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PubMed1996

Tuberous electroreceptor organs form in denervated regenerating skin of a weakly electric fish.

Weakly electric fish use tuberous electroreceptor organs to detect their own electric fields. We investigated the role of innervation upon regeneration and differentiation of tuberous electroreceptor organs. The left, infraorbital, anterior lateral line nerve of brown ghosts (Apteronotus leptorhynchus) was sectioned, and the proximal stump was dipped in ricin to prevent regrowth. Immediately after denervation, a piece of cheek skin (approximately 0.5 cm2) was removed bilaterally to induce skin regeneration. After survival periods of 3, 4, or 5 weeks, regenerated skin from the left (denervated) and the right (reinnervated) sides was removed and processed for immunocytochemistry or electron microscopy. Tuberous electroreceptor organs were present in regenerated reinnervated, as well as regenerated denervated skin patches at all survival times. With increased time after skin removal, the number of fully differentiated organs increased in the reinnervated regenerated skin while the number of organs with degenerating receptor cells or entirely devoid of receptor cells increased in the denervated regenerated skin. These results suggest that innervation is not essential for tuberous electroreceptor organ development, but that it is necessary for complete sensory cell differentiation and long-term survival.

Animals↗
PubMed1999

Central mechanisms of temporal analysis in the knollenorgan pathway of mormyrid electric fish

Mormyrid electric fish communicate using pulse-type electric organ discharges (EODs). The fine temporal structure of the waveforms of EODs varies widely throughout the 200 or more species of mormyrids. These signals carry information about the species, the sex and even the individual identity of the signaller. Behavioral experiments have shown that some species of fish are capable of using this information. Of the four known types of electroreceptors in mormyrid fish, the knollenorgan electroreceptor is the one most likely to be involved in the detection of conspecific EOD signals. Here, we review some recent advances in understanding how the central knollenorgan pathway might be analyzing the temporal structure of the EOD waveform. Fine temporal analysis appears to take place in the nucleus exterolateralis pars anterior (ELa), where tightly phase-locked inputs from the hindbrain drive a direct, excitatory input through a long axonal delay line and also drive an indirect, inhibitory input with negligible delay through the ELa large cell. These two inputs converge on ELa small cells, where they are hypothesized to interact in a 'delay-line/blanking' model. This initial temporal analysis is further refined in the nucleus exterolateralis pars posterior, where units tuned to ranges of pulse durations have been identified physiologically.

Journal Article↗
PubMed1981

Temporal coding of species recognition signals in an electric fish.

An electric fish in the African family Mormyridae recognizes members of its own species by "listening" to electric organ discharges, which are species-specific signatures. Reactions of fish in the field and of individual electroreceptors to both normal and modified computer-synthesized discharges emphasize the importance of the waveform (time-domain cues) in species recognition.

Animal Communication↗
PubMed2006

Analysis of behavior-related excitatory inputs to a central pacemaker nucleus in a weakly electric fish.

Gymnotid electric fish explore their environment and communicate with conspecifics by means of rhythmic electric organ discharges. The neural command for each electric organ discharge arises from activity of a medullary pacemaker nucleus composed of two neuronal types: pacemaker and relay cells. During different behaviors as in courtship, exploration and agonistic interactions, these species display specific electric organ discharge frequency and/or waveform modulations. The neural bases of these modulations have been explained in terms of segregation of inputs to pacemaker or relay cells, as well as differential activation of the glutamate receptors of these cells. One of the most conspicuous electric organ discharge frequency modulations in Gymnotus carapo results from the activation of Mauthner cells, a pair of reticulospinal neurons that are involved in the organization of sensory-evoked escape responses in teleost fish. The activation of Mauthner cells in these animals produces a prolonged increase in electric organ discharge rate, whose neural mechanisms involves the activation of both N-methyl-D-aspartate (NMDA) and metabotropic glutamatergic receptors of pacemaker cells. Here we provide evidence which indicates that pacemaker cells are the only cellular target of the synaptic inputs responsible for the Mauthner cell initiated electric organ discharge modulation at the medullary pacemaker nucleus. Additionally, although pacemaker cells express both NMDA and non-NMDA ionotropic receptors, we found that non-NMDA receptors are not involved in this synaptic action which suggests that NMDA and non-NMDA receptor subtypes are not co-localized at the subsynaptic membrane. NMDA receptor activation of pacemaker cells seems to be an efficient neural strategy to produce long-lasting enhancements of the fish sampling capability during Mauthner cell-initiated motor behaviors.

Action Potentials↗
PubMed1991

Regeneration of electroreceptors in weakly electric fish.

Weakly electric teleost fish possess two classes of electroreceptors: tuberous and ampullary organs. Ampullary organs are used for detecting prey, while tuberous organs detect the fish's own electric organ discharges (EODs) and those of conspecifics. EOD frequency varies among individuals within a species and a fish's tuberous receptors are sharply tuned to its own EOD frequency. In young, small fish both tuberous and ampullary afferents innervate only single organs. As fish grow new receptor cells are added to each organ and it divides into two daughter organs. This process continues resulting in numerous organs in a cluster; the afferent nerve innervates all the organs in a cluster. When a patch of skin is removed new skin grows back complete with new receptor organs of both classes. From our studies we have shown that: (1) new organs are found only in the presence of nerve fibres; (2) their morphological development during regeneration is similar to their normal development; (3) organs divide rapidly giving rise to daughter organs until each afferent fibre innervates the correct number of organs for a fish of its size; (4) receptor cells are broadly tuned below the EOD frequency of a given fish and they gradually increase their tuned frequency and sharpness of tuning until they become correctly tuned to that EOD frequency; (5) the correct matching of receptor tuning to EOD frequency occurs in fish in which the spinal cord has been severed or with lesions of the medullary pacemaker nucleus, thereby eliminating the EOD and any possible 'calibration' signal; and (6) basal and capsule cells of receptor organs in the intact skin around the wound divide after skin damage and are a possible source of precursor cells for new receptor organs.

Animals↗
PubMed1992

An internal current source yields immunity of electrosensory information processing to unusually strong jamming in electric fish.

The electric organ of a fish represents an internal current source, and the largely isopotential nature of the body interior warrants that the current associated with the fish's electric organ discharges (EODs) recruits all electroreceptors on the fish's body surface evenly. Currents associated with the EODs of a neighbor, however, will not penetrate all portions of the fish's body surface equally and will barely affect regions where the neighbor's current flows tangentially to the skin surface. The computational mechanisms of the jamming avoidance response (JAR) in Eigenmannia exploit the uneven effects of a neighbor's EOD current to calculate the correct frequency difference between the two interfering EOD signals even if the amplitude of a neighbor's signal surpasses that of the fish's own signal by orders of magnitude. The particular geometry of the fish's own EOD current thus yields some immunity against the potentially confusing effects of unusually strong interfering EOD currents of neighbors.

Animals↗
PubMed1998

Diversity of sexual dimorphism in electrocommunication signals and its androgen regulation in a genus of electric fish, Apteronotus.

Gymnotiform electric fish emit an electric organ discharge that, in several species, is sexually dimorphic and functions in gender recognition. In addition, some species produce frequency modulations of the electric organ discharge, known as chirps, that are displayed during aggression and courtship. We report that two congeneric species (Apteronotus leptorhynchus and A. albifrons) differ in the expression of sexual dimorphism in these signals. In A. leptorhynchus, males chirp more than females, but in A. albifrons chirping is monomorphic. The gonadosomatic index and plasma levels of 11-ketotestosterone were equivalent in both species, suggesting that they were in similar reproductive condition. Corresponding to this difference in dimorphism, A. leptorhynchus increases chirping in response to androgens, but chirping in A. albifrons is insensitive to implants of testosterone, dihydrotestosterone or 11-ketotestosterone. Species also differ in the sexual dimorphism and androgen sensitivity of electric organ discharge frequency. In A. leptorhynchus, male discharge at higher frequencies than females, and androgens increase electric organ discharge frequency. In A. albifrons, males discharge at lower frequencies than females, and androgens decrease electronic organ discharge frequency. Thus, in both chirping and electric organ discharge frequency, evolutionary changes in the presence or direction of sexual dimorphism have been accompanied and perhaps caused by changes in the androgen regulation of the electric organ discharge.

Androgens↗
PubMed2000

Parvocells: a novel interneuron type in the pacemaker nucleus of a weakly electric fish.

Gymnotiform weakly electric fish produce electric organ discharges (EODs) that function in electrolocation and communication. The command signal for the EOD is produced by the medullary pacemaker nucleus, which contains two well-characterized neuron types: pacemaker cells and relay cells. In this study, we characterized a third neuron type in the pacemaker nucleus. These neurons, which we have named parvocells, were smaller (7-15 microm in diameter) than relay and pacemaker cells. The parvocells were labeled with an antibody against the neuronal calcium-binding protein, parvalbumin, and were not labeled with several glial-specific antibodies. Parvocells had one to three fine processes that often terminated at the periphery of relay and pacemaker cell bodies. The parvalbumin-positive terminals of the parvocells colocalized with immunoreactivity for SV-2, suggesting that the parvocells form chemical synapses on the relay and pacemaker cells. Parvalbumin-positive neurons are frequently gamma-aminobutyric acid (GABA)ergic or glycinergic, and the cytoplasm of the parvocell somata was immunoreactive with a glycine antibody. Antibodies against glycine receptors and gephyrin, however, did not label any cells in the pacemaker nucleus, suggesting that the pacemaker nucleus does not contain glycine or GABA((A)) receptors. Electron microscopy revealed gap junctions between the membranes of parvocells and adjacent terminal-like structures. Furthermore, neurobiotin injected into individual pacemaker or relay cells labeled parvocells as well as other pacemaker and relay cells, demonstrating that the parvocells are dye-coupled to the other neuron types in the pacemaker nucleus. These findings indicate that the parvocells are histochemically distinct from relay and pacemaker cells and that they receive electrotonic inputs from and make chemical synapses back onto pacemaker and relay cells. Further study is needed to investigate the function of these neurons in regulating the EOD.

Animals↗
PubMed2006

Regulation and modulation of electric waveforms in gymnotiform electric fish.

Weakly electric gymnotiform fish specialize in the regulation and modulation of the action potentials that make up their multi-purpose electric signals. To produce communication signals, gymnotiform fish modulate the waveforms of their electric organ discharges (EODs) over timescales spanning ten orders of magnitude within the animal's life cycle: developmental, reproductive, circadian, and behavioral. Rapid changes lasting milliseconds to seconds are the result of direct neural control of action potential firing in the electric organ. Intermediate-term changes taking minutes to hours result from the action of melanocortin peptides, the pituitary hormones that induce skin darkening and cortisol release in many vertebrates. Long-term changes in the EOD waveform taking days to weeks result from the action of sex steroids on the electrocytes in the electric organ as well as changes in the neural control structures in the brain. These long-term changes in the electric organ seem to be associated with changes in the expression of voltage-gated ion channels in two gene families. Electric organs express multiple voltage-gated sodium channel genes, at least one of which seems to be regulated by androgens. Electric organs also express multiple subunits of the shaker (Kv1) family of voltage-gated potassium channels. Expression of the Kv1 subtype has been found to vary with the duration of the waveform in the electric signal. Our increasing understanding of the mechanisms underlying precise control of electric communication signals may yield significant insights into the diversity of natural mechanisms available for modifying the performance of ion channels in excitable membranes. These mechanisms may lead to better understanding of normal function in a wide range of physiological systems and future application in treatment of disease states involving pathology of excitable membranes.

Action Potentials↗
PubMed1995

In vitro study of phase resetting and phase locking in a time-comparison circuit in the electric fish, Eigenmannia.

The electric fish Eigenmannia generates on oscillating weak electric field. The amplitude and timing information of this electric field is perceived by electroreceptors distributed on its skin. The pathway of timing information, consisting of spherical cells and giant cells, was studied in an in vitro preparation. The giant cells were identified to be endogenous oscillators and thus have the functional advantage of phase locking more easily to a periodic stimulus with a frequency in the range of the intrinsic frequency. Their spontaneous rhythmic activity was perturbed by delivering excitatory single pulses or periodic pulses via their synaptic inputs. The regular and irregular dynamics produced by periodic stimulation were discussed in the context of a mathematical analysis of the response to single pulses. Ambiguous representations of the timing of the stimulus pulse were observed and could be related to this analysis. Some spontaneously firing cells could be silenced with periodic excitatory stimulation in a narrow frequency and amplitude range. Some irregularly firing cells continued to fire periodically for several seconds after phase locking to a periodic stimulus. This study is the first description of an endogenous oscillator in a system devoted to the precise timing of sensory events.

Animals↗
PubMed1992

Development of the jamming avoidance response and its morphological correlates in the gymnotiform electric fish, Eigenmannia.

The electric fish, Eigenmannia, will smoothly shift the frequency of its electric organ discharge away from an interfering electric signal. This shift in frequency is called the jamming avoidance response (JAR). In this article, we analyze the behavioral development of the JAR and the anatomical development of structures critical for the performance of the JAR. The JAR first appears when juvenile Eigenmannia are approximately 1 month old, at a total length of 13-18 mm. We have found that the establishment of much of the sensory periphery and of central connections precedes the onset of the JAR. We describe three aspects of the behavioral development of the JAR: (a) the onset and development of the behavior is closely correlated with size, not age; (b) the magnitude (in Hz) of the JAR increases with size until the juveniles display values within the adult range (10-20 Hz) at a total length of 25-30 mm; and (3) the JAR does not require prior experience or exposure to electrical signals. Raised in total electrical isolation from the egg stage, animals tested at a total length of 25 mm performed a correct JAR when first exposed to the stimulus. We examine the development of anatomical areas important for the performance of the JAR: the peripheral electrosensory system (mechano- and electroreceptors and peripheral nerves); and central electrosensory pathways and nuclei [the electrosensory lateral line lobe (ELL), the lateral lemniscus, the torus semicircularis, and the pace-maker nucleus]. The first recognizable structures in the developing electrosensory system are the peripheral neurites of the anterior lateral line nerve. The afferent nerves are established by day 2, which is prior to the formation of receptors in the epidermis. Thus, the neurites wait for their targets. This sequence of events suggests that receptor formation may be induced by innervation of primordial cells within the epidermis. Mechanoreceptors are first formed between day 3 and 4, while electroreceptors are first formed on day 7. Electroreceptor multiplication is observed for the first time at an age of 25 days and correlates with the onset of the JAR. The somata of the anterior lateral line nerve ganglion project afferents out to peripheral electroreceptors and also send axons centrally into the ELL. The first electroreceptive axons invade the ELL by day 6, and presumably a rough somatotopic organization and segmentation within the ELL may arise as early as day 7. Axonal projections from the ELL to the torus develop after day 18.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1998

Phenotypic conversion of distinct muscle fiber populations to electrocytes in a weakly electric fish.

In most groups of electric fish, the electric organ (EO) derives from striated muscle cells that suppress many muscle phenotypic properties. This phenotypic conversion is recapitulated during regeneration of the tail in the weakly electric fish Sternopygus macrurus. Mature electrocytes, the cells of the electric organ, are considerably larger than the muscle fibers from which they derive, and it is not known whether this is a result of muscle fiber hypertrophy and/or fiber fusion. In this study, electron micrographs revealed fusion of differentiated muscle fibers during the formation of electrocytes. There was no evidence of hypertrophy of muscle fibers during their phenotypic conversion. Furthermore, although fish possess distinct muscle phenotypes, the extent to which each fiber population contributes to the formation of the EO has not been determined. By using myosin ATPase histochemistry and anti-myosin heavy chain (MHC) monoclonal antibodies (mAbs), different fiber types were identified in fascicles of muscle in the adult tail. Mature electrocytes were not stained by the ATPase reaction, nor were they labeled by any of the anti-MHC mAbs. In contrast, mature muscle fibers exhibited four staining patterns. The four fiber types were spatially arranged in distinct compartments with little intermixing; peripherally were two populations of type I fibers with small cross-sectional areas, whereas more centrally were two populations of type II fibers with larger cross-sectional areas. In 2- and 3-week regenerating blastema, three fiber types were clearly discerned. Most (> 95%) early-forming electrocytes had an MHC phenotype similar to that of type II fibers. In contrast, fusion among type I fibers was rare. Together, ultrastructural and immunohistochemical analyses revealed that the fusion of muscle fibers gives rise to electrocytes and that this fusion occurs primarily among the population of type II fibers in regenerating blastema.

Adenosine Triphosphatases↗
PubMed2006

Circadian rhythms in electric waveform structure and rate in the electric fish Brachyhypopomus pinnicaudatus.

Weakly electric fish have long been known to express day-night oscillations in their discharge rates, and in the amplitude and duration of individual electric organ discharges (EODs). Because these oscillations are altered by social environment and neuroendocrine interactions, electric fish are excellent organisms for exploring the social and neuroendocrine regulation of circadian rhythm expression. Previous studies asserting that these oscillations are circadian rhythms have been criticized for failing to control temperature and randomize feeding regimes, or for running the fish under constant conditions for just 2-3 days. Here we show that the day-night oscillations in the EODs of the neotropical gymnotiform fish Brachyhypopomus pinnicaudatus free-run for over a week under constant photic and thermal conditions, and randomized food provisioning. Sex differences were apparent in strength and magnitude of the circadian oscillations; male oscillations were stronger and larger. All three parameters retain a common oscillation period while differing in the persistence of oscillation strength and magnitude, a difference consistent with proposals by others that declines of behavioral circadian rhythms may result from breakdowns downstream of the central oscillator.

Analysis of Variance↗
PubMed1996

Comparative analysis of the jamming avoidance response in African and South American wave-type electric fishes.

African wave-type electric fish, Gymnarchus, and South American wave-type electric fish, Eigenmannia, have evolved electrosensory and electromotor systems independently. Nevertheless, they exhibit a similar electrical behavior, the jamming avoidance response (JAR). When two individuals with slightly different frequencies of electric organ discharge (EOD) meet, they shift discharge frequencies away from each other to avoid mutual jamming of their electrolocation systems. These two genera of electric fishes perform this behavior using an identical set of complex computational rules. Reflecting their independent evolution, however, neuronal implementation of the computational steps appears to take different forms. One of the essential computational steps, phase comparison, is performed in the hindbrain in Gymnarchus and in the midbrain in Eigenmannia. The comparison of these two species in this paper revealed an example of how different brain structures perform functionally similar tasks in independently evolved systems that have a similar overall behavioral function.

Action Potentials↗
PubMed1998

Effects of 17alpha-methyltestosterone on sexually dimorphic characters in the weakly discharging electric fish, Brienomyrus niger (Günther, 1866) (Mormyridae): electric organ discharge, ventral body wall indentation, and anal-Fin ray bone expansion.

Adult males of African weakly discharging electric fish (family: Mormyridae) are distinguished from juveniles and adult females by a dorsally directed indentation of the posterior ventral body wall and by massive bone expansion of the bases of a select number of anal-fin rays. These sexually dimorphic structures seem to facilitate the anal-fin reflex that is displayed during courtship when the male envelopes its anal fin around the female's to form a common spawning pouch. Expanded bone could provide additional surface for muscle attachment and thus assist in part with the courtship sequence. Based on the fact that the expression of the male sexually dimorphic electric organ discharge (EOD) is under androgen control, and that the female EOD can be masculinized through testosterone administration, we hypothesized that androgens should also drive anal-fin ray bone expansion in male mormyrids and equally effect male-like changes in treated juveniles and adult females. Exogenous androgen treatment (17alpha-methyltestosterone) of adult female Brienomyrus niger resulted in a male-like EOD, and male-typical structural transformations (body wall indentation and anal-fin ray bone expansion). Some of these changes were immediate and receded following hormone withdrawal (EOD), while others developed more slowly and were apparently permanent (indentation and bone formation). 17alpha-Methyltestosterone administration affected only those targets in females that are normally involved in the male's reproductive behavior, i.e., its courtship signal (EOD) and two morphological features (body-wall indentation and bone expansion). Rays of the dorsal or caudal fins were never affected.

Animals↗
PubMed2006

Interruption of pacemaker signals by a diencephalic nucleus in the African electric fish, Gymnarchus niloticus.

The African electric fish Gymnarchus niloticus rhythmically emits electric organ discharges (EODs) for communication and navigation. The EODs are generated by the electric organ in the tail in response to the command signals from the medullary pacemaker complex, which consists of a pacemaker nucleus (PN), two lateral relay nuclei (LRN) and a medial relay nucleus (MRN). The premotor structure and its modulatory influences on the pacemaker complex have been investigated in this paper. A bilateral prepacemaker nucleus (PPn) was found in the area of the dorsal posterior nucleus (DP) of the thalamus by retrograde labeling from the PN. No retrogradely labeled neurons outside the pacemaker complex were found after tracer injection into the LRN or MRN. Accordingly, anterogradely labeled terminal fibers from PPn neurons were found only in the PN. Iontophoresis of L-glutamate into the region of the PPn induced EOD interruptions. Despite the exclusive projection of the PPn neurons to the PN, extracellular and intracellular recordings showed that PN neurons continue their firing while MRN neurons ceased their firing during EOD interruption. This mode of EOD interruption differs from those found in any other weakly electric fishes in which EOD cessation mechanisms have been known.

Action Potentials↗
PubMed1998

Behavioral actions of androgens and androgen receptor expression in the electrocommunication system of an electric fish, Eigenmannia virescens.

Gymnotiform electric fish emit an electric organ discharge (EOD) that, in many species, is sexually dimorphic and used in gender recognition. The glass knife fish Eigenmannia has been a major neuroethological model system, and there have been reports that its EOD is sexually dimorphic. However, no study has examined the role of steroids in establishing this dimorphism. We tested the effect of three androgens, testosterone, dihydrotestosterone, and 11-ketotestosterone (11kT), on the EOD of Eigenmannia virescens. Implants of any of these three androgens induced a decrease in EOD frequency, consistent with several studies showing that males have a lower EOD frequency than females. In a separate experiment, we found that 11kT treatment also increases EOD pulse duration, but has no effect on the duty cycle, the relative duration of the positive and negative phases of the wave, or the harmonic content of the EOD. Using immunocytochemistry, we found that the cells of the electric organ (the electrocytes) that produce the EOD and control its pulse duration label positively with an antibody to the androgen receptor. These experiments indicate that androgens decrease the firing frequency of the medullary pacemaker and alter the ion current kinetics in the electrocytes. Moreover, the presence of nuclear androgen receptors in electrocytes suggests that androgens act directly on the electric organ to modify EOD pulse duration.

Androgens↗
PubMed1993

Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish, Gymnarchus niloticus.

An African electric fish, Gymnarchus, and a South American electric fish, Eigenmannia, are believed to have evolved their electrosensory systems independently. Both fishes, nevertheless, gradually shift the frequency of electric organ discharge away when they encounter a neighbor of a similar discharge frequency. Computational algorithms employed by Gymnarchus for this jamming avoidance response have been identified in this study for comparison with those of extensively studied Eigenmannia. 1. Gymnarchus determines whether it should raise or lower its discharge frequency based solely upon the signal mixture of its own reafferent and the exafferent signal from a neighbor, and does not internally refer to the pacemaker command signal which drives its own discharge. 2. The signal mixture is analyzed in terms of the time courses of amplitude modulation and phase modulation at each area of the body surface. 3. Phase of the signal mixture at each area is compared with that of another area for the detection of phase modulation. 4. Unambiguous information necessary for the jamming avoidance response is extracted by integrating information from all body areas each of which yields ambiguous information. 5. These computational features are identical to those of Eigenmannia, suggesting that the neural circuit for jamming avoidance responses may have evolved from preexisting mechanisms for electrolocation in both fishes.

Algorithms↗