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PubMed2000

Temperature dependence of electrocommunication signals and their underlying neural rhythms in the weakly electric fish, Apteronotus leptorhynchus.

Weakly electric fish emit an electric communication signal that is controlled by a highly specialized neural circuit. In Apteronotus, the continuous electric organ discharge (EOD) is generated by electrotonically coupled neurons in the hindbrain pacemaker nucleus, and transient EOD modulations involve chemical synapses from descending midbrain and thalamic prepacemaker nuclei. We characterized the effects of temperature change (18-32 degrees C) on both the continuous EOD and EOD modulations, chirps, in A. leptorhynchus. EOD frequency was linearly related to temperature (Q(10)=1.62). By contrast, the temperature dependence of EOD amplitude changed with temperature. Amplitude increased steeply with temperature below 25 degrees C (Q(10)=2.0), but increased only gradually above 25 degrees C (Q(10)=1.15). EOD waveform, and consequently harmonic content, was also affected by temperature. The amplitude of the second harmonic was relatively high at both low and high temperature and relatively low at intermediate temperatures. The amplitude of the third harmonic increased monotonically with temperature. Thus, temperature has qualitative as well as quantitative effects on the production of the EOD. Chirp rate (Q(1)0=3.2) had a higher temperature dependence than that of the continuous EOD, which likely reflects its reliance on chemical rather than electrotonic synapses. In vitro pacemaker firing frequency had a similar, but slightly higher Q(10) (1.82) than that of the EOD frequency.

Animal Communication↗
PubMed2001

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 micros. 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 micros. 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 micros. 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.

Animals↗
PubMed1987

Electric fish approach stationary signal sources by following electric current lines.

African electric fish of a pulse species, Brienomyrus brachyistius (Mormyridae), housed singly in a large, circular arena, were presented with electrical stimuli which mimicked a conspecific intruder. Stimuli were produced with either dipolar or bipolar electrodes in three different geometries. We tracked the unconditioned approach response paths taken by the fish and compared tracks for each of the geometries. The results suggest that B. brachyistius can determine neither the distance nor the direction of an electric dipole from afar, but that they do manage to find the source by maintaining a precise alignment of their body axis parallel to the direction of the local electric field vector (parallel to current lines) while swimming. This behaviour ultimately leads to the current source. We propose that this behaviour may be a simple mechanism mediating the approach response of one electric fish to another.

Animals↗
PubMed2004

L-citrulline immunoreactivity reveals nitric oxide production in the electromotor and electrosensory systems of the weakly electric fish, Apteronotus leptorhynchus.

Weakly electric fish produce electric organ discharges (EODs) used for electrolocation and communication. In the brown ghost knifefish, Apteronotus leptorhynchus, several neuron types in brain regions that control the EOD or process electrosensory information express nitric oxide synthase (NOS). The present study used immunoreactivity for L-citrulline, a byproduct of the production of nitric oxide (NO) by NOS, to assess NO production in NOS-expressing neurons. A polyclonal antibody against L-citrulline produced specific labeling in most neuronal populations previously identified to express NOS. Specifically, several cell types that precisely encode temporal information and/or fire at high frequencies, including spherical cells in the electrosensory lateral line lobe, giant cells in layer VI of the dorsal torus semicircularis, and pacemaker and relay cells in the pacemaker nucleus, were strongly immunoreactive for L-citrulline. This suggests that these neurons produced high levels of NO. Notably, electromotor neurons, which also strongly express NOS, were not immunoreactive for L-citrulline, suggesting that NOS did not produce high levels of NO in these neurons. No apparent differences in L-citrulline distribution or intensity were observed between socially isolated fish and fish exposed to playback stimuli simulating the presence of a conspecific. This suggests that social stimulation by electrocommunication signals is not necessary for high levels of NO production in many NOS-positive neurons. Future studies focusing on regulation of NO production in these systems, and the effects of NO on electrosensory processing and electromotor pattern generation will help elucidate the function of NO signaling pathways in this system.

Animals↗
PubMed2003

Cyclic AMP modulates electrical signaling in a weakly electric fish.

Many species of electric fish show diurnal or socially elicited variation in electric organ discharge amplitude. In Sternopygus macrurus, activation of protein kinase A by 8-bromo-cAMP increases electrocyte sodium current magnitude. To determine whether the behavioral plasticity in electric organ discharge amplitude is controlled by electrocyte biophysical properties, we examined whether the effects of phosphorylation on ion currents in the electric organ translate directly into electric organ discharge changes. We injected the electric organ of restrained fish with 8-bromo-cAMP and monitored the electric organ discharge. The effect of protein kinase A activation on electrocyte action potentials was examined in isolated electric organ using two-electrode current clamp. Electric organ discharge and action potential amplitude and pulse duration increased in response to 8-bromo-cAMP. Pulse and action potential duration both increased by about 25%. However, the increase in electric organ discharge amplitude (approximately 400%) was several-fold greater than the action potential amplitude increase (approximately 40%). Resting membrane resistance decreased in electrocytes exposed to 8-bromo-cAMP. We propose that in the Thevenin equivalent circuit of the electric organ a moderate increase in action potential amplitude combined with a decrease in internal resistance produces a greater voltage drop across the external resistance (the water around the fish), accounting for the large increase in the externally recorded electric organ discharge.

8-Bromo Cyclic Adenosine Monophosphate↗
PubMed1991

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

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.

Animal Communication↗
PubMed2006

Social interaction and cortisol treatment increase cell addition and radial glia fiber density in the diencephalic periventricular zone of adult electric fish, Apteronotus leptorhynchus.

In electric fish, Apteronotus leptorhynchus, both long-term social interaction and cortisol treatment potentiates chirping, an electrocommunication behavior that functions in aggression. Chirping is controlled by the diencephalic prepacemaker nucleus (PPn-C) located just lateral to the ventricle. Cells born in adult proliferative zones such as the periventricular zone (PVZ) can migrate along radial glial fibers to other brain regions, including the PPn-C. We examined whether social interactions or cortisol treatment influenced cell addition and radial glia fiber formation by (1) pairing fish (4 or 7 days) or (2) implanting fish with cortisol (7 or 14 days). Adult fish were injected with bromodeoxyuridine 3 days before sacrifice to mark cells that were recently added. Other fish were sacrificed after 1 or 7 days of treatment to examine vimentin immunoreactivity (IR), a measure of radial glial fiber density. Paired fish had more cell addition than isolated fish at 7 days, coinciding temporally with the onset of socially induced increase in chirping behavior. Paired fish also had higher vimentin IR at 1 and 7 days. For both cell addition and vimentin IR, the effect was regionally specific, increasing in the PVZ adjacent to the PPn-C, but not in surrounding regions. Cortisol increased cell addition at 7 days, correlating with the onset of cortisol-induced changes in chirping, and in a regionally specific manner. Cortisol for 14 days increased cell addition, and cortisol for 7 days increased vimentin IR but in a regionally non-specific manner. The correlation between treatment-induced changes in chirping and regionally specific increases in cell addition, and radial glial fiber formation suggests a causal relationship between such behavioral and brain plasticity in adults, but this hypothesis will require further testing.

Animal Communication↗
PubMed1999

Waveform discrimination, phase sensitivity and jamming avoidance in a wave-type electric fish

The electric organ discharge (EOD) of most species of the freshwater knifefishes (Gymnotiformes) of South America is of the wave, not the pulse, type. Wave EODs are usually of constant frequency and amplitude, and show a bewildering multitude of species-characteristic waveforms. The EOD of Eigenmannia is sexually dimorphic in waveform and in the intensity of its higher harmonics. In a go/no go paradigm, trained food-rewarded fish discriminated between these waveforms, and naive (untrained) fish showed a significant preference. To determine whether spectral or waveform (time) cues are used by the fish, artificial stimuli of identical amplitude spectrum were synthesized that differed only in phase relationship between their harmonics, i.e. waveform, and the fish discriminated even among these stimulus waveforms (i.e. spectral cues are not required). Our sensory model predicts that, for successful waveform detection, a minimum frequency difference is required between the stimulus and the EOD. As expected, trained fish confused test stimuli of different waveform that were frequency-clamped and phase-locked to the EOD (frequency difference 0 Hz). Opening the electronic feedback loop immediately restored discrimination performance on an on/off basis, and a strong jamming avoidance response (JAR; a frequency shift away from the stimulus) accompanied every behavioural decision (to go for a food reward). The strong habituation of the JAR that occurs in response to stimuli of no behavioural consequence (the usual test situation) was not seen in the present experiments. The proposed sensory model (which is based on time-marking T electroreceptors) is supported by these experiments, and a biological function for the JAR - subserving EOD waveform discrimination is shown to be useful in a social context.

Journal Article↗
PubMed2000

Three-dimensional analysis of object properties during active electrolocation in mormyrid weakly electric fishes (Gnathonemus petersii).

Weakly electric fishes are nocturnal and orientate in the absence of vision by using their electrical sense. This enables them not only to navigate but also to perceive and recognize objects in complete darkness. They create an electric field around their bodies by producing electric signals with specialized electric organs. Objects within this field alter the electric current at electroreceptor organs, which are distributed over almost the entire body surface. During active electrolocation, fishes detect, localize and analyse objects by monitoring their self-produced electric signals. We investigated the ability of the mormyrid Gnathonemus petersii to perceive objects three-dimensionally in space. Within a range of about 12 cm, G. petersii can perceive the distance of objects. Depth perception is independent of object size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters (maximal slope and maximal amplitude) of the electrical image which each object projects onto the fish's skin. During active electrolocation, electric fishes cannot only locate objects in space but in addition can determine the three-dimensional shape of an object. Up to certain limits, objects are spontaneously categorized according to their shapes, but not according to their sizes or the materials of which they are made.

Animals↗
PubMed1987

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.

Animal Communication↗
PubMed2003

Diversity in the structure of electrocommunication signals within a genus of electric fish, Apteronotus.

Some gymnotiform electric fish modulate their electric organ discharge for intraspecific communication. In Apteronotus leptorhynchus, chirps are usually rapid (10-30 ms) modulations that are activated through non- N-methyl- d-aspartate (non-NMDA) glutamate receptors in the hindbrain pacemaker nucleus. Males produce longer chirp types than females and chirp at higher rates. In Apteronotus albifrons, chirp rate is sexually monomorphic, but chirp structure (change in frequency and amplitude during a chirp) was unknown. To better understand the neural regulation and evolution of chirping behavior, we compared chirp structure in these two species under identical stimulus regimes. A. albifrons, like A. leptorhynchus, produced distinct types of chirps that varied, in part, by frequency excursion. However, unlike in A. leptorhynchus, chirp types in A. albifrons varied little in duration, and chirps were all longer (70-200 ms) than those of A. leptorhynchus. Chirp type production was not sexually dimorphic in A. albifrons, but within two chirp types males produced longer chirps than females. We suggest that species differences in chirp duration might be attributable to differences in the relative proportions of fast-acting (non-NMDA) and slow-acting (NMDA) glutamate receptors in the pacemaker. Additionally, we map species difference onto a phylogeny and hypothesize an evolutionary sequence for the diversification of chirp structure.

Acoustics↗
PubMed2005

Electric interactions through chirping behavior in the weakly electric fish, Apteronotus leptorhynchus.

The weakly electric fish Apteronotus leptorhynchus produces wave-like electric organ discharges distinguished by a high degree of regularity. Transient amplitude and frequency modulations ("chirps") can be evoked in males by stimulation with the electric field of a conspecific. During these interactions, the males examined in this study produced six types of chirps, including two novel ones. Stimulation of a test fish with a conspecific at various distances showed that two electrically interacting fish must be within 10 cm of each other to evoke chirping behavior in the neighboring fish. The chirp rate of all but one chirp type elicited by the neighboring fish was found to be negatively correlated with the absolute value of the frequency difference between the two interacting fish, but independent of the sign of this difference. Correlation analysis of the instantaneous rates of chirp occurrence revealed two modes of interactions characterized by reciprocal stimulation and reciprocal inhibition. Further analysis of the temporal relationship between the chirps generated by the two fish during electric interactions showed that the chirps generated by one individual follow the chirps of the other with a short latency of approximately 500-1,000 ms. We hypothesize that this "echo response" serves a communicatory function.

Animal Communication↗
PubMed1999

Communication signals and sound production mechanisms of mormyrid electric fish.

The African weakly electric fishes Pollimyrus isidori and Pollimyrus adspersus (Mormyridae) produce elaborate acoustic displays during social communication in addition to their electric organ discharges (EODs). In this paper, we provide new data on the EODs of these sound-producing mormyrids and on the mechanisms they use to generate species-typical sounds. Although it is known that the EODs are usually species-specific and sexually dimorphic, the EODs of closely related sound-producing mormyrids have not previously been compared. The data presented demonstrate that there is a clear sexual dimorphism in the EOD waveform of P. isidori. Females have a multi-phasic EOD that is more complex than the male's biphasic EOD. In this respect, P. isidori is similar to its more thoroughly studied congener P. adspersus, which has a sexually dimorphic EOD. The new data also reveal that the EODs of these two species are distinct, thus showing for the first time that species-specificity in EODs is characteristic of these fishes, which also generate species-specific courtship sounds. The sound-generating mechanism is based on a drumming muscle coupled to the swimbladder. Transverse sections through decalcified male and female P. adspersus revealed a muscle that envelops the caudal pole of the swimbladder and that is composed of dorso-ventrally oriented fibers. The muscle is five times larger in males (14.5+/-4.4 microl, mean +/- s.d.) than in females (3.2+/-1.8 microl). The fibers are also of significantly larger diameter in males than in females. Males generate courtship sounds and females do not. The function of the swimbladder muscle was tested using behavioral experiments. Male P. adspersus normally produce acoustic courtship displays when presented with female-like electrical stimuli. However, local anesthesia of the swimbladder muscle muted males. In control trials, males continued to produce sounds after injection of either lidocaine in the trunk muscles or saline in the swimbladder muscles.

Air Sacs↗
PubMed2001

Cutaneous electrical oscillation in a weakly electric fish, Gymnarchus niloticus.

An African electric fish, Gymnarchus niloticus. ceases its electric organ discharge for a prolonged time in response to external electrical signals. During the cessation of electric organ discharges from the electric organ, a weak sinusoidal signal (approximately 0.1 mV cm(-1)) near the fish's previous discharge frequency was recorded near the body. The oscillatory potentials at all points on the body surface were synchronized and had a complex spatial distribution. The source of the potential was determined to be within the dermal tissue. Electroreceptive central neurons that responded to a moving target near the fish with normal electric organ discharges also responded to the same target when the electric organ discharge was interrupted and the potential from the skin existed. This result suggests that the fish may be able to electrolocate objects without the discharge from the electric organ.

Animals↗
PubMedDate not supplied

Distance discrimination during active electrolocation in the weakly electric fish Gnathonemus petersii.

Weakly electric fish use active electrolocation for orientation at night. They emit electric signals (electric organ discharges) which generate an electrical field around their body. By sensing field distortions, fish can detect objects and analyze their properties. It is unclear, however, how accurately they can determine the distance of unknown objects. Four Gnathonemus petersii were trained in two-alternative forced-choice procedures to discriminate between two objects differing in their distances to a gate. The fish learned to pass through the gate behind which the corresponding object was farther away. Distance discrimination thresholds for different types of objects were determined. Locomotor and electromotor activity during distance measurement were monitored. Our results revealed that all individuals quickly learned to measure object distance irrespective of size, shape or electrical conductivity of the object material. However, the distances of hollow, water-filled cubes and spheres were consistently misjudged in comparison with solid or more angular objects, being perceived as farther away than they really were. As training continued, fish learned to compensate for these 'electrosensory illusions' and erroneous choices disappeared with time. Distance discrimination thresholds depended on object size and overall object distance. During distance measurement, the fish produced a fast regular rhythm of EOD discharges. A mechanisms for distance determination during active electrolocation is proposed.

Animals↗
PubMed1997

Estrogen modifies an electrocommunication signal by altering the electrocyte sodium current in an electric fish, Sternopygus.

Many species of electric fish emit sexually dimorphic electrical signals that are used in gender recognition. In Sternopygus, mature females produce an electric organ discharge (EOD) that is higher in frequency and shorter in pulse duration than that of mature males. EOD pulse duration is determined by ion currents in the electrocytes, and androgens influence EOD pulse duration by altering the inactivation kinetics of the electrocyte sodium current. We examined whether estrogen modulates the female-specific EOD and, if so, whether it regulates EOD pulse duration by acting on the same androgen-sensitive ion current in the electrocytes. We implanted gonadectomized Sternopygus with either empty SILASTIC capsules (control), one capsule filled with estradiol-17beta (E2; low dose), or three capsules of E2 (high dose). Twelve days after implantation, E2-treated fish had plasma E2 levels approximately 3.3-fold (low dose) or approximately 7.1-fold (high dose) higher than controls. After implantation, both E2-treated groups had higher EOD frequency and shorter EOD pulse duration than controls and their own preimplantation values. Through immunocytochemistry, we identified immunoreactive estrogen receptors in the nuclei of electrocytes, indicating that these cells are directly responsive to estrogen. In addition, voltage-clamp studies showed that E2 affected the electrocyte ion currents kinetics: the sodium inactivation time constant was significantly lower in E2-treated fish than in controls. Thus, sexual dimorphism in the electrocommunication signal results, at least in part, from estrogens and androgens acting in opposite directions on the same ion current in the electrocytes.

Animals↗
PubMed1987

Hormone-induced and maturational changes in electric organ discharges and electroreceptor tuning in the weakly electric fish Apteronotus.

Plasticity in the frequency of the electric organ discharge (EOD) and electroreceptor tuning of weakly electric fish was studied in the genus Apteronotus. Both hormone-induced and maturational changes in EOD frequency and electroreceptor tuning were examined. Apteronotus is different from all other steroid-responsive weakly electric fish in that estradiol-17 beta, rather than androgens, induces discharge frequency decreases. This result can account for the 'reversed' discharge frequency dimorphism found in Apteronotus in which, counter to all other known sexually dimorphic electric fish, females have lower discharge frequencies than males. Studies of electroreceptor tuning in Apteronotus indicate that electroreceptors are closely tuned to the frequency of the EOD. This finding was noted not only in adult animals, but also in juvenile animals shortly after the onset of their EODs. Tuning plasticity in Apteronotus, as in other species studied, is associated with altered EOD frequencies and was noted in both maturational EOD changes and in estrogen-induced changes. Thus, tuning plasticity appears to be a general phenomenon which occurs concurrent with a variety of EOD changes.

Androgens↗
PubMed2001

Arginine vasotocin modulates a sexually dimorphic communication behavior in the weakly electric fish Apteronotus leptorhynchus.

South American weakly electric fish produce a variety of electric organ discharge (EOD) amplitude and frequency modulations including chirps or rapid increases in EOD frequency that function as agonistic and courtship and mating displays. In Apteronotus leptorhynchus, chirps are readily evoked by the presence of the EOD of a conspecific or a sinusoidal signal designed to mimic another EOD, and we found that the frequency difference between the discharge of a given animal and that of an EOD mimic is important in determining which of two categories of chirp an animal will produce. Type-I chirps (EOD frequency increases averaging 650 Hz and lasting approximately 25 ms) are preferentially produced by males in response to EOD mimics with a frequency of 50-200 Hz higher or lower than that of their own. The EOD frequency of Apteronotus leptorhynchus is sexually dimorphic: female EODs range from 600 to 800 Hz and male EODs range from 800 to 1000 Hz. Hence, EOD frequency differences effective in evoking type-I chirps are most likely to occur during male/female interactions. This result supports previous observations that type-I chirps are emitted most often during courtship and mating. Type-II chirps, which consist of shorter-duration frequency increases of approximately 100 Hz, occur preferentially in response to EOD mimics that differ from the EOD of the animal by 10-15 Hz. Hence these are preferentially evoked when animals of the same sex interact and, as previously suggested, probably represent agonistic displays. Females typically produced only type-II chirps. We also investigated the effects of arginine vasotocin on chirping. This peptide is known to modulate communication and other types of behavior in many species, and we found that arginine vasotocin decreased the production of type-II chirps by males and also increased the production of type-I chirps in a subset of males. The chirping of most females was not significantly affected by arginine vasotocin.

Animal Communication↗