Spatial distribution of the medullary command signal within the electric organ of Gymnotus carapo

The pacemaker nucleus of Gymnotus carapo contains two types of neurons: pacemaker cells which set up the frequency of the electric organ discharge (EOD) and relay cells which convey the command signal to the spinal cord. Direct activation of a single relay cell provides enough excitation to discharge a pool of spinal electromotor neurons and electrocytes, generating a small EOD (unit EOD). Different relay cells generate unit EODs of variable size and waveform, indicating the involvement of different groups of electrocytes. A special technique of EOD recording (multiple air-gap) was combined with intracellular stimulation of relay cells to study the spatial distribution within the electric organ (EO) of the command signal arising from different relay cells. Three types of relay cells could be identified: type I commanding the rostral 10% of the EO, type II which distribute their command all along the EO and type III driving the caudal 30%. Waveform analysis of unit EODs indicates that doubly innervated electrocytes which are the most relevant for attaining the specific EOD waveform, receive a favored command from the pacemaker nucleus.Abbreviations CV conduction velocity - EMF electromotive force - EMN electromotor neuron - EO electric organ - EOD electric organ discharge - PN pacemaker nucleus - uEOD unit electric organ discharge     

Waveform generation in Rhamphichthys rostratus (L.) (Teleostei,Gymnotiformes)

Rhamphichthys rostratus (L.) emits brief pulses (2 ms) repeated very regularly at 50 Hz. The electric organ shows a heterogeneous distribution of the electrocyte tubes and the occurrence of three electrocyte types (caudally innervated, rostrally innervated and marginallycaudally innervated). In the sub-opercular region the electric organ consists of a pair of tubes containing only caudally innervated electrocytes. At the abdominal region the EO consists of three pairs of tubes. Each pair contains one of the described electrocyte types. The number of electrocyte tubes increases toward the tail to reach nine or ten pairs in the most caudal segments. In the intermediate region most tubes contain doubly innervated electrocytes except the ventral pair that contains caudally innervated electrocytes. The caudal 25% contains exclusively caudally innervated electrocytes. The electric organ discharge consists of five wave components (V1 to V5). Electrophysiological data are consistent with the hypothesis that V1 results from the activity of the rostral faces of rostrally innervated electrocytes. V2 results from the activities of rostral faces of marginally-caudally innervated electrocytes while V3 results from the activities of caudal faces of most electrocytes. Curarization experiments demonstrated that V4 and V5 result from action potential invasion and are not directly elicited by neural activity.Abbreviations AEN1 anterior electromotor nerve 1 - AEN2 anterior electromotor nerve 2 - BMB boraxic methylene blue - CIE caudally innervated electrocytes - EMF electromotive force - EO electric organ - EOD electric organ discharge - I current amplitude - MCIE marginally-caudally innervated electrocytes - MT medial tubes - PEN posterior electromotor nerve - R _n internal impedance - RIE rostrally innervated electrocytes - Rl load resistor - SAT short abdominal tubes - V voltage 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.     

Waveform generation of the electric organ discharge inGymnotus carapo

Summary The electric organ (EO) ofGymnotus carapo was studied using different neurohistological techniques including conventional electron microscopy. The electric tissue extends along the fish body from the pectoral girdle to the tip of the tail, constituting a single, undivided organ. However, taking into account the number, arrangement, and innervation of the electrocytes, it is possible to divide the EO into three different portions. The more rostral portion is included within the ventral wall of the abdominal cavity. It consists of singly and doubly innervated electrocytes arranged in two rows at each side of the midline. Innervation of this zone is supplied by the first 5–7 segmental nerves and by the anterior electromotor nerves. Segmental nerves terminate on the rostral faces of doubly innervated electrocytes; axons stemming from the anterior electromotor nerves end on the caudal faces of both doubly and singly innervated electrocytes. There is an intermediate body-tail region in which the electrocytes are arranged in four dorsoventral tubes (tubes 1 to 4) on each side of the midline. In this zone, doubly innervated electrocytes (confined within tube 1) coexist together with singly innervated ones, receiving nerve terminals on their caudal faces (tubes 2, 3, and 4). The innervation characteristics appear modified at more distal portions of the tail where the doubly innervated electrocytes of tube 1 are replaced by singly innervated units. The most distal portion of the EO (approximately its terminal 30%) consists of numerous, homogeneously innervated electrocytes with nerve endings distributed exclusively on their caudal faces. Nerve supply to the intermediate and distal regions derives from the posterior electromotor nerves (PENs) which appear as well-defined anatomical entities beyond the level of metamere XXVII. At the bodytail and more distal regions the innervation pattern of the EO is particularly complex. Thin nerve trunks arise from the PENs and project ventrally toward the electrocyte tubes. Before reaching the electric tissue the electromotor axons branch frequently. Our anatomical studies indicate that the EO is heterogeneous, a feature consistent with most recent electrophysiological and biophysical experiments.Abbreviations AEN anterior electromotor nerve - EMN electromotoneurons - EO electric organ - EOD electric organ discharge - LLN lateral line nerve - PEN posterior electromotor nerve     

Distinct mechanisms of modulation in a neuronal oscillator generate different social signals in the electric fishHypopomus

Summary The medullary pacemaker nucleus of the gymnotiform electric fish,Hypopomus, is a relatively simple neuronal oscillator which contains pacemaker cells and relay cells. The pacemaker cells generate a regular discharge cycle and drive the relay cells which trigger pulse-like electric organ discharges (EODs). The diencephalic prepacemaker nucleus (PPN) projects to the pacemaker nucleus and modulates its activity to generate a variety of specific discharge patterns which serve as communicatory signals (Figs. 2 and 3).While inducing such signals by microiontophoresis of L-glutamate to the region of the PPN (Fig. 4) of curarized animals, we monitored the activity of neurons in the pacemaker nucleus intracellularly. We found that pacemaker cells and relay cells were affected differently in a manner specific to the type of EOD modulation (Figs. 5–10). The normal sequence of pacemaker cell and relay cell firing was maintained during gradual rises and falls in discharge rate. Both types of cells ceased to fire during interruptions following a decline in discharge rate. During sudden interruptions, however, relay cells were steadily depolarized, while pacemaker cells continued to fire regularly. Short and rapid barrages of EODs, called chirps, were generated through direct and synchronous activation of the relay cells whose action potentials invaded pacemaker cells antidromically and interfered with their otherwise regular firing pattern.Abbreviations EOD electric organ discharge - HRP horseradish peroxidase - NMDA N-Methyl-D-Aspartate - PPN prepacemaker nucleus     

Single electrocytes produce a sexually dimorphic signal in South American electric fish,Hypopomus occidentalis (Gymnotiformes,Hypopomidae)

Summary Hypopomus occidentalis is a weakly electric Gymnotiform fish with a pulse-type electric organ discharge (EOD).Hypopomus used in this study were taken from one of the northernmost boundaries of this species, the Atlantic drainage of Panama where the animals breed at the beginning of the dry season (December). In normal breeding populations,Hypopomus occidentalis exhibit a sexual dimorphism in EOD and morphology. Mature males are large with a broad tail and have an EOD characterized by a low peak power frequency. Females and immature males are smaller, having a slender tail and EODs with higher peak power frequencies (Fig. 1). This study describes differences in the EOD and electric organ morphology between breeding field populations of male and femaleHypopomus. Changes in physiology, morphology and EOD shape which may accompany this seasonal change were examined in steroid injected fish, using standard histological and physiological techniques.A group of females were injected with hormones (5-dihydrotestosterone (DHT), estrogen or saline) to assess changes in their morphology and EOD. Animals treated with DHT developed characteristics which mimicked the sexually dimorphic characteristics of a male, while the other groups did not (see Fig. 5). Tissue from the tails of breeding males and females, and females treated with DHT, were sampled to measure the size of the electrocytes in the tail. The broader tail of males and DHT-females is composed of large electrocytes, whereas the slender tail of normal females is composed of smaller electrocytes. Therefore, the increase in the tail width in the female DHT group is caused by an enlargement of the electrocytes in this area.Intracellular recordings from the electrocytes of saline and DHT injected females show a difference in the responses of the rostral faces of the electrocytes from the two groups, which reflect the differences in their EODs. Saline-treated animals had symmetrical EODs (the first and second phase of the EOD were equal in duration and amplitude), while the physiological responses from each face of the electrocytes yielded responses that were similarly equal in duration and amplitude. DHT-treated animals had asymmetrical EODs (the first phase of the EOD was similar to that of saline treated fish and larger in amplitude and shorter in duration than the second phase) and the physiological responses of the electrocytes reflected this asymmetry. The differential recordings across the caudal face were similar to those from saline treated fish, while the responses from the rostral face were longer in duration and smaller in amplitude.These data suggest that the effects of androgens underlie the changes in single electrocytes which produce the sexually dimorphic signals and morphology present in natural breeding populations ofHypopomus occidentalis.     

Spinal mechanisms of electric organ discharge synchronization in Gymnotus carapo

Summary The duration of the electric organ discharge (EOD) in Gymnotus carapo is brief and independent of fish size. Spinal mechanisms involved in electrocyte synchronization were explored by recording spontaneous action potentials of single fibers from the electromotor bulbospinal tract (EBST). Using the field potential of the medullary electromotor nucleus (MEN) as a temporal reference we calculated the orthodromic conduction velocity (CV) of these fibers (range: 10.7–91 m/s).The CVs (in m/s) of fibers recorded at the same level of the spinal cord were significantly different in small and large fish; this difference disappeared when CV were expressed as percentage of body length/ms. Plotting these values against conduction distance (also in %) showed that low CV fibers predominate in the rostral cord while only fast fibers are found at distal levels. Moreover, antidromic stimulation of the distal cord was only effective on high CV fibers. The orthodromic CVs in the distal portion of the recorded fibers were calculated by collision experiments; no significant differences were found between proximal and distal portions.The spatial distribution of CV values within the EBST is proposed to play the main role in synchronizing the electromotoneurons' activity along the spinal cord.Abbreviations EOD electric organ discharge - EO electric organ - EBST electromotor bulbospinal tract - MEN medullary electromotor nucleus - CV conduction velocity - EMN electromotoneuron     

A field potential analysis of the electromotor system in Gymnotus carapo

To investigate the synchronization mechanisms operating in the electromotor system, electric organ discharge related field potentials of neural origin were recorded in intact fish. Components corresponding to the relay nucleus, the bulbar-spinal electromotor tract, the electromotoneurons and the peripheral nerves were identified. Delays between components were used to estimate the following intervals: (1) the conduction time along the cord (central conduction interval), (2) the interval between the local activation of the tract and the electromotoneuron firing within a restricted portion of the cord (coupling interval) and (3) the conduction time along the peripheral axons plus the time taken by synaptic activation of the electrocytes (peripheral interval). While central conduction interval increases with the distance from the pacemaker, the coupling interval diminishes. Peripheral interval also diminishes from rostral to caudal targets in the electric organ. It is concluded that the electrocyte synchronization, resulting from matching the three above-defined intervals, is achieved by a cascade of synergetic mechanisms.Abbreviations EBST electromotor bulbar-spinal tract - EMN electromotoneuron - EO electric organ - EOD electric organ discharge - PEN posterior electromotor nerve - PNA peripheral nerve activity - SFP skin surface field potentials     

Interruption of pacemaker signals is mediated by GABAergic inhibition of the pacemaker nucleus in the African electric fish <Emphasis Type="Italic">Gymnarchus niloticus</Emphasis>

The wave-type African weakly electric fish Gymnarchus niloticus produces electric organ discharges (EODs) from an electric organ in the tail that is driven by a pacemaker complex in the medulla, which consists of a pacemaker nucleus, two lateral relay nuclei and a medial relay nucleus. The prepacemaker nucleus (PPn) in the area of the dorsal posterior nucleus of the thalamus projects exclusively to the pacemaker nucleus and is responsible for EOD interruption behavior. The goal of the present study is to test the existence of inhibition of the pacemaker nucleus by the PPn. Immunohistochemical results showed clear anti-GABA immunoreactive labeling of fibers and terminals in the pacemaker nucleus, but no apparent anti-glycine immunoreactivity anywhere in the pacemaker complex. GABA injection into the pacemaker nucleus could induce EOD interruptions that are comparable to the interruptions induced by glutamate injection into the PPn. Application of the GABA_A receptor blocker bicuculline methiodide reversibly eliminated the effects of stimulation of the PPn. Thus the EOD interruption behavior in Gymnarchus is mediated through GABAergic inhibition of the pacemaker nucleus by the PPn.     

A hormone-sensitive communication system in an electric fish

The electric communication system includes both special muscle-derived cells or electrocytes that produce species-typical electric signals, or electric organ discharges (EODs), and specialized sensory receptors, or electroreceptors, that encode the electric fields set up by EODs. Steroid hormones can influence the characteristic properties of both EODs and electroreceptors. Steroids appear to directly effect the anatomy and physiology of the electrocytes that generate an EOD. In contrast, the steroid effect on electroreceptors may be predominantly via an indirect mechanism whereby changes in the spectral characteristics of the EOD appear to induce changes in the spectral sensitivity of electroreceptors. Continued studies of electrosensory and electromotor systems will offer insights into the cellular bases for the development and evolution of steroid-sensitive pathways in the vertebrate nervous system.     

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.     

The coding of signals in the electric communication of the gymnotiform fish Eigenmannia: From electroreceptors to neurons in the torus semicircularis of the midbrain

Summary In the context of aggression and courtship, Eigenmannia repeatedly interrupts its electric organ discharges (EODs) These interruptions (Fig. 1) contain low-frequency components as well as high-frequency transients and, therefore, stimulate ampullary and tuberous electroreceptors, respectively (Figs. 2, 3). Information provided by these two classes of receptors is relayed along separate pathways, via the electrosensory lateral line lobe (ELL) of the hindbrain, to the dorsal torus semicircularis (TSd) of the midbrain. Some neurons of the torus receive inputs from both types of receptors (Figs. 14, 15), and some respond predominantly to EOD interruptions while being rather insensitive to other forms of signal modulations (Figs. 12, 13). This high selectivity appears to result from convergence and gating of inputs from individually less selective neurons.Abbreviations CP central posterior thalamic nucleus - Df frequency difference between neighbor's EOD and fish's own - DPn dorsal posterior nucleus (thalamus) - EOD electric organ discharge - ELL electrosensory lateral line lobe - JAR jamming avoidance response - LMR lateral mesencephalic reticular formation - nE nucleus electrosensorius - nEb nucleus electrosensorius, beat-related area - nE nucleus electrosensorius, area causing rise of EOD frequency - nE nucleus electrosensorius, area causing fall of EOD frequency - nEar nucleus electrosensorius-acusticolateralis area - NPd nucleus praeeminentialis, pars dorsalis - PPn prepacemaker nucleus - PT pretectal nucleus - SE nucleus subelectrosensorius - TeO optic tectum - TSd dorsal (electrosensory) torus semicircularis - TSv ventral (mechano-sensory and auditory) torus semicircularis     

Electric signaling behavior and the mechanisms of electric organ discharge production in mormyrid fish.

Mormyrid fish communicate and navigate using electric organ discharges (EODs). The EOD is highly stereotyped and provides information on sender identity, including species, sex, reproductive condition, and possibly relative status and individual identity. By contrast, the sequence of pulse intervals (SPI) is variable and plays more of a role in signaling behavioral states. Various types of SPI displays may be produced, including tonic patterns such as 'random' and 'regularized', and phasic patterns such as 'bursts' and cessations'. Certain displays have been linked to specific behaviors such as aggression, submission, courtship and active exploration. In addition, interacting pairs of fish may produce stereotyped displays involving the relative timing of their EODs. The EOD waveform is controlled by the morphological and physiological properties of cells in the electric organ termed electrocytes. Differences in the innervation, morphology, size and membrane characteristics of electrocytes have been directly linked to species and sex differences in the EOD. The generation of each EOD is initiated in the medullary command nucleus (CN), which thereby determines the timing of EOD output. CN does not have any properties of a pacemaker, but rather appears to integrate descending inputs that affect the probability of EOD production. The precommand nucleus (PCN) provides a major source of excitatory input to CN and is itself inhibited by corollary discharge feedback following the production of each EOD. Changes in the activity of PCN and its inhibitory feedback neurons modify EOD output, and therefore drive the generation of SPI patterns. Current studies are addressing the mechanisms underlying the generation of these patterns and preliminary results suggest that different types of signals may be controlled by distinct components of the electromotor system. This is similar to findings in other electrogenic teleosts, suggesting that it may be a general feature in the motor control of signaling behavior.     

Structure and function of neurons in the complex of the nucleus electrosensorius of the gymnotiform fish Eigenmannia: Detection and processing of electric signals in social communication

Summary The complex of the diencephalic nucleus electrosensorius (nE) provides an interface between the electrosensory processing performed by the torus semicircularis and the control of specific behavioral responses. The rostral portion of the nE comprises two subdivisions that differ in the response properties and projection patterns of their neurons. First, the nEb (Fig. 1 B), which contains neurons that are driven almost exclusively by beat patterns generated by the interference of electric organ discharges (EODs) of similar frequencies. Second, the area medial to the nEb, comprising the lateral pretectum (PT) and the nE-acusticolateralis region (nEar, Fig. 1 B-D), which contains neurons excited predominantly by EOD interruptions, signals associated with aggression and courtship. Neurons in the second area commonly receive convergent inputs originating from ampullary and tuberous electroreceptors, which respond to the low-frequency and high-frequency components of EOD interruptions, respectively. Projections of these neurons to hypothalamic areas linked to the pituitary may mediate modulations of a fish's endocrine state that are caused by exposure to EOD interruptions of its mate.Abbreviations a axon - ATh anterior thalamic nucleus - CCb corpus cerebelli - CE central nucleus of the inferior lobe - CP central posterior thalamic nucleus - Df frequency difference between neighbor's EOD and fish's own - DFl nucleus diffusus lateralis of the inferior lobe - DFm nucleus diffusus medialis of the inferior lobe - DTn dorsal tegmental nucleus - EOD electric organ discharge - G glomerular nucleus - Hc caudal hypothalamus - Hd dorsal hypothalamus - Hl lateral hypothalamus - Hv ventral hypothalamus - JAR jamming avoidance response - LL lateral lemniscus - MGT magnocellular tegmental nucleus - MLF medial longitudinal fasciculus - nB nucleus at the base of the optic tract - nE nucleus electrosensorius - nEar nucleus electrosensorius-acusticolateral region - nEb nucleus electrosensorius-beat related area - nE nucleus electrosensorius, area causing rise of EOD frequency - nE nucleus electrosensorius, area causing fall of EOD frequency - nLT nucleus tuberis lateralis - nLV nucleus lateralis valvulae - PC posterior commissure - Pd nucleus praeeminentialis, pars dorsalis - PeG periglomerular complex - PG preglomerular nucleus - PLm medial division of the perilemniscal nucleus - Pn pacemaker nucleus - PPn prepacemaker nucleus - PT pretectal nucleus - PTh prethalamic nucleus - R red nucleus - Sc suprachiasmatic nucleus - SE nucleus subelectrosensorius - TAd nucleus tuberis anterior-dorsal subdivision - TAv nucleus tuberis anterior-ventral subdivision - TeO optic tectum - TL torus longitudinalis - TSd dorsal (electrosensory) torus semicircularis - TSv ventral (mechanosensory and auditory) torus semicircularis - tTB tecto-bulbar tract - VCb cerebellar valvula - VP valvular peduncle - VPn nucleus of the valvular peduncle     

Signal variation and its morphological correlates in <Emphasis Type="Italic">Paramormyrops kingsleyae</Emphasis> provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish

We describe patterns of geographic variation in electric signal waveforms among populations of the mormyrid electric fish species Paramormyrops kingsleyae. This analysis includes study of electric organs and electric organ discharge (EOD) signals from 553 specimens collected from 12 localities in Gabon, West-Central Africa from 1998 to 2009. We measured time, slope, and voltage values from nine defined EOD “landmarks” and determined peak spectral frequencies from each waveform; these data were subjected to principal components analysis. The majority of variation in EODs is explained by two factors: the first related to EOD duration, the second related to the magnitude of the weak head-negative pre-potential, P0. Both factors varied clinally across Gabon. EODs are shorter in eastern Gabon and longer in western Gabon. Peak P0 is slightly larger in northern Gabon and smaller in southern Gabon. P0 in the EOD is due to the presence of penetrating-stalked (Pa) electrocytes in the electric organ while absence is due to the presence of non-penetrating stalked electrocytes (NPp). Across Gabon, the majority of P. kingsleyae populations surveyed have only individuals with P0-present EODs and Pa electrocytes. We discovered two geographically distinct populations, isolated from others by barriers to migration, where all individuals have P0-absent EODs with NPp electrocytes. At two sites along a boundary between P0-absent and P0-present populations, P0-absent and P0-present individuals were found in sympatry; specimens collected there had electric organs of intermediate morphology. This pattern of geographic variation in EODs is considered in the context of current phylogenetic work. Multiple independent paedomorphic losses of penetrating stalked electrocytes have occurred within five Paramormyrops species and seven genera of mormyrids. We suggest that this key anatomical feature in EOD signal evolution may be under a simple mechanism of genetic control, and may be easily influenced by selection or drift throughout the evolutionary history of mormyrids.     

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.     

The development of the Jamming Avoidance Response (JAR) in Eigenmannia: An innate behavior indeed

Summary In its Jamming Avoidance Response (JAR), the gymnotiform electric fish Eigenmannia shifts its electric organ discharge (EOD) frequency away from similar interfering frequencies. Continual behavioral measurements were carried out in 164 juvenile fish until a correct JAR emerged. Sixty-four of these fish were raised in complete isolation, the remainder in a community of their siblings. A correct JAR emerged in fish of 1.2–1.6 cm in body length, corresponding to a developmental age of 24–32 days. In 6 of 164 fish, the emergence of a correct JAR followed an interim appearance of an incorrect JAR, which involved frequency shifts in the direction opposite to those of a correct JAR. The fish raised in isolation developed the same forms of behavior and showed the same sequence in their appearance as did socially raised fish. This indicates that the JAR and its developmental schedule are innate. The appearance of an incorrect JAR suggests initial errors or incompleteness in the wiring of central nervous connections. A correct JAR ultimately emerged even if a stimulus regimen was offered that rewarded frequency shifts in the direction opposite to those of a correct JAR. This indicates that the development of the JAR is immune to experimental alterations of sensory experience.Abbreviations Df frequency difference between a jamming stimulus and fish's EOD - ELL electrosensory lateral line lobe - EO electric organ - EOD electric organ discharge - JAR Jamming Avoidance Response - nE nucleus electrosensorius - nE subnucleus of nE, causing drop of EOD frequency - nE subnucleus of nE, causing rise of EOD frequency - Pn pacemaker nucleus - PPn prepacemaker nucleus     

The jamming avoidance response ofEigenmannia: properties of a diencephalic link between sensory processing and motor output

Summary Brain regions participating in the control ofEigenmannia's electric organ discharge frequency were localized by electrical microstimulation and anatomically identified by means of horseradish peroxidase deposition. A diencephalic region was found which, when stimulated, caused electric organ discharge (EOD) frequency increases of similar magnitude and time course as the frequency increases seen during the jamming avoidance response. Single unit recordings from this region revealed one cell type which preferentially responded to stimuli that cause the acceleration phase of the jamming avoidance response (electric organ discharge frequency increase). A second cell type responded preferentially to stimuli which cause EOD frequency decrease, and both cell types were tuned to stimuli which evoked maximal jamming avoidance behaviors.The results of the horseradish peroxidase experiments showed that the recording and stimulation sites correspond to the previously described nucleus electrosensorius. Our results confirm the earlier finding that this nucleus receives output from the torus semicircularis and we also found that the N. electrosensorius projects to the mesencephalic prepacemaker nucleus. The prepacemaker projects to the medullary pacemaker nucleus which generates the commands that evoke electric organ discharges.The anatomical and physiological results described here establish this diencephalic region as a link between the major sensory processing region for the jamming avoidance response, the torus semicircularis, and a mesencephalic pre-motor region, the prepacemaker nucleus.Abbreviations AM amplitude modulation - DF Delta F - ELLL electrosensory lateral line lobe - EOD electric organ discharge - JAR jamming avoidance response - NE nucleus electrosensorius - PPN prepacemaker nucleus - PN pacemaker nucleus     

Hormone‐mediated modulation of the electromotor CPG in pulse‐type weakly electric fish. Commonalities and differences across species

Like stomatogastric activity in crustaceans, vocalization in teleosts and frogs, and locomotion in mammals, the electric organ discharge (EOD) of weakly electric fish is a rhythmic and stereotyped electromotor pattern. The EOD, which functions in both perception and communication, is controlled by a two‐layered central pattern generator (CPG), the electromotor CPG, which modifies its basal output in response to environmental and social challenges. Despite major anatomo‐functional commonalities in the electromotor CPG across electric fish species, we show that Gymnotus omarorum and Brachyhypopomus gauderio have evolved divergent neural processes to transiently modify the CPG outputs through descending fast neurotransmitter inputs to generate communication signals. We also present two examples of electric behavioral displays in which it is possible to separately analyze the effects of neuropeptides (mid‐term modulation) and gonadal steroid hormones (long‐term modulation) upon the CPG. First, the nonbreeding territorial aggression of G. omarorum has been an advantageous model to analyze the status‐dependent modulation of the excitability of CPG neuronal components by vasotocin. Second, the seasonal and sexually dimorphic courtship signals of B. gauderio have been useful to understand the effects of sex steroids on the responses to glutamatergic inputs in the CPG. Overall, the electromotor CPG functions in a regime that safeguards the EOD waveform. However, prepacemaker influences and hormonal modulation enable an enormous versatility and allows the EOD to adapt its functional state in a species‐, sex‐, and social context‐specific manners.     

Individual prepacemaker neurons can modulate the pacemaker cycle of the gymnotiform electric fish,Eigenmannia

Summary The prepacemaker nucleus (PPN) in the midbrain of the gymnotiform electric fishEigenmannia provides the only known neuronal input to the medullary pacemaker nucleus, which triggers each electric organ discharge (EOD) cycle by a single command pulse. Electrical stimulation of the PPN elicited two distinct forms of modulations in the pacemaker activity, brief accelerations, hence referred to as chirps, and gradual frequency shifts with a time constant of approximately one second. The associated EOD modulations were indistinguishable from natural communication signals. Depending upon the site of stimulation, the two forms of modulation could be elicited alone or superimposed (Fig. 1). Stimulation sites eliciting only chirps could be separated from sites eliciting only gradual shifts by as little as 60 m. The magnitude of the elicited chirps depended upon the timing of the pulse stimulus with reference to the phase of the pacemaker cycle (Figs. 2, 3).Extracellular and intracellular recordings of single PPN neurons revealed that an action potential from a single neuron generates a chirp, and that the magnitude of the chirp depends upon the timing of the action potential with reference to the phase of the pacemaker cycle (Figs. 4, 5). The spike activity of these neurons had no relation to the jamming avoidance response (JAR), suggesting independent neuronal mechanisms for chirps and the JAR. Depolarization of such neurons by current injection produced bursts of chirps (Fig. 6), and intracellular injection of Lucifer Yellow identified these cells as a large type of PPN neuron which could also be retrogradely labeled from the pacemaker with horseradish peroxidase (HRP) (Fig. 7). We were unable to record from neurons linked to gradual shifts of the pacemaker frequency, although the JAR was elicited continually during the experiments. A smaller cell type of the PPN which can be retrogradely labeled with HRP but so far could not be recorded may control gradual frequency shifts.Abbreviations PPN prepacemaker nucleus - JAR jamming avoidance response - EOD electric organ discharge - Df neighbor's EOD frequency (or its mimic) minus animal's own EOD frequency (or its mimic)