Electric organ corollary discharge pathways in mormyrid fish

Corollary discharge signals associated with the motor command that elicits the electric organ discharge are prominent in the electrosensory lobe of mormyrid fish (Gnathonemus petersii). Central pathways and structures that convey these signals from the motor command nucleus to the electrosensory lobe are known anatomically, but these structures and their contributions to the various corollary discharge phenomena have not been examined physiologically. This study examines one such structure, the mesencephalic command associated nucleus (MCA).Recordings from MCA cells show a highly stereotyped two spike response. The first spike of the response has a latency of about 2.5 ms following the initiation of the electric organ discharge (EOD) motor command which is about 5.5 ms before the occurrence of the EOD.Results from stimulation and lesion experiments indicate that MCA is responsible for: 1) the gate-like corollary discharge-driven inhibition of the knollenorgan pathway; 2) the gate-like corollary discharge-driven excitation of granule cells in the mormyromast regions of the electrosensory lobe; and 3) various excitatory effects on other cells in the mormyromast regions.Some corollary discharge phenomena are still present after MCA lesions, including the earliest corollary discharge effects and the plasticity that follows pairing with electrosensory stimuli. These phenomena must be mediated by structures other than MCA.Abbreviations BCA bulbar command associated nucleus - C EOD motor command - C3 central cerebellar lobule 3 - COM EOD motor command nucleus - DLZ dorsolateral zone of ELL cortex - EGa eminentia granularis anterior - EGp eminentia granularis posterior - ELa nucleus exterolateralis anterior - ELL electrosensory lobe - ELLml molecular layer of ELL cortex - EOD electric organ discharge - gang ganglion layer - gran granule layer - jlem juxtalemniscal region - JLl lateral juxtalobar nucleus - JLm medial juxtalobar nucleus - lat nucleus lateralis - ll lateral lemniscus - MCA mesencephalic command associated nucleus - mol molecular layer - MOml molecular layer of the medial octavolateral nucleus - MRN medullary relay nucleus - MZ medial zone of ELL cortex - nALL anterior lateral line nerve - NELL nucleus of the electrosensory lobe - nX cranial nerve X (vagus) - OT optic tectum - PCA paratrigeminal command associated nucleus - pee praeeminentialis electrosensory tract - plex plexiform layer - prae nucleus praeeminentialis - sublem sublemniscal nucleus - TEL telencephalon - VLZ ventrolateral zone of ELL cortex - vped valvular peduncle     

Electric organ discharge patterns during group hunting by a mormyrid fish

Weakly electric fish emit and receive low-voltage electric organ discharges (EODs) for electrolocation and communication. Since the discovery of the electric sense, their behaviours in the wild have remained elusive owing to their nocturnal habits and the inaccessible environments in which they live. The transparency of Lake Malawi provided the first opportunity to simultaneously observe freely behaving mormyrid fish and record their EODs. We observed a piscivorous mormyrid, Mormyrops anguilloides, hunting in small groups in Lake Malawi while feeding on rock-frequenting cichlids of the largest known vertebrate species flock. Video recordings yielded the novel and unexpected finding that these groups resembled hunting packs by being largely composed of the same individuals across days. We show that EOD accelerations accompany prey probing and size estimation by M. anguilloides. In addition, group members occasionally synchronize bursts of EODs with an extraordinary degree of precision afforded by the mormyrid echo response. The characteristics and context of burst synchronization suggest that it may function as a pack cohesion signal. Our observations highlight the potential richness of social behaviours in a basal vertebrate lineage, and provide a framework for future investigations of the neural mechanisms, behavioural rules and ecological significance of social predation in M. anguilloides.     

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.     

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     

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     

Ontogeny of the electric organ discharge and the electric organ in the weakly electric pulse fish Brachyhypopomus pinnicaudatus (Hypopomidae, Gymnotiformes)

I recorded the electric organ discharges (EODs) of 331 immature Brachyhypopomus pinnicaudatus 6–88 mm long. Larvae produced head-positive pulses 1.3 ms long at 7 mm (6 days) and added a second, small head-negative phase at 12 mm. Both phases shortened duration and increased amplitude during growth. Relative to the whole EOD, the negative phase increased duration until 22 mm and amplitude until 37 mm. Fish above 37 mm produced a “symmetric” EOD like that of adult females. I stained cleared fish with Sudan black, or fluorescently labeled serial sections with anti-desmin (electric organ) or anti-myosin (muscle). From day 6 onward, a single electric organ was found at the ventral margin of the hypaxial muscle. Electrocytes were initially cylindrical, overlapping, and stalk-less, but later shortened along the rostrocaudal axis, separated into rows, and formed caudal stalks. This differentiation started in the posterior electric organ in 12-mm fish and was complete in the anterior region of fish with “symmetric” EODs. The lack of a distinct “larval” electric organ in this pulse-type species weakens the hypothesis that all gymnotiforms develop both a temporary (larval) and a permanent (adult) electric organ. Accepted: 1 March 1997     

Androgens alter electric organ discharge pulse duration despite stability in electric organ discharge frequency.

Weakly electric fish in the genus Sternopygus emit a sinusoidal, individually distinct, and sexually dimorphic electric organ discharge (EOD) that is used in electrolocation and communication. Systemically applied androgens decrease EOD frequency, which is set by a medullary pacemaker nucleus, and increase pulse duration, which is determined by the cells of the electric organ (the electrocytes), in a coordinated fashion. One possibility is that androgens broaden the EOD pulse duration by acting on the pacemaker neurons, thereby effecting a change in pacemaker firing frequency, and that the change in EOD pulse duration is due to an activity-dependent process. To determine whether androgens can alter pulse duration despite a stable pacemaker nucleus firing frequency, we implanted small doses of dihydrotestosterone in the electric organ. We found that androgen implants increased EOD pulse duration, but did not influence EOD frequency. In addition, using immunocytochemistry, we found that electrocytes label positively with an androgen receptor antibody. While it is not known on which cells androgens act directly, together these experiments suggest that they likely act on the electrocytes to increase EOD pulse duration. Since pulse duration is determined by electrocyte action potential duration and ionic current kinetics, androgens may therefore play a causative role in influencing individual variation and sexual dimorphism in electrocyte electrical excitability, an important component of electrocommunicatory behavior.     

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     

Plasticity of the electric organ discharge waveform of the electric fish Brachyhypopomus pinnicaudatus I. Quantification of day-night changes

The electric organ discharge of the gymnotiform fish Brachyhypopomus pinnicaudatus is a biphasic waveform. The female's electric organ discharge is nearly symmetric but males produce a longer second phase than first phase. In this study, infrared-sensitive video cameras monitored the position of unrestrained fish, facilitating precise measurement of electric organ discharge duration and amplitude every 2 h for 24 h. Males (n=27) increased electric organ discharge duration by 37 ± 12% and amplitude by 24 ± 9% at night and decreased it during the day. In contrast, females (n=8) exhibited only minor electric organ discharge variation over time. Most of a male's increase occurred rapidly within the first 2–3 h of darkness. Electric organ discharge values gradually diminished during the second half of the dark period and into the next morning. Modulation of the second phase of the biphasic electric organ discharge produced most of the duration change in males, but both phases changed amplitude by similar amounts. Turning the lights off at mid-day triggered an immediate increase in electric organ discharge, suggesting modification of existing ion channels in the electric organ, rather than altered genomic expression. Exaggeration of electric organ discharge sex differences implies a social function. Daily reduction of duration and amplitude may reduce predation risk or energy expenditure. Accepted: 12 September 1998     

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.     

Sex recognition and neuronal coding of electric organ discharge waveform in the pulse-type weakly electric fish, Hypopomus occidentalis

1. Hypopomus occidentalis, a weakly electric gymnotiform fish with a pulse-type discharge, has a sexually dimorphic electric organ discharge (Hagedorn 1983). The electric organ discharges (EODs) of males in the breeding season are longer in duration and have a lower peak-power frequency than the EODs of females. We tested reproductively mature fish in the field by presenting electronically generated stimuli in which the only cue for sex recognition was the waveshape of individual EOD-like pulses in a train. We found that gravid females could readily discriminate male-like from female-like EOD waveshapes, and we conclude that this feature of the electric signal is sufficient for sex recognition. 2. To understand the possible neural bases for discrimination of male and female EODs by H . occidentalis, we conducted a neurophysiological examination of both peripheral and central neurons. Our studies show that there are sets of neurons in this species which can discriminate male or female EODs by coding either temporal or spectral features of the EOD. 3. Temporal encoding of stimulus duration was observed in evoked field potential recordings from the magnocellular nucleus of the midbrain torus semicircularis. This nucleus indirectly receives pulse marker electroreceptor information. The field potentials suggest that comparison is possible between pulse marker activity on opposite sides of the body. 4. From standard frequency-threshold curves, spectral encoding of stimulus peak-power frequency was measured in burst duration coder electroreceptor afferents. In both male and female fish, the best frequencies of the narrow-band population of electroreceptors were lower than the peak-power frequency of the EOD. Based on this observation, and the presence of a population of wide-band receptors which can serve as a frequency-independent amplitude reference, a slope-detection model of frequency discrimination is advanced. 5. Spectral discrimination of EOD peak-power frequency was also shown to be possible in a more natural situation similar to that present during behavioral discrimination. As the fish's EOD mimic slowly scanned through and temporally coincided with the neighbor's EOD mimic, peak spike rate in burst duration coder afferents was measured. Spike rate at the moment of coincidence changed predictably as a function of the neighbor's EOD peak-power frequency. 6. Single-unit threshold measurements were made on afferents from peripheral burst duration coder receptors in the amplitude-coding pathway, and midbrain giant cells in the time-coding pathway.(ABSTRACT TRUNCATED AT 400 WORDS)     

Electric organ discharge frequency and plasma sex steroid levels during gonadal recrudescence in a natural population of the weakly electric fish Sternopygus macrurus

1. Sternopygus macrurus were collected in Venezuela during the period of gonadal recrudescence in early or late dry season. Electric organ discharge (EOD) frequencies were recorded, blood samples were taken for analysis of steroid titers, and gonads were taken for determination of reproductive condition. 2. Mean EOD frequencies were significantly lower in males than in females in all samples. EOD frequency was inversely correlated with body length in males in late, but not early, dry season, and these parameters were never correlated in females. 3. Plasma levels of testosterone (T) and 11-ketotestosterone (11-KT), but not estradiol-17 beta (E2), were inversely correlated with EOD frequency in males. No 11-KT was observed in plasma of females, and plasma levels of T and E2 in females were comparable to those of males. Neither T nor E2 were correlated with EOD frequency in females. 4. Testes collected in late dry season were more mature than those from early dry season; androgen levels and EOD frequency were correlated with testicular maturity. Ovaries collected in early dry season were immature, while those from late dry season were more mature. There was no relationship between EOD frequency and stage of ovarian development. 5. These results suggest that plasma androgens modulate EOD frequency in males during the reproductive season and that plasma E2 has little relationship to EOD frequency in either sex.     

A temporal analysis of testosterone-induced changes in electric organs and electric organ discharges of mormyrid fishes

The electric organ discharge (EOD) of several species of mormyrid fishes within the genus Brienomyrus is sexually dimorphic during the breeding season: the duration of the male's EOD is much longer than the duration of the female's (for a review see Hopkins, 1986). The mormyrid used here, Brienomyrus sp., exhibits similar alterations in the duration of the triphasic EOD after treatment with testosterone, as do other members of this genus (for reviews see Bass, 1986a,b). In this experiment, animals were intraperitoneally implanted with pellets of either 11-ketotestosterone or 17 a-methyltestosterone, and the time course of the changes in the duration of each of the three phases of the EOD were quantified. Additionally, the time course of changes in the morphology of the electric organ, after testosterone treatment, was also quantified using electron microscopic techniques. The results suggest that the change in the duration of the first phase of the EOD is due exclusively to the change in the thickness of the electrocyte body: this is consistent with a model proposed by Bennett and Grundfest (1961) for the electrogenesis of a triphasic EOD. Changes in the duration of the second and third phases of the EOD are highly correlated with the changes in the surface area of the posterior and anterior faces of the electrocyte, respectively. The results support the hypothesis that gonadal steroid hormone-induced changes in the EOD are due to structural changes in the electrocyte's membranes, and that all of the observed changes in the discharge of this system can be explained by the action of steroid hormones on the peripheral target cells (electrocytes).     

Spontaneous modulations of the electric organ discharge in the weakly electric fish, Apteronotus leptorhynchus: a biophysical and behavioral analysis

Brown ghosts, Apteronotus leptorhynchus, are weakly electric gymnotiform fish whose wave-like electric organ discharges are distinguished by their enormous degree of regularity. Despite this constancy, two major types of transient electric organ discharge modulations occur: gradual frequency rises, which are characterized by a relatively fast increase in electric organ discharge frequency and a slow return to baseline frequency; and chirps, brief and complex frequency and amplitude modulations. Although in spontaneously generated gradual frequency rises both duration and amount of the frequency increase are highly variable, no distinct subtypes appear to exist. This contrasts with spontaneously generated chirps which could be divided into four "natural" subtypes based on duration, amount of frequency increase and amplitude reduction, and time-course of the frequency change. Under non-evoked conditions, gradual frequency rises and chirps occur rather rarely. External stimulation with an electrical sine wave mimicking the electric field of a neighboring fish leads to a dramatic increase in the rate of chirping not only during the 30 s of stimulation, but also in the period immediately following the stimulation. The rate of occurrence of gradual frequency rises is, however, unaffected by such a stimulation regime.