Sensory cues for the gradual frequency fall responses of the gymnotiform electric fish, Rhamphichthys rostratus

The sensory cues for a less known form of frequency shifting behavior, gradual frequency falls, of electric organ discharges (EODs) in a pulse-type gymnotiform electric fish, Rhamphichthys rostratus, were identified. We found that the gradual frequency fall occurs independently of more commonly observed momentary phase shifting behavior, and is due to perturbation of sensory feedback of the fish's own EODs by EODs of neighboring fish. The following components were identified as essential features in the signal mixture of the fish's own and the neighbor's EOD pulses: (1) the neighbor's pulses must be placed within a few millisecond of the fish's own pulses, (2) the neighbor's pulses, presented singly at low frequencies (0.2–4 Hz), were sufficient, (3) the frequency of individual pulse presentation must be below 4 Hz, (4) amplitude modulation of the sensory feedback of the fish's own pulses induced by such insertions of the neighbor's pulses must contain a high frequency component: sinusoidal amplitude modulation of the fish's own EOD feedback at these low frequencies does not induce gradual frequency falls. Differential stimulation across body surfaces, which is required for the jamming avoidance response (JAR) of wave-type gymnotiform electric fish, was not necessary for this behavior. We propose a cascade of high-pass and low-pass frequency filters within the amplitude processing pathway in the central nervous system as the mechanism of the gradual frequency fall response.Abbreviations EOD electric organ discharge - f frequency of EOD or pacemaker command signal - JAR jamming avoidance response - S ₁ stimulus mimicking fish's own EOD - f ₁ frequency of S₁ - S ₂ stimulus mimicking neighbor's EOD - f ₂ frequency of S₂     

A neural mechanism of hyperaccurate detection of phase advance and delay in the jamming avoidance response of weakly electric fish

 The weakly electric fish Eigenmannia can detect the phase difference between a jamming signal and its own signal down to 1 s. To clarify the neuronal mechanism of this hyperaccurate detection of phase difference, we present a neural network model of the torus of the midbrain which plays an essential role in the detection of phase advances and delays. The small-cell model functions as a coincidence detector and can discriminate a time difference of more than 100 s. The torus model consists of laminae 6 and 8. The model of lamina 6 is made with multiple encoding units, each of which consists of a single linear array of small cells and a single giant cell. The encoding unit encodes the phase difference into its spatio-temporal firing pattern. The spatially random distribution of small cells in each encoding unit improves the encoding ability of phase modulation. The neurons in lamina 8 can discriminate the phase advance and delay of jamming electric organ discharges (EODs) compared with the phase of the fish's own EOD by integrating simultaneously the outputs from multiple encoding units in lamina 6. The discrimination accuracy of the feature-detection neurons is of the order of 1 s. The neuronal mechanism generating this hyperacuity arises from the spatial feature of the system that the innervation sites of small cells in different encoding units are distributed randomly and differently on the dendrites of single feature-detection neurons. The mechanism is similar to that of noise-enhanced information transmission. Received: 10 July 2000 / Accepted in revised form: 19 January 2001     

Androgen modulates the kinetics of the delayed rectifying K+ current in the electric organ of a weakly electric fish

Weakly electric fish such as Sternopygus macrurus utilize a unique signal production system, the electric organ (EO), to navigate within their environment and to communicate with conspecifics. The electric organ discharge (EOD) generated by the Sternopygus electric organ is quasi-sinusoidal and sexually dimorphic; sexually mature males produce long duration EOD pulses at low frequencies, whereas mature females produce short duration EOD pulses at high frequencies. EOD frequency is set by a medullary pacemaker nucleus, while EOD pulse duration is determined by the kinetics of Na+ and K+ currents in the electric organ. The inactivation of the Na+ current and the activation of the delayed rectifying K+ current of the electric organ covary with EOD frequency such that the kinetics of both currents are faster in fish with high (female) EOD frequency than those with low (male) EOD frequencies. Dihydrotestosterone (DHT) implants masculinize the EOD centrally by decreasing frequency at the pacemaker nucleus (PMN). DHT also acts at the electric organ, broadening the EO pulse, which is at least partly due to a slowing of the inactivation kinetics of the Na+ current. Here, we show that chronic DHT treatment also slows the activation and deactivation kinetics of the electric organ's delayed rectifying K+ current. Thus, androgens coregulate the time-varying kinetics of two distinct ion currents in the EO to shape a sexually dimorphic communication signal.     

‘Communication’ in weakly electric fish, Gnathonemus petersii (Mormyridae) II. Interaction of electric organ discharge activities of two fish

The electric organ discharges (EODs) of pairs of weakly electric fish, Gnathonemus petersii, were simultaneously recorded to study the significance of the EODs as communication signals. In a 400-litre tank a larger fish (12 to 15 cm) was passively moved within a shelter tube toward a smaller specimen (6 to 9 cm), either in steps or a continuous move. The movement was stopped at that distance when at least one fish significantly lowered or ceased its EOD activity. From this ‘threshold interfish distance’ the spatial range of a ‘communication field’ was found to extend about 30 cm from the fish. At threshold distances an EOD frequency increase caused a temporary EOD activity cessation in the second fish. The spontaneous irregular EOD pattern of the fish displaying the increased EOD rate changed into a regular one with almost equal time intervals between fish pulses.     

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)     

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.     

EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips.

Weakly electric "wave" fish make highly regular electric organ discharges (EODs) for precise electrolocation. Yet, they modulate the ongoing rhythmicity of their EOD during social interactions. These modulations may last from a few milliseconds to tens of minutes. In this paper we describe the different types of EOD modulations, what they may signal to recipient fish, and how they are generated on a neural level. Our main conclusions, based on a species called the brown ghost (Apteronotus leptorhynchus) are that fish: (1) show sexual dimorphism in the signals that they generate; (2) make different signals depending on Whether they are interacting with a fish of the opposite sex or, within their own sex, to a fish of that which is dominant or subordinate to it; (3) are able to assess relative dominance from electrical cues; (4) have a type of plasticity in the pacemaker nucleus, the control center for the EOD, that occurs after stimulation of NMDA receptors that causes a long-lasting (tens of minutes to hours) change in EOD frequency; (5) that this NMDA receptor-dependent change may occur in reflexive responses, like the jamming avoidance response (JAR), as well as after certain long-lasting social signals. We propose that NMDA-receptor dependent increases in EOD frequency during the JAR adaptively shift the EOD frequency to a new value to avoid jamming by another fish and that such increases in EOD frequency during social encounters may be advantageous since social dominance seems to be positively correlated with EOD frequency in both sexes.     

Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish,Apteronotus, during modulatory behaviors

1. The weakly electric gymnotiform fish, Apteronotus leptorhynchus, can be induced to perform a variety of modulations of its quasi-sinusoidal, electric organ discharge (EOD) in acute physiological preparations. These modulations, many of which are communicatory in function, include the jamming avoidance response (JAR). We have recorded intracellularly from neurons of the medullary pacemaker nucleus which is responsible for maintaining the ongoing EOD frequency during these modulatory behaviors. 2. We have used dye-filled microelectrodes to characterize single cell morphology of the two types of cells in the pacemaker nucleus (relay and pacemaker cells) and to localize anatomically the site of the differing responses we see during frequency modulations. We have also recorded with KCl-filled electrodes and attributed these data to cell type and location on the basis of characteristic behavior during these modulations. 3. Much of our data deals with chirps, brief accelerations of the EOD frequency lasting 10 to 14 ms. We see distinct patterns of activity in the pacemaker nucleus corresponding to different anatomical locations: the relay cell soma and axon, and the pacemaker cell soma and axon. Most of these loci show a marked rise in baseline voltage during the acceleration in spike frequency. The most unusual of these is the pacemaker cell axon which displays an often extreme decline in spike amplitude concurrent with the chirp (Fig. 7A). 4. 'Yodeling' (Dye 1987) appears to involve similar, characteristic changes in the pattern of firing as those seen during chirping. Similar quantitative analyses suggest that the JAR involves a different mechanism, however.     

A role of synchronicity of neural activity based on dynamic plasticity of synapses in encoding spatiotemporal features of electrosensory stimuli

It is quite important for investigation of sensory mechanism to understand how dynamical property of neurons is used for encoding the feature of spatiotemporally varying stimuli. To consider concretely the problem, we focus our study on electrosensory system of a weakly electric fish. Weakly electric fish generate electric field around their body using electric organ discharge (EOD) and accurately detect the location of an object through the modulation of electric field induced by the object. We made a neural network model of electrosensory lateral-line lobe (ELL). Here we show that the features of EOD modulation depending specifically distance and size of an object are encoded into the timing of burst firing of ELL neurons. These features can be represented by the spatial area of synchronous burst firing and the interburst interval in the ELL network. We show that short-term changes of excitatory and inhibitory synapses, induced by efferent signals, regulate the ELL activity so as to effectively encode the features of EOD modulation.     

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.     

Pharmacological characterization of ionic currents that regulate high‐frequency spontaneous activity of electromotor neurons in the weakly electric fish,Apteronotus leptorhynchus

The neural circuit that controls the electric organ discharge (EOD) of the brown ghost knifefish (Apteronotus leptorhynchus) contains two spontaneous oscillators. Both pacemaker neurons in the medulla and electromotor neurons (EMNs) in the spinal cord fire spontaneously at frequencies of 500–1000 Hz to control the EOD. These neurons continue to fire in vitro at frequencies that are highly correlated with in vivo EOD frequency. Previous studies used channel blocking drugs to pharmacologically characterize ionic currents that control high‐frequency firing in pacemaker neurons. The goal of the present study was to use similar techniques to investigate ionic currents in EMNs, the other type of spontaneously active neuron in the electromotor circuit. As in pacemaker neurons, high‐frequency firing of EMNs was regulated primarily by tetrodotoxin‐sensitive sodium currents and by potassium currents that were sensitive to 4‐aminopyridine and κA‐conotoxin SIVA, but resistant to tetraethylammonium. EMNs, however, differed from pacemaker neurons in their sensitivity to some channel blocking drugs. Alpha‐dendrotoxin, which blocks a subset of Kv1 potassium channels, increased firing rates in EMNs, but not pacemaker neurons; and the sodium channel blocker μO‐conotoxin MrVIA, which reduced firing rates of pacemaker neurons, had no effect on EMNs. These results suggest that similar, but not identical, ionic currents regulate high‐frequency firing in EMNs and pacemaker neurons. The differences in the ionic currents expressed in pacemaker neurons and EMNs might be related to differences in the morphology, connectivity, or function of these two cell types. © 2005 Wiley Periodicals, Inc. J Neurobiol, 2006     

Pharmacological characterization of ionic currents that regulate high-frequency spontaneous activity of electromotor neurons in the weakly electric fish, Apteronotus leptorhynchus

The neural circuit that controls the electric organ discharge (EOD) of the brown ghost knifefish (Apteronotus leptorhynchus) contains two spontaneous oscillators. Both pacemaker neurons in the medulla and electromotor neurons (EMNs) in the spinal cord fire spontaneously at frequencies of 500-1,000 Hz to control the EOD. These neurons continue to fire in vitro at frequencies that are highly correlated with in vivo EOD frequency. Previous studies used channel blocking drugs to pharmacologically characterize ionic currents that control high-frequency firing in pacemaker neurons. The goal of the present study was to use similar techniques to investigate ionic currents in EMNs, the other type of spontaneously active neuron in the electromotor circuit. As in pacemaker neurons, high-frequency firing of EMNs was regulated primarily by tetrodotoxin-sensitive sodium currents and by potassium currents that were sensitive to 4-aminopyridine and kappaA-conotoxin SIVA, but resistant to tetraethylammonium. EMNs, however, differed from pacemaker neurons in their sensitivity to some channel blocking drugs. Alpha-dendrotoxin, which blocks a subset of Kv1 potassium channels, increased firing rates in EMNs, but not pacemaker neurons; and the sodium channel blocker muO-conotoxin MrVIA, which reduced firing rates of pacemaker neurons, had no effect on EMNs. These results suggest that similar, but not identical, ionic currents regulate high-frequency firing in EMNs and pacemaker neurons. The differences in the ionic currents expressed in pacemaker neurons and EMNs might be related to differences in the morphology, connectivity, or function of these two cell types.     

Cav1.2 calcium channels modulate the spiking pattern of hippocampal pyramidal cells

Ca(v)1.2 L-type calcium channels support hippocampal synaptic plasticity, likely by facilitating dendritic Ca2+ influx evoked by action potentials (AP) back-propagated from the soma. Ca2+ influx into hippocampal neurons during somatic APs is sufficient to activate signalling pathways associated with late phase LTP. Thus, mechanisms controlling AP firing of hippocampal neurons are of major functional relevance. We examined the excitability of CA1 pyramidal cells using somatic current-clamp recordings in brain slices from control type mice and mice with the Ca(v)1.2 gene inactivated in principal hippocampal neurons. Lack of the Ca(v)1.2 protein did not affect either affect basic characteristics, such as resting membrane potential and input resistance, or parameters of single action potentials (AP) induced by 5 ms depolarising current pulses. However, CA1 hippocampal neurons from control and mutant mice differed in their patterns of AP firing during 500 ms depolarising current pulses: threshold voltage for repetitive firing was shifted significantly by about 5 mV to more depolarised potentials in the mutant mice (p<0.01), and the latency until firing of the first AP was prolonged (73.2+/-6.6 ms versus 48.1+/- 7.8 ms in control; p<0.05). CA1 pyramidal cells from the mutant mice also showed a lowered initial spiking frequency within an AP train. In control cells, isradipine had matching effects, while BayK 8644 facilitated spiking. Our data demonstrate that Ca(v)1.2 channels are involved in regulating the intrinsic excitability of CA1 pyramidal neurons. This cellular mechanism may contribute to the known function of Ca(v)1.2 channels in supporting synaptic plasticity and memory.     

Evidence for a direct effect of androgens upon electroreceptor tuning

Tuberous electroreceptors of individual wave type weakly electric fish are tuned to the fundamental frequency of that fish's electric organ discharge (EOD). EOD frequency and receptor best frequency (BF) are both lowered following systemic injection of 5-alpha-dihydrotestosterone (DHT). A previous study (Meyer et al. 1984) showed that the effect of DHT on the EOD generating circuitry was independent of an ongoing EOD and suggested that its effect on electroreceptor tuning was indirect, possibly mediated by the electric field. We have continued these studies to determine the factors which influence electroreceptor tuning. Baseline recordings of EOD frequency, receptor oscillations, and single afferent tuning curves were taken. After fish were electrically silenced by spinal cord transection they were injected daily with either DHT or saline or were implanted with either DHT-filled or empty silastic capsules. As previously reported, the EOD frequency (determined from pacemaker nucleus recordings) was lowered in DHT-treated, transected fish and increased in control fish. Similarly, receptor tuning was lowered in the DHT-treated, silenced fish. Oscillation frequencies decreased in both treated and control groups, but significantly more in the hormone group. Single afferent best frequencies were lowered in both DHT groups and raised in their respective control groups. In another series of experiments exogenous electric fields capable of driving receptors in a 1-to-1 phase-locked manner were placed around silenced fish. We were unable to elicit any shift in pacemaker frequency or electroreceptor tuning regardless of stimulus field geometry. Four transected fish were injected with DHT and placed in exogenous electric fields of higher frequency than their original EOD. Even in the presence of a higher frequency electric field, DHT lowered EOD frequency and afferent BF. We conclude that androgens produce effects both on the EOD generating circuitry, probably at the level of the pacemaker nucleus, and on electroreceptors, probably, ultimately, on receptor cell membrane conductances. These effects occur in parallel allowing the two parameters to remain well matched. In contrast to former predictions, exogenous electric fields alone appear unable to shift receptor tuning.     

An in vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish, Apteronotus

1. An in vitro preparation of the medullary pacemaker nucleus of the weakly electric fish Apteronotus leptorhynchus was studied which fires regularly and synchronously at the fish's characteristic frequency of electric organ discharge (EOD). Upon bipolar stimulation of tissue regions through which pass prepacemaker nucleus afferents to the pacemaker, a brief, transient increase in discharge frequency ensued at short-latency (Fig. 1A). 2. Intracellular recordings revealed that the acceleration was accompanied by a depolarization and decline in action potential amplitude. The magnitude of these changes was both phase- (Fig. 5) and amplitude-dependent, with the latter showing an evident threshold effect (Figs. 4 and 12). The response was reversibly blocked by high Mg2+ saline (Fig. 1B), and the magnitude of the accelerations showed marked facilitation during repeated stimulation (Fig. 6). 3. Optical and histological identification allowed characteristically different responses in the intracellular recordings to be attributed to the two cell types of the pacemaker nucleus: pacemaker and relay cells (Figs. 2 and 3). Similar responses have been observed at these respective recording locations in the intact animal during chirping (Dye and Heiligenberg 1987). 4. Simultaneous recordings of pairs of cells revealed a transient change in the phase relationship of firing during the accelerations which was most marked between relay and pacemaker cells (Fig. 7). These dual recordings also revealed that the relay cells depolarize and accelerate more than pacemaker cells (Fig. 10), suggesting that they are the principal effectors of this behavioral modulation. 5. Trains of pulses additionally elicited a long-lasting frequency elevation which occurred at a slightly higher threshold than the brief accelerations. This slow frequency change relaxed back to baseline following a biexponential time course which closely resembled that of a distinct behavior seen in intact fish, termed 'yodeling' (Dye 1987).     

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     

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.     

Individual variation and hormonal modulation of a sodium channel beta subunit in the electric organ correlate with variation in a social signal

The sodium channel beta1 subunit affects sodium channel gating and surface density, but little is known about the factors that regulate beta1 expression or its participation in the fine control of cellular excitability. In this study we examined whether graded expression of the beta1 subunit contributes to the gradient in sodium current inactivation, which is tightly controlled and directly related to a social behavior, the electric organ discharge (EOD), in a weakly electric fish Sternopygus macrurus. We found the mRNA and protein levels of beta1 in the electric organ both correlate with EOD frequency. We identified a novel mRNA splice form of this gene and found the splicing preference for this novel splice form also correlates with EOD frequency. Androgen implants lowered EOD frequency and decreased the beta1 mRNA level but did not affect splicing. Coexpression of each splice form in Xenopus oocytes with either the human muscle sodium channel gene, hNav1.4, or a Sternopygus ortholog, smNav1.4b, sped the rate of inactivation of the sodium current and shifted the steady-state inactivation toward less negative membrane potentials. The translational product of the novel mRNA splice form lacks a previously identified important tyrosine residue but still functions normally. The properties of the fish alpha and coexpressed beta1 subunits in the oocyte replicate those of the electric organ's endogenous sodium current. These data highlight the role of ion channel beta subunits in regulating cellular excitability.     

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.