Electrocommunication signals in female brown ghost electric knifefish, Apteronotus leptorhynchus

Female communication behaviors are often overlooked by researchers in favor of male behaviors, which are usually more overt and easier to elicit. Very little is known about female electrocommunication behaviors in brown ghost knifefish, a weakly electric wavetype Gymnotiform fish. Most behavioral studies have focused on males, and fish are usually restrained and played a stimulus near their own electric organ discharge frequency to evoke chirps (abrupt short-term frequency rises) or the jamming avoidance response. Our study focuses on categorizing and describing spontaneous and evoked electric organ discharge modulations in free-swimming female fish that were either electrically coupled to tanks containing a conspecific (male or female), or left isolated. Cluster analysis of signals produced under isolated and social conditions revealed three categories of rises: short rise, medium rise and long rise; and one category of frequency decrease (dip). Females produce significantly more short rises when electrically coupled to tanks containing lower-frequency females, and produce more long rises when electrically coupled to tanks containing males. Short rises may have an intrasexual aggressive function, while long rises may serve as an advertisement of status or reproductive condition in intersexual interactions.     

Electric organ morphology of Sternopygus macrurus, a wave-type, weakly electric fish with a sexually dimorphic EOD.

In several species of electric fish with a sex difference in their pulse-type electric organ discharge (EOD), the action potential-generating cells of the electric organ (electrocytes) of males are larger and more invaginated compared to females. Androgen treatment of females and juveniles produces a longer-duration EOD pulse that mimics the mature male EOD, with a concurrent increase in electrocyte size and/or membrane infolding. In Sternopygus macrurus, which generates a wave-type EOD, androgen also increases EOD pulse duration. To investigate possible morphological correlates of hormone-dependent changes in EOD in Sternopygus, we examined electric organs from both fish collected in the field, and untreated and androgen-treated specimens in the laboratory. The electrocytes are cigar shaped, with prominent papillae on the posterior, innervated end. Electrocytes of field-caught specimens were significantly larger in all parameters than were electrocytes of specimens maintained in the laboratory. EOD pulse duration and frequency were highly correlated, and were significantly different between the sexes in sexually mature fish. Nevertheless, no sex difference in electrocyte morphology was observed, nor did any parameters of electrocyte morphology correlate with EOD pulse duration or frequency. Further, whereas androgen treatment significantly lowered EOD frequency and broadened EOD pulse duration, there was no difference in electrocyte morphology between hormone-treated and control groups. Thus, in contrast to results from studies on both mormyrid and gymnotiform pulse fish, electrocyte morphology is not correlated with EOD waveform characteristics in the gymnotiform wave-type fish Sternopygus. The data, therefore, suggest that sex differences in EOD are dependent on changes in active electrical properties of electrocyte membranes.     

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.     

Electric organ morphology of Sternopygus macrurus,a wave-type,weakly electric fish with a sexually dimorphic EOD

In several species of electric fish with a sex difference in their pulse-type electric organ discharge (EOD), the action potential-generating cells of the electric organ (electrocytes) of males are larger and more invaginated compared to females. Androgen treatment of females and juveniles produces a longer-duration EOD pulse that mimics the mature male EOD, with a concurrent increase in electrocyte size and/or membrane infolding. In Sternopygus macrurus, which generates a wave-type EOD, androgen also increases EOD pulse duration. To investigate possible morphological correlates of hormone-dependent changes in EOD in Sternopygus, we examined electric organs from both fish collected in the field, and untreated and androgen-treated specimens in the laboratory. The electrocytes are cigar shaped, with prominent papillae on the posterior, innervated end. Electrocytes of field-caught specimens were significantly larger in all parameters than were electrocytes of specimens maintained in the laboratory. EOD pulse duration and frequency were highly correlated, and were significantly different between the sexes in sexually mature fish. Nevertheless, no sex difference in electrocyte morphology was observed, nor did any parameters of electrocyte morphology correlate with EOD pulse duration or frequency. Further, whereas androgen treatment significantly lowered EOD frequency and broadened EOD pulse duration, there was no difference in electrocyte morphology between hormone-treated and control groups. Thus, in contrast to results from studies on both mormyrid and gymnotiform pulse fish, electrocyte morphology is not correlated with EOD waveform characteristics in the gymnotiform wave-type fish Sternopygus. The data, therefore, suggest that sex differences in EOD are dependent on changes in active electrical properties of electrocyte membranes. © 1992 John Wiley & Sons, Inc.     

Dynamics and stimulus-dependence of pacemaker control during behavioral modulations in the weakly electric fish,Apteronotus

1. Weakly electric fish generate around their bodies low-amplitude, AC electric fields which are used both for the detection of objects and intraspecific communication. The types of modulation in this signal of which the high-frequency wave-type gymnotiform, Apteronotus, is capable are relatively few and stereotyped. Chief among these is the chirp, a signal used in courtship and agonistic displays. Chirps are brief and rapid accelerations in the normally highly regular electric organ discharge (EOD) frequency. 2. Chirping can be elicited artificially in these animals by the use of a stimulus regime identical to that typically used to elicit another behavior, the jamming avoidance response (JAR). The neuronal basis for the JAR, a much slower and lesser alteration in EOD frequency, is well understood. Examination of the stimulus features which induce chirping show that, like the JAR, there is a region of frequency differences between the fish's EOD and the interfering signal that maximally elicits the response. Moreover, the response is sex-specific with regard to the sign of the frequency difference, with females chirping preferentially on the positive and most males on the negative Df. These features imply that the sensory mechanisms involved in the triggering of these communicatory behaviors are fundamentally similar to those explicated for the JAR. 3. Additionally, two other modulatory behaviors of unknown significance are described. The first is a non-selective rise in EOD frequency associated with a JAR stimulus, occurring regardless of the sign of the Df. This modulation shares many characteristics with the JAR. The second behavior, which we have termed a 'yodel', is distinct from and kinetically intermediate to chirping and the JAR. Moreover, unlike the other studied electromotor behaviors it is generally produced only after the termination of the eliciting stimulus.     

Cellular characterization of synaptic modulations of a neuronal oscillator in electric fish

The two closely related gymnotiform electric fish, Eigenmannia and Apteronotus, modulate the rate of their electric organ discharges during orientation and communication behaviors in similar ways. These modulations are controlled through three prepacemaker nuclei that provide excitatory inputs to the medullary pacemaker nucleus. Whereas the projections from the prepacemaker nuclei onto the two identified cell types of the pacemaker nucleus appear to be very similar, species-specific differences in the synaptic effects of these connections exist. We examined the modulatory premotor inputs on relay and pacemaker cells in Eigenmannia and Apteronotus by performing intracellular in␣vivo recordings while pharmacologically stimulating the three prepacemaker nuclei. In both taxa, activation of the lateral portion of the diencephalic prepacemaker causes a depolarization of baseline and a lowering of peak voltage primarily in relay cells. Activation of the medial portion of the diencephalic prepacemaker depolarizes mainly pacemaker cells in both fish, yet also has different effects on peak voltage in each species. Excitation of the sublemniscal prepacemaker in Apteronotus results in a depolarization of relay cells, whereas its inhibition in Eigenmannia causes a lowering of peak voltage without affecting baseline voltage. Our results complement earlier pharmacological investigations by expanding them to the cellular level. They provide neurophysiological evidence for different receptor subtypes on relay and pacemaker cells mediating different behaviors. Accepted: 14 May 1997     

From oscillators to modulators: behavioral and neural control of modulations of the electric organ discharge in the gymnotiform fish, Apteronotus leptorhynchus.

The brown ghost (Apteronotus leptorhynchus) is a weakly electric gymnotiform fish that produces wave-like electric organ discharges distinguished by their enormous degree of regularity. Transient modulations of these discharges occur both spontaneously and when stimulating the fish with external electric signals that mimic encounters with a neighboring fish. Two prominent forms of modulations are chirps and gradual frequency rises. Chirps are complex frequency and amplitude modulations lasting between 20 ms and more than 200 ms. Based on their biophysical characteristics, they can be divided into four distinct categories. Gradual frequency rises consist of a rise in discharge frequency, followed by a slow return to baseline frequency. Although the modulatory phase may vary considerably between a few 100 ms and almost 100 s, there is no evidence for the existence of distinct categories of this type of modulation signal. Stimulation of the fish with external electric signals results almost exclusively in the generation of type-2 chirps. This effect is independent of the chirp type generated by the respective individual under non-evoked conditions. By contrast, no proper stimulation condition is known to evoke the other three types of chirps or gradual frequency rises in non-breeding fish. In contrast to the type-2 chirps evoked when subjecting the fish to external electric stimulation, the rate of spontaneously produced chirps is quite low. However, their rate appears to be optimized according to the probability of encountering a conspecific. As a result, the rate of non-evoked chirping is increased during the night when the fish exhibit high locomotor activity and in the time period following external electric stimulation. These, as well as other, observations demonstrate that both the type and rate of modulatory behavior are affected by a variety of behavioral conditions. This diversity at the behavioral level correlates with, and is likely to be causally linked to, the diversity of inputs received by the neurons that control chirps and gradual frequency rises, respectively. These neurons form two distinct sub-nuclei within the central posterior/prepacemaker nucleus in the dorsal thalamus. In vitro tract-tracing experiments have elucidated some of the connections of this complex with other brain regions. Direct input is received from the optic tectum. Indirect input arising from telencephalic and hypothalamic regions, as well as from the preoptic area, is relayed to the central posterior/prepacemaker nucleus via the preglomerular nucleus. Feedback loops may be provided by projections of the central posterior/prepacemaker nucleus to the preglomerular nucleus and the nucleus preopticus periventricularis.     

Environmental and hormonal influences upon EOD waveform in gymnotiform pulse fish.

Temperature is a major variable that affects all biological systems. Environmental temperature determines animal geographical distribution and activity, and influences their reproductive cycle, particularly within the temperate zone. Temperature, as a physical parameter, also strongly affects excitable tissues. The hypothesis of temperature as the most important environmental cue for the onset of breeding in gymnotiform pulse fish of the temperate zone is supported by: (a) a clear temporal correlation that was observed in the wild between water temperature and sexual maturity, and (b) the induction of gonadal maturation and sexual differences after acclimation at high temperature (28 degrees C) in the laboratory. Temperature sensitivity of EOD waveform (described in Brachyhypopomus pinnicaudatus and Gymnotus carapo) is characterized by the decrease of the EOD's late head-negative phase as temperature increases. This phenomenon depends on electrocyte properties since: (a) experimentally induced changes of discharge rate at constant temperature generate smaller EOD distortion, and (b) the effect of temperature upon EOD also depends on water conductivity. Temperature sensitivity of EOD waveform is negatively correlated with gonadal maturity in Brachyhypopomus pinnicaudatus. High temperature sensitivity was observed during the non-breeding season, whereas low temperature sensitivity was recorded during the breeding season. Temperature sensitivity of EOD waveform in both Brachyhypopomus pinnicaudatus and Gymnotus carapo was modulated by: (a) testosterone treatment (100 microg/g) that decreased temperature sensitivity, and (b) acclimation at high temperature (28 degrees C, 1 month) that also decreased temperature sensitivity. Temperature is probably acting through the neuroendocrine system, and ultimately interacting with steroid hormones in their effects upon EOD waveform.     

The control of pacemaker modulations for social communication in the weakly electric fish Sternopygus

Summary Nearly sinusoidal electric organ discharges (EODs) of the weakly electric fish Sternopygus, occur at a regular rate within a range from 50 to 200 Hz and are commanded by a medullary pacemaker nucleus (Pn). During courtship and aggression, the rate of EODs is modulated as smooth EOD-frequency rises or brief EOD-interruptions (Hopkins 1974b). The present study examines the control of such modulations. Rises were elicited by L-glutamate stimulation of the diencephalic prepacemaker nucleus, the only previously known source of input to the Pn. We demonstrate an additional input to the Pn, the sublemniscal prepacemaker nucleus (SPPn). L-glutamate stimulation of this area caused EOD-interruptions.The Pn contains electrotonically coupled pacemaker cells which generate the rhythm of the EODs, as well as relay cells which transmit the command pulse to the spinal motor neurons that innervate the electric organ. Pacemaker cells recorded intracellularly during EOD-interruptions continued firing at their regular frequency but with slightly increased jitter. Relay cells, on the other hand, were strongly depolarized and fired spikelets at a greatly increased frequency during EOD-interruptions. Thus EOD-interruptions were caused by SPPn input to relay cells that caused their massive depolarization, blocking the normal input from pacemaker cells without greatly affecting pacemaker cell firing characteristics.Application to the Pn of an antagonist to NMDA-type glutamate receptors blocked EOD-frequency rises and EOD-interruptions. Antagonists to quisqualate/ kainate receptor-types were ineffective.Abbreviations EOD Electric Organ Discharge - JAR Jamming Avoidance Response - Pn pacemaker nucleus - PPn diencephalic prepacemaker nucleus - SPPn sublemniscal prepacemaker nucleus     

Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish

The first stage of information processing in the electrosensory system involves the encoding of local changes in transdermal potential into trains of action potentials in primary electrosensory afferent nerve fibers. To develop a quantitative model of this encoding process for P-type (probability-coding) afferent fibers in the weakly electric fish Apteronotus leptorhynchus, we recorded single unit activity from electrosensory afferent axons in the posterior branch of the anterior lateral line nerve and analyzed responses to electronically generated sinusoidal amplitude modulations of the local transdermal potential. Over a range of AM frequencies from 0.1 to 200 Hz, the modulation transfer function of P-type afferents is high-pass in character, with a gain that increases monotonically up to AM frequencies of 100 Hz where it begins to roll off, and a phase advance with a range of 15–60 degrees. Based on quantitative analysis of the observed gain and phase characteristics, we present a computationally efficient model of P-type afferent response dynamics which accurately characterizes changes in afferent firing rate in response to amplitude modulations of the fish's own electric organ discharge over a wide range of AM frequencies relevant to active electrolocation. Accepted: 14 June 1997     

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

Serotonin (5-HT) is an indirect modulator of the electric organ discharge (EOD) in the weakly electric gymnotiform fish, Brachyhypopomus pinnicaudatus. Injections of 5-HT enhance EOD waveform "masculinity", increasing both waveform amplitude and the duration of the second phase. This study investigated the pharmacological identity of 5-HT receptors that regulate the electric waveform and their effects on EOD amplitude and duration. We present evidence that two sets of serotonin receptors modulate the EOD in opposite directions. We found that the 5HT1AR agonist 8-OH-DPAT diminishes EOD duration and amplitude while the 5HT1AR antagonist WAY100635 increases these parameters. In contrast, the 5HT2R agonist alpha-Me-5-HT increases EOD amplitude but not duration, yet 5-HT-induced increases in EOD duration can be inhibited by blocking 5HT2A/2C-like receptors with ketanserin. These results show that 5-HT exerts bi-directional control of EOD modulations in B. pinnicaudatus via action at receptors similar to mammalian 5HT1A and 5HT2 receptors. The discordant amplitude and duration response suggests separate mechanisms for modulating these waveform parameters.     

Model of P- and T-electroreceptors of weakly electric fish.

To clarify the microscopic mechanisms by which P- and T-receptors encode amplitude modulation and zero crossing time of jamming signals, we present a model of P- and T-receptors based on their physiological and anatomical properties. The model consists of a receptor cell, supporting cells, and an afferent nerve fiber. The basal membrane of the receptor cell includes voltage-sensitive Ca2+ channels, Ca(2+)-activated K+ channels, and leak channels of Na+, K+, and Cl-. The driving force of potential change under stimulation is generated by the voltage-sensitive Ca2+ channels, and the suppressing force of the change is generated by Ca(2+)-activated K+ channels. It has been shown that in T-receptor cells the driving force is much stronger than the suppressing force, whereas in P-receptor cells the driving force is comparable with the suppressing force. The difference in various kinds of response properties between P- and T-receptors have been consistently explained based on the difference in the relative strengths of the driving and suppressing forces between P- and T-receptor cells. The response properties considered are encoding function, probability of firing of afferent nerve, pattern of damped oscillation, shape of tuning curves, values of the optimum frequency, and response latency.     

Transient electric birefringence studies of T2 bacteriophage and T2 ghost

The transient electric birefringence behavior of bacteriophage T2 and the T2 ghost or protein coal was studied. The field free relaxation measurements show both the intact virus and its ghost to have two rotary diffusion coefficients. These coefficients have values of 555 ± 54 and 111 ± 22 sec.^?1 for the intact virus and 688 ± 89 and 161 ± 29 sec.^?l for the ghost. The equivalent ellipsoids for the fast and slow relaxation coefficients were obtained by use of Perrin's equation and were related to the bacteriophage structure in terms of a possible extension of the tail fibers or an enlargement of the head structure. The saturation of the specific birefringence of the phage and the ghost when compared with the specific birefringence of the free nucleic acid gave an average optical orientation of 10 to 18% of the nucleic acid parallel to the main axis of the phage. The analysis of the birefringence versus applied field strength in the Kerr region gave the following values for the anisotropy of the polarixability. α_e,33 – α_e,11 and intrinsic dipole, μ, of both phage and ghost : for T2 phage α_e,33 – α_e,11 = 5.0 × 10^?14 cm.³ and μ = 64,400 Debyes; for T2 ghost α_e,33 – α_e,11 = 7.9 × 10^?14cm.³ and μ = 57,200 Debyes. The high intrinsic dipole for phage and ghost is interpreted as to be associated with the mechanisms of the virus for attachment, to the host cell wall.     

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.     

Multimodal sensory integration in weakly electric fish: a behavioral account.

The ability to integrate multisensory information is a fundamental characteristic of the brain serving to enhance the detection and identification of external stimuli. Weakly electric fish employ multiple senses in their interactions with one another and with their inanimate environment (electric, visual, acoustic, mechanical, chemical, thermal, and hydrostatic pressure) and also generate signals using some of the same stimulus energies (electric, acoustic, visual, mechanical). A brief overview provides background on the sensory and motor channels available to the fish followed by an examination of how weakly electric fish 'benefit' from integrating various stimulus modalities that assist in prey detection, schooling, foraging, courtship, and object location. Depending on environmental conditions, multiple sensory inputs can act synergistically and improve the task at hand, can be redundant or contradictory, and can substitute for one another. Over time, in repeated encounters with familiar surrounds, loss of one modality can be compensated for through learning. Studies of neuronal substrates and an understanding of the computational algorithms that underlie multisensory integration ought to expose the physiological corollaries to widely published concepts such as internal representation, sensory expectation, sensory generalization, and sensory transfer.     

The electric image in weakly electric fish: I. A data-based model of waveform generation inGymnotus carapo

Understanding how electrosensory images are generated and perceived in actively electrolocating fish requires the study of the characteristics of fish bodies as electric sources. This paper presents a model ofGymnotus carapo based on measurements of the electromotive force generated by the electric organ and the impedance of the passive tissues. A good agreement between simulated and experimentally recorded transcutaneous currents was obtained. Passive structures participate in the transformation of the electromotive force pattern into transcutaneous current profiles. These spatial filtering properties of the fish's body were investigated using the model. The shape of the transcutaneous current profiles depends on tissue resistance and on the geometry and size of the fish. Skin impedance was mainly resistive. The effect of skin resistance on the spatial filtering properties of the fish's body was theoretically analyzed.The model results show that generators in the abdominal and central regions produce most of the currents through the head. This suggests that the electric organ discharge (EOD), generated in the abdominal and central regions is critical for active electrolocation. In addition, the well-synchronized EOD components generated all along the fish produce large potentials in the far field. These components are probably involved in long-distance electrocommunication.Preliminary results of this work were published as a symposium abstract.