioral tasks but does not use it for the jamming avoidance response? In this study, I recorded from and labeled medullary neuronal structures that either generate or convey the pacemaker signal for electric organ discharges to examine whether this information is also sent directly to any sensory areas. The pacemaker nucleus was identified as the site of generation of the pacemaking signal. The pacemaker neurons project exclusively to the lateral relay nucleus which, in turn projects exclusively to the medial relay nucleus. Neurons in the medial relay nucleus send unbranched axons to the spinal electromotoneurons. These neurons are entirely devoted to drive the electric organ discharges, and no axon collaterals from these neurons were found to project to any sensory areas. This indicates that Gymnarchus does not possess the neuronal hardware for a corollary discharge mechanism.     

Androgen binding in the brain and electric organ of a mormyrid fish

Summary The mormyrid fish of Africa produce a weak electric pulse called an Electric Organ Discharge (EOD) that functions in electrical guidance and communication. TheEOD waveform describes the appearance of a single pulse which is produced by the electric organ's excitable cells, the electrocytes. For some species, there is a sex difference in the appearance and duration of the EOD waveform, which is under the control of gonadal steroid hormones. We now show, using biochemical techniques, that the steroid-sensitivity of the myogenic electric organ correlates with the presence of comparatively high levels of androgen-binding activity in the cytosol of electrocytes.TheEOD rhythm describes the rate at which the electric organ fires and is under the control of a central electromotor pathway. Sex differences have also been described for the EOD rhythm. Using steroid autoradiographic techniques, we found uptake of tritium-labelled dihydrotestosterone (³H-DHT) by cells within the reticular formation that lie adjacent to the medullary relay nucleus which innervates the spinal electromotoneurons that excite the electric organ. However, no DHT-binding was observed in the relay or electromotor nuclei.Steroid-concentrating cells were also found in several other brainstem regions, the hypothalamus, and the thalamus. In particular, a group of DHT-concentrating, motoneuron-like cells were observed in the caudal medulla and were identified as aswimbladder orsonic motor nucleus.The biochemical data suggest that the electric organ has evolved a sensitivity to gonadal steroid hormones that may underlie the development of known sex differences in the EOD waveform. The autoradiographic results suggest that if steroids do affect the development of sex differences in the EOD rhythm, it is at some level removed from known spinal and medullary electromotor nuclei.Abbreviations ac anterior commissure - AD area dorsalis telencephali - AV area ventralis telencephali - CBL cerebellum - DT dorsal thalamus - E electromotoneuron - En entopeduncular nucleus,ef lateral line efferent nucleus - EG eminentia granularis - ELLL electroreceptive lateral line lobe,EO electric organ,FV folded part of valvula of cerebellum - H hypothalamus - M mesencephalon - MO medulla oblongota - OB olfactory bulb - OT optic tectum - PO preoptic area - R medullary relay nucleus - rf reticular formation - SC spinal cord - SMN sonic motor nucleus - T telencephalon - TP posterior tuber of diencephalon - TS torus semicircularis - UV unfolded part of valvula of cerebellum,v ventricle - VT ventral thalamus     

Phantoms in the brain: Ambiguous representations of stimulus amplitude and timing in weakly electric fish

In wave-type weakly electric fish, two distinct types of primary afferent fibers are specialized for separately encoding modulations in the amplitude and phase (timing) of electrosensory stimuli. Time-coding afferents phase lock to periodic stimuli and respond to changes in stimulus phase with shifts in spike timing. Amplitude-coding afferents fire sporadically to periodic stimuli. Their probability of firing in a given cycle, and therefore their firing rate, is proportional to stimulus amplitude. However, the spike times of time-coding afferents are also affected by changes in amplitude; similarly, the firing rates of amplitude-coding afferents are also affected by changes in phase. Because identical changes in the activity of an individual primary afferent can be caused by modulations in either the amplitude or phase of stimuli, there is ambiguity regarding the information content of primary afferent responses that can result in ‘phantom’ modulations not present in an actual stimulus. Central electrosensory neurons in the hindbrain and midbrain respond to these phantom modulations. Phantom modulations can also elicit behavioral responses, indicating that ambiguity in the encoding of amplitude and timing information ultimately distorts electrosensory perception. A lack of independence in the encoding of multiple stimulus attributes can therefore result in perceptual illusions. Similar effects may occur in other sensory systems as well. In particular, the vertebrate auditory system is thought to be phylogenetically related to the electrosensory system and it encodes information about amplitude and timing in similar ways. It has been well established that pitch perception and loudness perception are both affected by the frequency and intensity of sounds, raising the intriguing possibility that auditory perception may also be affected by ambiguity in the encoding of sound amplitude and timing.     

Androgen correlates of socially induced changes in the electric organ discharge waveform of a mormyrid fish

Weakly electric fish from the family Mormyridae produce pulsatile electric organ discharges (EODs) for use in communication. For many species, male EODs are seasonally longer in duration than those of females, and among males, there are also individual differences in EOD duration. While EOD elongation can be induced by the administration of exogenous androgens, androgen levels have never before been assessed under natural or seminatural conditions. By simulating the conditions occurring during the breeding season in the laboratory, we provide evidence of a sex difference in EOD duration as well as document levels of circulating androgens in males. In this study, we analyzed the nature of social influences on male EOD duration and plasma androgen levels in Brienomyrus brachyistius. Individual males, first housed with a single female and then placed into social groups consisting of three males and three females, showed status-dependent changes in EOD duration. Top-ranking males experienced a relatively large increase in EOD duration. Second-ranking males experienced a more modest increase, and low-ranking males experienced a decrease in EOD duration. These changes were paralleled by differences in circulating levels of plasma 11-ketotestosterone (11-KT), but not testosterone, suggesting that the changes in EOD duration may have been mediated by changes in plasma 11-KT levels. Thus, it appears that EOD duration is an accurate indicator of male status, which is under social and hormonal control.     

Orientation in the dark: brain circuits involved in the perception of electric signals in mormyrid electric fish.

Weakly electric fish produce electric signals with a specialised organ in their tail. In addition, they are electrosensitive and can perceive their self-generated signals (for electrolocation) and electric signals of other electric fishes (for electrocommunication). Mormyrids possess three types of peripheral electroreceptor organs, one used for electrocommunication and two types involved in electolocation. They are innervated by afferent fibres, which project to different zones in the electrosensory lateral line lobe (ELL) in the medulla. Brain circuits for electrolocation and electrocommunication are separated almost throughout the whole brain. Electrolocation pathways run from the ELL-cortex to the torus semicircularis of the midbrain and then via the valvula cerebelli towards the telencephalon. Pathways involved in electrocommunication run from the nucleus of the ELL to another part of the torus and from there through the isthmic granule nucleus to the valvula. In addition, a pathway via the preglomerular complex to the telencephalon might exist. In both the electrolocation and the electrocommunication circuits, prominent recurrent pathways are present.     

Electric signaling behavior and the mechanisms of electric organ discharge production in mormyrid fish.

Mormyrid fish communicate and navigate using electric organ discharges (EODs). The EOD is highly stereotyped and provides information on sender identity, including species, sex, reproductive condition, and possibly relative status and individual identity. By contrast, the sequence of pulse intervals (SPI) is variable and plays more of a role in signaling behavioral states. Various types of SPI displays may be produced, including tonic patterns such as 'random' and 'regularized', and phasic patterns such as 'bursts' and cessations'. Certain displays have been linked to specific behaviors such as aggression, submission, courtship and active exploration. In addition, interacting pairs of fish may produce stereotyped displays involving the relative timing of their EODs. The EOD waveform is controlled by the morphological and physiological properties of cells in the electric organ termed electrocytes. Differences in the innervation, morphology, size and membrane characteristics of electrocytes have been directly linked to species and sex differences in the EOD. The generation of each EOD is initiated in the medullary command nucleus (CN), which thereby determines the timing of EOD output. CN does not have any properties of a pacemaker, but rather appears to integrate descending inputs that affect the probability of EOD production. The precommand nucleus (PCN) provides a major source of excitatory input to CN and is itself inhibited by corollary discharge feedback following the production of each EOD. Changes in the activity of PCN and its inhibitory feedback neurons modify EOD output, and therefore drive the generation of SPI patterns. Current studies are addressing the mechanisms underlying the generation of these patterns and preliminary results suggest that different types of signals may be controlled by distinct components of the electromotor system. This is similar to findings in other electrogenic teleosts, suggesting that it may be a general feature in the motor control of signaling behavior.     

Ontogenetic development of electric-organ discharges in a mormyrid fish, the bulldog Marcusenius macrolepidotus (South African form)

The emergence and development of the electric-organ discharge (EOD) in larvae and juvenile bulldog Marcusenius macrolepidotus was investigated. Larvae hatched 4–5 days after spawning, and the first EODs were recorded on days 9 and 10 at a standard length ( L _S) of c. 6·5 mm. The larval EOD waveform was virtually monopolar, with a strong head-positive phase followed by a weak head-negative phase of long duration. A small separate potential preceded the EOD by c. 1·6 ms (believed to represent postsynaptic potential from electrocyte stalks). In contrast to previous reports on Pollimyrus adspersus with its distinct larval and adult EODs, in M. macrolepidotus there was a gradual transformation of the larval into the adult EOD waveform. The transformation started at an L _S of c. 17 mm (at an age of c. 40 days), first indications being a decrease in duration of the head-negative phase, and an increase of its peak amplitude relative to that of the head-positive phase. Still later, the weak postpotential of the adult EOD emerged on the rising edge of the head-negative phase. The transformation was nearly completed at an L _S of c. 30 mm (at an age of c. 60 days). Evolutionary and behavioural consequences of this alternative path of EOD ontogeny are discussed.     

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     

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.     

Melanocortins regulate the electric waveforms of gymnotiform electric fish

The hypothalamic-pituitary-adrenal/interrenal axis couples serotonergic activity in the brain to the peripheral regulators of energy balance and response to stress. The regulation of peripheral systems occurs largely through the release of peptide hormones, especially the melanocortins (adrenocorticotropic hormone [ACTH] and alpha melanocyte stimulating hormone [α-MSH]), and beta-endorphin. Once in circulation, these peptides regulate a wide range of processes; α-MSH in particular regulates behaviors and physiologies with sexual and social functions. We investigated the role of the HPI and melanocortin peptides in regulation of electric social signals in the gymnotiform electric fish, Brachyhypopomus pinnicaudatus. We found that corticotropin releasing factor, thyrotropin-releasing hormone, and α-MSH, three peptide hormones of the HPI/HPA, increased electric signal waveform amplitude and duration when injected into free-swimming fish. A fourth peptide, a synthetic cyclic-α-MSH analog attenuated the normal circadian and socially-induced EOD enhancements in vivo. When applied to the electrogenic cells (electrocytes) in vitro, only α-MSH increased the amplitude and duration of the electrocyte discharge similar to the waveform enhancements seen in vivo. The cyclic-α-MSH analog had no effect on its own, but blocked or attenuated α-MSH-induced enhancements in the single-cell discharge parameters, demonstrating that this compound functions as a silent antagonist at the electrocyte. Overall, these results strongly suggest that the HPI regulates the EOD communication signal, and demonstrate that circulating melanocortin peptides enhance the electrocyte discharge waveform.     

The otic gasbladder as an ancillary auditory structure in a mormyrid fish

Mormyrid fishes use acoustic signals for long-distance communication and a weakly electric field for short-distance interaction. Mormyrids are unique in having an otic gasbladder attached directly to the saccule on each side of the inner ear. Karl von Frisch (1938) hypothesized that the tightly coupled otic gasbladder might aid mormyrid hearing. Using the mormyrid fish (Brienomyrus brachyistius), this study manipulated gas in the otic gasbladder to test this hypothesis and histological sections were made to examine the anatomical relationship between the gasbladder and inner ear. The hearing sensitivity curves (audiograms) were obtained with the auditory brainstem response protocol. Audiograms were obtained from normal fish and from fish in which gas was withdrawn from either one or two otic gasbladders. Removal of gas from one otic gasbladder did not result in a significant change in either hearing ability or acoustically evoked brainwaves as compared to the control fish. Bilateral deflation of the otic gasbladders led to significant threshold changes. Histological sections revealed a particularly close coupling between the otic gasbladder and the saccule chamber. These results support von Frisch's hypothesis that the otic gasbladders of mormyrids assist in underwater sound detection. Accepted: 14 April 2000     

The code for stimulus direction in a cell assembly in the cockroach

Summary The cockroachPeriplaneta americana responds to the approach of a predator by turning away. A gentle wind gust, caused by the predator's approach, excites cereal wind receptors, which encode both the presence and the direction of the stimulus. These cells in turn excite a group of giant interneurons (GI's) whose axons convey the directional information to thoracic motor centers. A given wind direction is coded not by a single GI functioning as a labeled line, but rather by some relationship among the spike trains in an assembly of GI's. This paper analyzes the code in this assembly.It is shown that all three pairs of GI's with the largest axonal diameters respond differentially to wind from left front vs. right front (Figs. 3, 4; Table 2). Each GI encodes these angles by both the time of its first action potential, and the number of action potentials, relative to its contralateral homolog. It is shown that the behavioral discrimination cannot rely solely upon the leftright differences in the time of the first action potential.A model of the assembly code is developed that involves a comparison of the numbers of action potentials in the left vs. the right group of giant interneurons. The model is shown to account for a large number of pre-existing experimental data on direction discrimination. The model requires, however, the involvement of additional cells in the left and right groups, besides the specific GI's whose role had been tested in prior experiments. The model is then tested by further experiments designed to verify the involvement of these added cells. These experiments support the model.Abbreviations A abdominal ganglion - GI giant interneuron