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     

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     

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     

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     

Stimulus discrimination in the diencephalon ofEigenmannia: the emergence and sharpening of a sensory filter

Summary Neuronal reliability and sensitivity to behaviorally relevant stimulus patterns were investigated in a higher-order nucleus of the diencephalon believed to participate in the jamming avoidance response (JAR) of the weakly electric fish,Eigenmannia. The fish raises or lowers its frequency of electric organ discharge (EOD) to minimize interference from a neighboring fish's EOD. Proper JARs require determination of the sign of the difference frequency (Df) between the neighboring fish's EOD and the fish's own EOD. Bastian and Yuthas (1984) recently described diencephalic neurons within the nucleus electrosensorius that are able to make this determination. In the present study, response properties of such neurons were compared with those of lower-level sign-selective cells found in the torus semicircularis and the optic tectum (Heiligenberg and Rose 1985) as well as with properties of the intact behavior.Most sign-selective cells within the nucleus electrosensorius show a high degree of selectivity for one sign of the difference frequency; cells with either sign preference were found in approximately equal numbers. The sign preference and the degree of sign selectivity is most often independent of the spatial orientation of the jamming stimulus. In contrast, the responses of toral and tectal cells are less robust and consistent and are often highly dependent on the geometry of the jamming stimulus.Determination of the sign of the difference frequency requires the analysis of amplitude modulations coupled with modulations in phase (timing) differences between pairs of areas of the body surface. The most sensitive cells recorded in the nucleus electrosensorius can determine the sign of the difference frequency with timing differences of 1 s or less, roughly comparable to the behavioral threshold of 400 ns (Carr et al. 1986). The best toral/tectal response required at least a 16 s modulation.Cells within the nucleus electrosensorius thus code the sign of Df with a high degree of reliability and sensitivity. Ambiguities persist, however, which suggest that single cells at this level cannot completely account for the behavioral discrimination. Additional processing may be necessary to transform a still primarily sensory code into a motor program for control of the JAR (Rose et al. 1988).Abbreviations EOD electric organ discharge - JAR jammning avoidance response - Df difference frequency between jamming signal and fish's own EOD - S ₁ sinusoidal EOD mimic of subject fish - S ₂ sinusoidal EOD mimic of neighbor     

A new electroreceptive teleost:Xenomystus nigri (Osteoglossiformes: Notopteridae)

Summary The African knife fish,Xenomystus nigri, is found to be sensitive to weak electric fields by the method of averaged evoked potentials from the brain. Slow waves and spikes were recorded in or near the lateral line area of the medulla and the torus semicircularis of the mesencephalon in response to long pulses (best > 50 ms) and low frequency sine waves (best ca. 10 Hz) of voltage gradients down to < 10 V/cm. Evoked waves in the lateral line area are a sequence of negative and positive deflections beginning with a first peak at ca. 24 ms; in the torus semicircularis the first peak is at ca. 37 ms. Spikes are most likely in the torus between 50 and 80 ms after ON. At each recording locus there is a best axis of the homogeneous electric field and a better polarity. Effects of stimulus intensity, duration and repetition are described. The physiological properties are similar to those of ampullary receptor systems in mormyriforms, gymnotiforms and siluriforms.Confirming Braford (1982),Xenomystus has a large medullary nucleus resembling the nucleus otherwise peculiar to mormyriforms, gymnotiforms and siluriforms and now called the electrosensory lateral line lobe (ELLL; formerly the posterior lateral line lobe). We describe the projections of anterior and posterior lateral line nerves by HRP applied to the proximal stump of a cut nerve. A descending central ramus of the anterior lateral line nerve and a lateral component of the ascending ramus of the posterior lateral line nerve end in part in the ELLL.Electroreception, including the system of discrete central structures mediating it, is for the first time found to be less than an ordinal or even a family character, but apparently a characteristic of the subfamily Xenomystinae. Species of the other subfamily, Notopterinae as well as of the other families of osteoglossiforms (Osteoglossidae, Hiodontidae and Pantodontidae), lack the ELLL.Notopterus andPantodon are found to lack the evoked potential.The positive finding of evoked activity to feeble electric field is found to be the most practical method for searching widely among fishes for the presence of the electrosense modality and its central pathways. The anatomical criterion of an ELLL can now be taken to be a good criterion for the presence of this sensory system. The absence of evoked response correlates well with the absence of an ELLL.Abbreviations ELLL electrosensory lateral line lobe - HRP horseradish peroxidase - TS torus semicircularis     

Androgen binding in the brain and electric organ of a mormyrid fish

Summary The mormyrid fish of Africa produce a weak electric pulse called an Electric Organ Discharge (EOD) that functions in electrical guidance and communication. TheEOD waveform describes the appearance of a single pulse which is produced by the electric organ's excitable cells, the electrocytes. For some species, there is a sex difference in the appearance and duration of the EOD waveform, which is under the control of gonadal steroid hormones. We now show, using biochemical techniques, that the steroid-sensitivity of the myogenic electric organ correlates with the presence of comparatively high levels of androgen-binding activity in the cytosol of electrocytes.TheEOD rhythm describes the rate at which the electric organ fires and is under the control of a central electromotor pathway. Sex differences have also been described for the EOD rhythm. Using steroid autoradiographic techniques, we found uptake of tritium-labelled dihydrotestosterone (³H-DHT) by cells within the reticular formation that lie adjacent to the medullary relay nucleus which innervates the spinal electromotoneurons that excite the electric organ. However, no DHT-binding was observed in the relay or electromotor nuclei.Steroid-concentrating cells were also found in several other brainstem regions, the hypothalamus, and the thalamus. In particular, a group of DHT-concentrating, motoneuron-like cells were observed in the caudal medulla and were identified as aswimbladder orsonic motor nucleus.The biochemical data suggest that the electric organ has evolved a sensitivity to gonadal steroid hormones that may underlie the development of known sex differences in the EOD waveform. The autoradiographic results suggest that if steroids do affect the development of sex differences in the EOD rhythm, it is at some level removed from known spinal and medullary electromotor nuclei.Abbreviations ac anterior commissure - AD area dorsalis telencephali - AV area ventralis telencephali - CBL cerebellum - DT dorsal thalamus - E electromotoneuron - En entopeduncular nucleus,ef lateral line efferent nucleus - EG eminentia granularis - ELLL electroreceptive lateral line lobe,EO electric organ,FV folded part of valvula of cerebellum - H hypothalamus - M mesencephalon - MO medulla oblongota - OB olfactory bulb - OT optic tectum - PO preoptic area - R medullary relay nucleus - rf reticular formation - SC spinal cord - SMN sonic motor nucleus - T telencephalon - TP posterior tuber of diencephalon - TS torus semicircularis - UV unfolded part of valvula of cerebellum,v ventricle - VT ventral thalamus     

Differential distribution of ampullary and tuberous processing in the torus semicircularis of Eigenmannia

Summary Gymnotiform electric fish sense low-and high frequency electric signals with ampullary and tuberous electroreceptors, respectively. We employed intracellular recording and labeling methods to investigate ampullary and tuberous information processing in laminae 1–5 of the dorsal torus semicircularis of Eigenmannia. Ampullary afferents arborized extensively in laminae 1–3 and, in some cases, lamina 7. Unlike tuberous afferents to the torus, ampullary afferents had numerous varicosities along their finest-diameter branches. Neurons that were primarily ampullary were found in lamina 3. Neurons primarily excited by tuberous stimuli were found in lamina 5 and, more rarely, in lamina 4. Cells that had dendrites in lamina 1–3 and 5 could be recruited by both ampullary and tuberous stimuli. These bimodal cells were found in lamina 4. During courtship, Eigenmannia produces interruptions of its electric organ discharges. These interruptions stimulate ampullary and tuberous receptors. The integration of ampullary and tuberous information may be important in the processing of these communication signals.Abbreviations JAR jamming avoidance response - EOD electric organ discharge - S1 sinusoidal signal mimicking fish's EOD - S2 jamming signal - Df frequency difference (S2-S1) or between a neighbor's EODs and fish's own EODs - CNS central nervous system     

Comparison of calbindin D 28K and cytochrome c oxidase in electrosensory nuclei of high- and low-frequency weakly electric fish (Gymnotiformes)

Summary Weakly electric fish (Gymnotiformes) emit quasi-sinusoidal electric organ discharges within speciesspecific frequency ranges. The electrosensory system is organized into 2 parallel pathways which convey either the amplitude or the timing of each electric organ discharge cycle. Two putative metabolic activity markers, calbindin D 28K and cytochrome c oxidase, and their relationship with the electrosensory nuclei of high- and low-frequency species were studied. Calbindin is found in the somata of the spherical neurons in the first-order electrosensory recipient nucleus, the electrosensory lateral-line lobe, and in layer VI of the midbrain's torus semicircularis, in Eigenmannia virescens, an intermediate-frequency species, and Apteronotus leptorhynchus, a high-frequency species. Calbindin immunoreactivity was completely absent in these nuclei in Sternopygus macrurus, a closely related, low-frequency species. Cytochrome c oxidase levels were inversely related to calbindin immunoreactivity since relatively high levels were observed in the electrosensory lateral-line lobe and torus semicircularis of S. macrurus but were absent in these nuclei in A. leptorhynchus. Our studies indicate that calbindin immunoreactivity is present in tonic, repetitively firing neurons with high frequencies.     

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.     

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     

Neural simulations of adaptive reafference suppression in the elasmobranch electrosensory system

The electrosensory system of elasmobranchs is extremely sensitive to weak electric fields, with behavioral thresholds having been reported at voltage gradients as low as 5 nV/cm. To achieve this amazing sensitivity, the electrosensory system must extract weak extrinsic signals from a relatively large reafferent background signal associated with the animal's own movements. Ventilatory movements, in particular, strongly modulate the firing rates of primary electrosensory afferent nerve fibers, but this modulation is greatly suppressed in the medullary electrosensory processing nucleus, the dorsal octavolateral nucleus. Experimental evidence suggests that the neural basis of reafference suppression involves a common-mode rejection mechanism supplemented by an adaptive filter that fine tunes the cancellation. We present a neural model and computer simulation results that support the hypothesis that the adaptive component may involve an anti-Hebbian form of synaptic plasticity at molecular layer synapses onto ascending efferent neurons, the principal output neurons of the nucleus. Parallel fibers in the molecular layer carry a wealth of proprioceptive, efference copy, and sensory signals related to the animal's own movements. The proposed adaptive mechanism acts by canceling out components of the electrosensory input signal that are consistently correlated with these internal reference signals.Abbreviations AEN ascending efferent neuron - AFF primary afferent nerve fiber - DGR dorsal granular ridge - DON dorsal octavolateral nucleus - ELL electrosensory lateral line lobe - GABA -aminobutyric acid - IN inhibitory interneuron - ISI interspike interval - ST stellate cell     

Two modes of information processing in the electrosensory system of the paddlefish (Polyodon spathula)

Paddlefish are uniquely adapted for the detection of their prey, small water fleas, by primarily using their passive electrosensory system. In a recent anatomical study, we found two populations of secondary neurons in the electrosensory hind brain area (dorsal octavolateral nucleus, DON). Cells in the anterior DON project to the contralateral tectum, whereas cells in the posterior DON project bilaterally to the torus semicircularis and lateral mesencephalic nucleus. In this study, we investigated the properties of both populations and found that they form two physiologically different populations. Cells in the posterior DON are about one order of magnitude more sensitive and respond better to stimuli with lower frequency content than anterior cells. The posterior cells are, therefore, better suited to detect distant prey represented by low-amplitude signals at the receptors, along with a lower frequency spectrum, whereas cells in the anterior DON may only be able to sense nearby prey. This suggests the existence of two distinct channels for electrosensory information processing: one for proximal signals via the anterior DON and one for distant stimuli via the posterior DON with the sensory input fed into the appropriate ascending channels based on the relative sensitivity of both cell populations.     

Electric organ corollary discharge pathways in mormyrid fish

Corollary discharge signals associated with the motor command that elicits the electric organ discharge are prominent in the electrosensory lobe of mormyrid fish (Gnathonemus petersii). Central pathways and structures that convey these signals from the motor command nucleus to the electrosensory lobe are known anatomically, but these structures and their contributions to the various corollary discharge phenomena have not been examined physiologically. This study examines one such structure, the mesencephalic command associated nucleus (MCA).Recordings from MCA cells show a highly stereotyped two spike response. The first spike of the response has a latency of about 2.5 ms following the initiation of the electric organ discharge (EOD) motor command which is about 5.5 ms before the occurrence of the EOD.Results from stimulation and lesion experiments indicate that MCA is responsible for: 1) the gate-like corollary discharge-driven inhibition of the knollenorgan pathway; 2) the gate-like corollary discharge-driven excitation of granule cells in the mormyromast regions of the electrosensory lobe; and 3) various excitatory effects on other cells in the mormyromast regions.Some corollary discharge phenomena are still present after MCA lesions, including the earliest corollary discharge effects and the plasticity that follows pairing with electrosensory stimuli. These phenomena must be mediated by structures other than MCA.Abbreviations BCA bulbar command associated nucleus - C EOD motor command - C3 central cerebellar lobule 3 - COM EOD motor command nucleus - DLZ dorsolateral zone of ELL cortex - EGa eminentia granularis anterior - EGp eminentia granularis posterior - ELa nucleus exterolateralis anterior - ELL electrosensory lobe - ELLml molecular layer of ELL cortex - EOD electric organ discharge - gang ganglion layer - gran granule layer - jlem juxtalemniscal region - JLl lateral juxtalobar nucleus - JLm medial juxtalobar nucleus - lat nucleus lateralis - ll lateral lemniscus - MCA mesencephalic command associated nucleus - mol molecular layer - MOml molecular layer of the medial octavolateral nucleus - MRN medullary relay nucleus - MZ medial zone of ELL cortex - nALL anterior lateral line nerve - NELL nucleus of the electrosensory lobe - nX cranial nerve X (vagus) - OT optic tectum - PCA paratrigeminal command associated nucleus - pee praeeminentialis electrosensory tract - plex plexiform layer - prae nucleus praeeminentialis - sublem sublemniscal nucleus - TEL telencephalon - VLZ ventrolateral zone of ELL cortex - vped valvular peduncle     

Postmetamorphic changes in auditory sensitivity of the bullfrog midbrain

During metamorphosis, the lateral line system of ranid frogs (Rana catesbeiana) degenerates and an auditory system sensitive to airborne sounds develops. We examined the onset of function and developmental changes in the central auditory system by recording multi-unit activity from the principal nucleus of the torus semicircularis (TSp) of bullfrogs at different postmetamorphic stages in response to tympanically-presented auditory stimuli. No responses were recorded to stimuli of up to 95 dB SPL from latemetamorphic tadpoles, but auditory responses were recorded within 24 hours of completion of metamorphosis. Audiograms from froglets (SVL < 5.5 cm) were relatively flat in shape with high thresholds, and showed a decrease in most sensitive frequency (MSF) from about 2500 Hz to about 1500 Hz throughout the first 7–10 days after completion of metamorphosis. Audiograms from frogs larger than 5.5 cm showed continuous downward shifts in MSF and thresholds, and increases in sharpness around MSF until reaching adult-like values. Spontaneous activity in the TSp increased throughout postmetamorphic development. The torus increased in volume by approximately 50% throughout development and displayed changes in cell density and nuclear organization. These observations suggest that the onset of sensitivity to tympanically presented airborne sounds is limited by peripheral, rather than central, auditory maturation.Abbreviations CF characteristic frequency - MSF most sensitive frequency - PB phasic burst - PL primary like - S sustained - SVL snout-vent length - TS torus semicircularis - TSl laminar nucleus of TS - TSm magnocellular nucleus of TS - TSp principal nucleus of TS - TW tympanic width     

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)     

Neural coding of difference frequencies in the midbrain of the electric fishEigenmannia: Reading the sense of rotation in an amplitude-phase plane

Eigenmannia is able to discriminate the sign of the difference, Df, between the frequency of a neighbor's electric organ discharge (EOD) and that of its own EOD. This discrimination can be demonstrated at the level of individual neurons of the midbrain. Intracellular and extracellular recordings of such sign-selective cells revealed the following: Units preferring positive Dfs and units preferring negative Dfs were found with equal frequency. The degree of selectivity was also similar for these two classes of neurons. All sign-selective units were sensitive to the magnitude of the frequency difference, i.e. the beat rate. Most units responded best to beat rates in the 4-8 Hz range. Sign-selectivity was observed only when the jamming signal (S2) was presented through electrodes other than those used to deliver the mimic (S1) of the fish's EOD, i.e. only when amplitude modulations were accompanied by modulations of differential phase. Intracellular studies suggest that most sign-selective neurons of the tectum are large, multipolar cells in the stratum album centrale. These cells send projections to the reticular formation, to lamina 9 of the torus semicircularis and to the N. electrosensorius.     

Electrosensory phase sensitivity in the weakly electric fish Eigenmannia in the detection of signals similar to its own

The electric organ discharge (EOD) of the South American knifefish Eigenmannia sp. is a permanently present wave signal of usually constant amplitude and frequency (similar to a sine wave). A fish perceives discharges of other fish as a modulation of its own. At frequency identity (F = 0 Hz) the phase difference between a fish's own electric discharge and that of another fish affects the superimposed waveform. It was unclear whether or not the electrosensory stimulus-intensity threshold as behaviourally determined depends on the phase difference between a fish's own EOD and a sine-wave stimulus (at F = 0 Hz). Also the strength of the jamming avoidance response (JAR), a discharge frequency shift away from a stimulus that is sufficiently close to the EOD frequency, as a function of phase difference was studied. Sine-wave stimuli were both frequency-clamped and phase-locked to a fish's discharge frequency (F = 0 Hz). In food-rewarded fish, the electrosensory stimulus-intensity threshold depended significantly on the phase difference between a fish's discharge and the stimulus. Stimulus-intensity thresholds were low (down to 3 V/cm, peak-to-peak) when the superimposed complex wave changed such that the shift in zero-crossings times relative to the original EOD was large but amplitude change minimal; stimulus-intensity thresholds were high (up to 16.9 V/cm, peak-to-peak) when the shift in zero-crossings times was small but amplitude change maximal. Similar results were obtained for the non-conditioned JAR: at constant supra-threshold stimulus intensities and F = 0 Hz, the phase difference significantly affected the strength of the JAR, although variability between individuals was higher than that observed in the conditioned experiments.Abbreviations ACP active phase coupling - EOD electric organ discharge - JAR jamming avoidance response - F frequency (fish) — frequency (stimulus) [Hz] - p-p peak-to-peak     

Effects of global electrosensory signals on motion processing in the midbrain of <Emphasis Type="Italic">Eigenmannia</Emphasis>

Wave-type weakly electric fish such as Eigenmannia produce continuous sinusoidal electric fields. When conspecifics are in close proximity, interaction of these electric fields can produce deficits in electrosensory function. We examined a neural correlate of such jamming at the level of the midbrain. Previous results indicate that neurons in the dorsal layers of the torus semicircularis can (1) respond to jamming signals, (2) respond to moving electrosensory stimuli, and (3) receive convergent information from the four sensory maps of the electrosensory lateral line lobe (ELL). In this study we recorded the intracellular responses of both tuberous and ampullary neurons to moving objects. Robust Gaussian-shaped or sinusoidal responses with half-height durations between 55 ms and 581 ms were seen in both modalities. The addition of ongoing global signals with temporal-frequencies of 5 Hz attenuated the responses to the moving object by 5 dB or more. In contrast, the responses to the moving object were not attenuated by the addition of signals with temporal frequencies of 20 Hz or greater. This occurred in both the ampullary and tuberous systems, despite the fact that the ampullary afferents to the torus originate in a single ELL map whereas the tuberous afferents emerge from three maps.     

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.