Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish

 Gymnotiform fish of the genera Apteronotus and Eigenmannia provide an excellent vertebrate model system to study neural mechanisms controlling behavioral plasticity. These teleosts generate, by means of an electric organ, quasi-sinusoidal discharges of extremely stable frequency and waveform. Modulations consisting of transient rises in discharge frequency are produced during social encounters, and play an important role in communication. These so-called “chirps” exhibit a remarkable sexual dimorphism, as well as an enormous seasonal and individual variability. Chirping behavior is controlled by a subset of neurons in the complex of the central posterior/prepacemaker nucleus in the diencephalon. It is hypothesized that the plasticity in the performance of chirping behavior is, at least in part, governed by two mechanisms: first, by seasonally induced structural changes in dendritic morphology of neurons of the prepacemaker nucleus, thus leading to pronounced alterations in excitatory input. Second, by androgen-controlled changes in the innervation pattern of the prepacemaker nucleus by fibers expressing the neuropeptide substance P. In addition to these two dynamic processes, cells are generated continuously and at high number in the central posterior/prepacemaker nucleus during adulthood. This phenomenon may provide the basis for a “refreshment”, thus facilitating possible changes in the underlying neural network. Accepted: 17 September 1990     

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

The electric fish, Eigenmannia, will smoothly shift the frequency of its electric organ discharge away from an interfering electric signal. This shift in frequency is called the jamming avoidance response (JAR). In this article, we analyze the behavioral development of the JAR and the anatomical development of structures critical for the performance of the JAR. The JAR first appears when juvenile Eigenmannia are approximately 1 month old, at a total length of 13–18 mm. We have found that the establishment of much of the sensory periphery and of central connections precedes the onset of the JAR. We describe three aspects of the behavioral development of the JAR: (a) the onset and development of the behavior is closely correlated with size, not age; (b) the magnitude (in Hz) of the JAR increases with size until the juveniles display values within the adult range (10–20 Hz) at a total length of 25–30 mm; and (3) the JAR does not require prior experience or exposure to electrical signals. Raised in total electrical isolation from the egg stage, animals tested at a total length of 25 mm performed a correct JAR when first exposed to the stimulus. We examine the development of anatomical areas important for the performance of the JAR: the peripheral electrosensory system (mechano- and electroreceptors and peripheral nerves); and central electrosensory pathways and nuclei [the electrosensory lateral line lobe (ELL), the lateral lemniscus, the torus semicircularis, and the pacemaker nucleus]. The first recognizable structures in the developing electrosensory system are the peripheral neurites of the anterior lateral line nerve. The afferent nerves are established by day 2, which is prior to the formation of receptors in the epidermis. Thus, the neurites wait for their targets. This sequence of events suggests that receptor formation may be induced by innervation of primordial cells within the epidermis. Mechanoreceptors are first formed between day 3 and 4, while electroreceptors are first formed on day 7. Electroreceptor multiplication is observed for the first time at an age of 25 days and correlates with the onset of the JAR. The somata of the anterior lateral line nerve ganglion project afferents out to peripheral electroreceptors and also send axons centrally into the ELL. The first electroreceptive axons invade the ELL by day 6, and presumably a rough somatotopic organization and segmentation within the ELL may arise as early as day 7. Axonal projections from the ELL to the torus develop after day 18. Within the torus semicircularis, giant cells are necessary for the performance of the JAR. Giant cell numbers increase exponentially during development and the onset of the JAR coincides with a minimum of at least 150 giant cells and the attainment of a total length of at least 15 mm and at least 150 giant cells. Pacemaker and relay cells comprise the adult Eigenmannia pacemaker nucleus. The growth and differentiation of these cell types also correlates with the onset of the JAR in developing animals. We describe a gradual improvement of sensory abilities, as opposed to an explosive onset of the mature JAR. We further suggest that this may be a rule common in most developing behavioral systems. © 1992 John Wiley & Sons, Inc.     

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

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

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     

Melanocortins regulate the electric waveforms of gymnotiform electric fish

The hypothalamic-pituitary-adrenal/interrenal axis couples serotonergic activity in the brain to the peripheral regulators of energy balance and response to stress. The regulation of peripheral systems occurs largely through the release of peptide hormones, especially the melanocortins (adrenocorticotropic hormone [ACTH] and alpha melanocyte stimulating hormone [α-MSH]), and beta-endorphin. Once in circulation, these peptides regulate a wide range of processes; α-MSH in particular regulates behaviors and physiologies with sexual and social functions. We investigated the role of the HPI and melanocortin peptides in regulation of electric social signals in the gymnotiform electric fish, Brachyhypopomus pinnicaudatus. We found that corticotropin releasing factor, thyrotropin-releasing hormone, and α-MSH, three peptide hormones of the HPI/HPA, increased electric signal waveform amplitude and duration when injected into free-swimming fish. A fourth peptide, a synthetic cyclic-α-MSH analog attenuated the normal circadian and socially-induced EOD enhancements in vivo. When applied to the electrogenic cells (electrocytes) in vitro, only α-MSH increased the amplitude and duration of the electrocyte discharge similar to the waveform enhancements seen in vivo. The cyclic-α-MSH analog had no effect on its own, but blocked or attenuated α-MSH-induced enhancements in the single-cell discharge parameters, demonstrating that this compound functions as a silent antagonist at the electrocyte. Overall, these results strongly suggest that the HPI regulates the EOD communication signal, and demonstrate that circulating melanocortin peptides enhance the electrocyte discharge waveform.     

Ultrastructural evidence of GABA-ergic inhibition and glutamatergic excitation in the pacemaker nucleus of the gymnotiform electric fish,Hypopomus

The medullary pacemaker nucleus of Hypopomus triggers each electric organ discharge (EOD) by a single command pulse. It consists of electrotonically coupled pacemaker cells, which generate the rhythm, and relay cells, which follow the pacemaker cells and excite the spinal motoneurons of the electric organ. The pacemaker cells receive two inputs from the complex of the diencephalic prepacemaker nucleus (PPn), a GABA-ergic inhibition and a glutamatergic excitation. Relay cells, on the other hand, receive two glutamatergic inputs, one from a subnucleus of the PPn, the PPn-C, and a second from the sublemniscal prepacemaker nucleus (SPPn).We have labelled afferents to the pacemaker nucleus by injecting HRP to specific sites of the prepacemaker complex. By using immunogold-labelled antibodies and en-grid staining techniques, we demonstrated GABA and glutamate immunoreactivity in labelled synaptic profiles of ultra-thin sections of the pacemaker nucleus. The two types of synapses were interspersed on the surfaces of pacemaker cells, with GABA-immunoreactive synapses apparently representing the GABA-mediated input of the PPn-I, an inhibitory subdivision of the PPn, and glutamate-immunoreactive synapses representing the input of the PPn-G, an excitatory subdivision of the PPn. Only glutamate-immunoreactive synapses were found on relay cells.Abbreviations AMPA -Amino-3-hydroxy-5-methylisoxazole-4-propionic acid - CP central posterior nucleus - EOD electric organ discharge - GABA -aminobutyric acid - GAD L-glutamate decarboxylase - HRP horseradish peroxidase - JAR jamming avoidance response - NMDA N-methyl-D-aspartate - PPn (diencephalic) prepacemaker nucleus - SPPn sublemniscal prepacemaker nucleus     

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     

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.     

Ontogeny and evolution of electric organs in gymnotiform fish

In order to further our understanding of the evolution of electric organs in the Neotropical gymnotiform fish, we studied the ontogeny of the electric organs in eight species. In Eigenmannia virescens, Sternopygus macrurus, and Apteronotus leptorhynchus the earliest electrocytes are located between muscle fibres of the hypaxial muscle (Type A electrocytes). We present arguments that these Type A electrocytes represent the plesiomorphic condition. In S. macrurus, in addition to the electrocytes in the hypaxial muscle, additional electrocytes were found in the epaxial muscle. In A. leptorhynchus a neurogenic organ develops later during ontogeny in the medial part of the hypaxial muscle in addition to the early myogenic organ. In E. virescens the early electrocytes in hypaxial muscle will degenerate later during ontogeny, and this organ will be replaced functionally by electrocytes located in the caudal appendage and below the hypaxial muscle. In Electrophorus electricus, two Gymnotus species, Rhamphichthys sp., and Brachyhypopomus pinnicaudatus the first electrocytes were found below the hypaxial muscle (Type B electrocytes); they are assumed to be the more derived stage. In R. sp., and B. pinnicaudatus the electrocytes of Type B developed directly into the adult organ. In the two Gymnotus ssp. electrocytes were also found in the medial part of the organ in-between muscle fibres of the hypaxial muscle. In E. electricus a germinative zone was observed to separate from the ventral myotome. This zone is generating electrocytes continuously so that, as a consequence, the relative proportion of electric organ to muscle increases greatly. In 45 mm long E. electricus a separation of low voltage orientation pulses and high voltage trains of pulses (shocks) was observed. A first appearance of Hunter’s organ was found in 140 mm specimens of E. electricus. The first discharges of all species studied were head- positive, with the exception of R. sp., which produced a triphasic discharge, its main component, however, being head-positive. The arguments presented indicate that the Type A electrocytes found in E. virescens, S. macrurus, and A. leptorhynchus would represent the plesiomorphic condition. On the basis of the evidence regarding the formation, cytological appearance, and anatomical location, as well as the early electrical recordings, we would hypothesise that during the evolution of gymnotiforms wave type species evolved first, and in a second step pulse type species followed. This view, however, is corroborated by only some phylogenetic hypotheses.     

Simulations of a phase comparing neuron of the electric fish Eigenmannia

1. Investigations of the jamming avoidance response in the weakly electric fish Eigenmannia have shown that the 'small cell', an identified cell type in lamina 6 of the torus semicircularis, can distinguish a brief time difference between the phase of externally applied sinusoidally varying electrical fields. Computer simulations were performed to determine what physiological and anatomical features of the small cell could permit this. 2. The small cell shows apparent inhibition despite having no identified inhibitory synaptic input. This effect was produced in the model using voltage-sensitive membrane channels. These permit an initial sub-threshold excitatory post-synaptic potential (EPSP) to increase the threshold to firing, preventing a subsequent EPSP from firing the cell. 3. Noise and conduction failure appeared to improve the range of cell responsivity. The addition of noise permitted a gradual change in cell firing with change in time disparity, allowing the cell to signal more subtle changes in disparity at the expense of decreased selectivity for a specific absolute time disparity. 4. The cell's multiple dendrites permit a 47% reduction in jitter for incoming signals. Other aspects of dendrite organization did not appear to contribute to the cell's precision.     

Inputs to the torus semicircularis in the electric fish Eigenmannia virescens

Summary The posterior lateral-line lobe, contrary to present belief, projects bilaterally to the torus semicircularis, although the contralateral projection is considerably more extensive. The torus also receives bilateral inputs from the medial octavo-lateralis nuclear complex, the reticular formation, a sublemniscal nucleus, and the nucleus prae-eminentialis. Unilateral inputs to the torus were found originating from the ipsilateral mesencephalic tectum and the contralateral lobus caudalis of the cerebellum. Extensive commissural systems between the right and left torus are also described for the first time.     

Capacitance detection in the wave-type electric fish Eigenmannia during active electrolocation

Weakly electric fish can detect nearby objects and analyse their electric properties during active electrolocation. Four individuals of the South American gymnotiform fish Eigenmannia sp., which emits a continuous wave-type electric signal, were tested for their ability to detect capacitive properties of objects and discriminate them from resistive properties. For individual fish, capacitive values of objects had to be greater than 0.22–1.7 nF (`lower threshold') and smaller than 120–680 nF (`upper threshold') in order to be detected. The capacitive values of natural objects fall well within this detection range. All fish trained could discriminate unequivocally between capacitive and resistive object properties. Thus, fish perceive capacitive properties as a separate object quality. The effects of different types of objects on the locally occurring electric signals which stimulate electroreceptors during electrolocation were examined. Purely resistive objects altered mainly local electric organ discharge (EOD) amplitude, but capacitive objects with values between about 0.5 and 600 nF changed the timing of certain EOD parameters (phase-shift) and EOD waveform. A mechanism for capacitance detection in wave-type electric fish based on time measurements is proposed and compared with the capacitance detection mechanism in mormyrid pulse-type fish, which is based on waveform measurements. Accepted: 31 July 1997     

Mauthner cell-evoked synaptic actions on pacemaker medullary neurons of a weakly electric fish

The present study was designed to examine the synaptic events in neurons of the pacemaker nucleus of Gymnotus carapo during the increase in rate of the electric organ discharge following activation of Mauthner cells. Pacemaker and relay cells were investigated using intracellular recordings which were performed under two different conditions: (1) with the pacemaker nucleus spontaneously discharging and (2) after its activity was abolished by anesthesia. Mauthner axon activation induced an increase in the rate of pacemaker cell discharges. This response was accompanied by an increase in the slope of the pacemaker potential (up to 110%) and a depolarization of these cells. The discharges of relay cells followed one to one those of pacemaker cells. In contrast to that observed in pacemaker cells, only brief depolarizing antidromic effects could be evoked in relay cells after Mauthner axon activation. In quiescent pacemaker cells, Mauthner cell activation induced a prolonged (up to 500 ms) depolarizing potential with an average amplitude of 1.92 ± 0.82 mV; its latency was 4.43 ± 1.14 ms. Our data indicate that, within the pacemaker nucleus, the population of pacemaker cells is the only target for Mauthner cell-evoked, short-latency excitatory synaptic actions. Accepted: 1 March 1997     

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

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

From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish,Eigenmannia

Summary During their jamming avoidance response (JAR), weakly electric fish of the genusEigenmannia shift their electric organ discharge (EOD) frequency away from a similar EOD frequency of a neighboring fish. The behavioral rules and neural substrates for stimulus recognition and motor control of the JAR have been extensively studied (see review by Heiligenberg 1986). The diencephalic nucleus electrosensorius (nE) links sensory processing within the torus semicircularis and optic tectum with the mesencephalic prepacemaker nucleus which, in turn, modulates the medullary pacemaker nucleus and hence the EOD frequency. Two separate areas within the nE responsible for JAR-related EOD frequency rises and frequency falls, respectively, were identified by iontophoresis of the excitatory amino acid L-glutamate. Bilateral lesion of the areas causing EOD frequency rises resulted in elimination of JAR-related frequency rises above a baseline frequency obtained in the absence of a jamming stimulus. Similarly, bilateral lesion of the areas causing frequency falls resulted in a loss of JAR-related frequency falls below the baseline frequency. Whether these areas are also responsible for non-JAR-related frequency shifts is not known. The strength of response and spatial extent of the areas causing frequency shifts varied among fish and also varied in individual fish, reflecting the strength of JAR-related frequency shifts and the balance of activities in frequency-rise and frequency-fall areas. Local application of bicuculline-methiodide or GABA demonstrated a tonic inhibitory input to each area and suggests a reciprocal inhibitory interaction between the two ipsilateral areas, possibly accounting for much of the individual plasticity.The nE thus is a site for neuronal transformation from distributed, topographically organized processing within the laminated structures of the torus and tectum to discrete cell clusters which control antagonistic motor responses.Abbreviations EOD electric organ discharge - JAR jamming avoidance response - Df difference frequency between jamming signal and the fish's own EOD - nE nucleus electrosensorius - PPn prepacemaker nucleus     

Time disparity sensitive behavior and its neural substrates of a pulse-type gymnotiform electric fish, Brachyhypopomus gauderio

Roles of the time coding electrosensory system in the novelty responses of a pulse-type gymnotiform electric fish, Brachyhypopomus, were examined behaviorally, physiologically, and anatomically. Brachyhypopomus responded with the novelty responses to small changes (100 μs) in time difference between electrosensory stimulus pulses applied to different parts of the body, as long as these pulses were given within a time period of ~500 μs. Physiological recording revealed neurons in the hindbrain and midbrain that fire action potentials time-locked to stimulus pulses with short latency (500–900 μs). These time-locked neurons, along with other types of neurons, were labeled with intracellular and extracellular marker injection techniques. Light and electron microscopy of the labeled materials revealed neural connectivity within the time coding system. Two types of time-locked neurons, the pear-shaped cells and the large cells converge onto the small cells in a hypertrophied structure, the mesencephalic magnocellular nucleus. The small cells receive a calyx synapse from a large cell at their somata and an input from a pear-shaped cell at the tip of their dendrites via synaptic islands. The small cells project to the torus semicircularis. We hypothesized that the time-locked neural signals conveyed by the pear-shaped cells and the large cells are decoded by the small cells for detection of time shifts occurring across body areas.