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     

A role of burst firings in encoding of spatiotemporally-varying stimulus

To investigate a role of burst firings of neurons in encoding of spatiotemporally-varying stimulus, we focus on electrosensory system of a weakly electric fish. Weakly electric fish generates electric field around its body using electric organ discharge and can accurately detect the location of an object using the modulation of electric field induced by the object. We developed a model of fish body by which we numerically describe the spatiotemporal patterns of electric field around the fish body. We also made neural models of electroreceptor distributed on the fish body and of electrosensory lateral-line lobe (ELL) to investigate what kinds of information of electric field distorted by an object they detect. Here we show that the spatiotemporal features of electric field around the fish body are encoded by the timing of burst firings of ELL neurons. The information of object distance is extracted by the area of synchronous firings of neurons in a higher nucleus, torus semicircularis.     

Distribution of Kv1-like potassium channels in the electromotor and electrosensory systems of the weakly electric fish Apteronotus leptorhynchus

The electromotor and electrosensory systems of the weakly electric fish Apteronotus leptorhynchus are model systems for studying mechanisms of high-frequency motor pattern generation and sensory processing. Voltage-dependent ionic currents, including low-threshold potassium currents, influence excitability of neurons in these circuits and thereby regulate motor output and sensory filtering. Although Kv1-like potassium channels are likely to carry low-threshold potassium currents in electromotor and electrosensory neurons, the distribution of Kv1 alpha subunits in A. leptorhynchus is unknown. In this study, we used immunohistochemistry with six different antibodies raised against specific mammalian Kv1 alpha subunits (Kv1.1-Kv1.6) to characterize the distribution of Kv1-like channels in electromotor and electrosensory structures. Each Kv1 antibody labeled a distinct subset of neurons, fibers, and/or dendrites in electromotor and electrosensory nuclei. Kv1-like immunoreactivity in the electrosensory lateral line lobe (ELL) and pacemaker nucleus are particularly relevant in light of previous studies suggesting that potassium currents carried by Kv1 channels regulate neuronal excitability in these regions. Immunoreactivity of pyramidal cells in the ELL with several Kv1 antibodies is consistent with Kv1 channels carrying low-threshold outward currents that regulate spike waveform in these cells (Fernandez et al., J Neurosci 2005;25:363-371). Similarly, Kv1-like immunoreactivity in the pacemaker nucleus is consistent with a role of Kv1 channels in spontaneous high-frequency firing in pacemaker neurons. Robust Kv1-like immunoreactivity in several other structures, including the dorsal torus semicircularis, tuberous electroreceptors, and the electric organ, indicates that Kv1 channels are broadly expressed and are likely to contribute significantly to generating the electric organ discharge and processing electrosensory inputs.     

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     

Pyramidal-cell plasticity in weakly electric fish: a mechanism for attenuating responses to reafferent electrosensory inputs

Recordings within the posterior eminentia granularis of the weakly electric fish, Apteronotus leptorhynchus, revealed multiple types of proprioceptive units responsive to changes in the position of the animal's trunk and tail. Intracellular labelling showed that the proprioceptor recordings were made from axons that ramify extensively within the EGp. The location of the somata giving rise to these axons is presently unknown. Electroreceptor afferent responses to electric organ discharge amplitude modulations caused by movement of the animal's tail were compared to responses caused by electronically generated AMs of similar amplitude and time course. These did not differ. Electrosensory lateral line lobe pyramidal cells responded significantly less to electric organ discharge amplitude modulations caused by changing the animal's posture as compared to electronically produced AMs, suggesting that central mechanisms attenuate pyramidal cell responses to reafferent electrosensory inputs. Experiments in which the pattern of reafferent input associated with changes in posture was altered revealed that the pyramidal cells learn, over a time course of several minutes, to reject new patterns of input. Both proprioceptive input and descending electrosensory input to the posterior eminentia granularis are involved in generating the observed plastic changes in pyramidal cell responsiveness.Abbreviations AM amplitude modulation - EGp posterior eminentia granularis - ELL electrosensory lateral line lobe - EOD electric organ discharge - HRP horseradish peroxidase - LTD long-term depression - LTP long-term potentiation     

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.     

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.     

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     

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     

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.     

Diversity of sexual dimorphism in electrocommunication signals and its androgen regulation in a genus of electric fish, Apteronotus

Gymnotiform electric fish emit an electric organ discharge that, in several species, is sexually dimorphic and functions in gender recognition. In addition, some species produce frequency modulations of the electric organ discharge, known as chirps, that are displayed during aggression and courtship. We report that two congeneric species (Apteronotus leptorhynchus and A. albifrons) differ in the expression of sexual dimorphism in these signals. In A. leptorhynchus, males chirp more than females, but in A. albifrons chirping is monomorphic. The gonadosomatic index and plasma levels of 11-ketotestosterone were equivalent in both species, suggesting that they were in similar reproductive condition. Corresponding to this difference in dimorphism, A. leptorhynchus increases chirping in response to androgens, but chirping in A. albifrons is insensitive to implants of testosterone, dihydrotestosterone or 11-ketotestosterone. Species also differ in the sexual dimorphism and androgen sensitivity of electric organ discharge frequency. In A. leptorhynchus, males discharge at higher frequencies than females, and androgens increase electric organ discharge frequency. In A.␣albifrons, males discharge at lower frequencies than females, and androgens decrease electric organ discharge frequency. Thus, in both chirping and electric organ discharge frequency, evolutionary changes in the presence or direction of sexual dimorphism have been accompanied and perhaps caused by changes in the androgen regulation of the electric organ discharge. Accepted: 18 February 1998     

Orientation in the dark: brain circuits involved in the perception of electric signals in mormyrid electric fish.

Weakly electric fish produce electric signals with a specialised organ in their tail. In addition, they are electrosensitive and can perceive their self-generated signals (for electrolocation) and electric signals of other electric fishes (for electrocommunication). Mormyrids possess three types of peripheral electroreceptor organs, one used for electrocommunication and two types involved in electolocation. They are innervated by afferent fibres, which project to different zones in the electrosensory lateral line lobe (ELL) in the medulla. Brain circuits for electrolocation and electrocommunication are separated almost throughout the whole brain. Electrolocation pathways run from the ELL-cortex to the torus semicircularis of the midbrain and then via the valvula cerebelli towards the telencephalon. Pathways involved in electrocommunication run from the nucleus of the ELL to another part of the torus and from there through the isthmic granule nucleus to the valvula. In addition, a pathway via the preglomerular complex to the telencephalon might exist. In both the electrolocation and the electrocommunication circuits, prominent recurrent pathways are present.     

Commissural neurons of the electrosensory lateral line lobe of Apteronotus leptorhynchus: morphological and physiological characteristics

Extracellular injections of horseradish peroxidase were used to label commissural cells connecting the electrosensory lateral line lobes of the weakly electric fish Apteronotus leptorhynchus. Multiple commissural pathways exist; a caudal commissure is made up of ovoid cell axons, and polymorphic cells' axons project via a rostral commissure. Intracellular recording and labeling showed that ovoid cells discharge spontaneously at high rates, fire at preferred phases to the electric organ discharge, and respond to increased receptor afferent input with short latency partially adapting excitation. Ovoid cell axons ramify extensively in the rostro-caudal direction but are otherwise restricted to a single ELL subdivision. Polymorphic cells are also spontaneously active, but their firing is unrelated to the electric organ discharge waveform. They respond to increased receptor afferent activity with reduced firing frequency and response latency is long. Electrical stimulation of the commissural axons alters the behavior of pyramidal cells in the contralateral ELL. Basilar pyramidal cells are hyperpolarized and nonbasilar pyramidal cells are depolarized by this type of stimulation. The physiological results indicate that the ovoid cells participate in common mode rejection mechanisms and also suggest that the ELLs may function in a differential mode in which spatially restricted electrosensory stimuli can evoke heightened responses.Abbreviations ccELL caudal commissure of the ELL - CE contralaterally excited - DML dorsal molecular layer - ELL electrosensory lateral line lobe - EOD electric organ discharge - HRP horseradish peroxidase - IE ipsilaterally excited - MTI mouth-tail inverted - MTN mouth-tail normal - rcELL rostral commissure of the ELL - TRI transverse inverted - TRN transverse normal     

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     

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

Sensory neurons encode natural stimuli by changes in firing rate or by generating specific firing patterns, such as bursts. Many neural computations rely on the fact that neurons can be tuned to specific stimulus frequencies. It is thus important to understand the mechanisms underlying frequency tuning. In the electrosensory system of the weakly electric fish, Apteronotus leptorhynchus, the primary processing of behaviourally relevant sensory signals occurs in pyramidal neurons of the electrosensory lateral line lobe (ELL). These cells encode low frequency prey stimuli with bursts of spikes and high frequency communication signals with single spikes. We describe here how bursting in pyramidal neurons can be regulated by intrinsic conductances in a cell subtype specific fashion across the sensory maps found within the ELL, thereby regulating their frequency tuning. Further, the neuromodulatory regulation of such conductances within individual cells and the consequences to frequency tuning are highlighted. Such alterations in the tuning of the pyramidal neurons may allow weakly electric fish to preferentially select for certain stimuli under various behaviourally relevant circumstances.     

An internal current source yields immunity of electrosensory information processing to unusually strong jamming in electric fish

Summary The electric organ of a fish represents an internal current source, and the largely isopotential nature of the body interior warrants that the current associated with the fish's electric organ discharges (EODs) recruits all electroreceptors on the fish's body surface evenly. Currents associated with the EODs of a neighbor, however, will not penetrate all portions of the fish's body surface equally and will barely affect regions where the neighbor's current flows tangentially to the skin surface. The computational mechanisms of the jamming avoidance response (JAR) in Eigenmannia exploit the uneven effects of a neighbor's EOD current to calculate the correct frequency difference between the two interfering EOD signals even if the amplitude of a neighbor's signal surpasses that of the fish's own signal by orders of magnitude. The particular geometry of the fish's own EOD current thus yields some immunity against the potentially confusing effects of unusually strong interfering EOD currents of neighbors.Abbreviations DF frequency difference - ELL electrosensory lateral line lobe - EOD electric organ discharge - JAR jamming avoidance response     

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

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

Immunohistochemical identification of substance P in cutaneous sensory organs (electroreceptors) of gymnotid teleost fish

Summary The distribution of the neuropeptide substance P, which is considered to be a neurotransmitter or neuromodulator of the central nervous system, has been studied in the cutaneous electroreceptor organs (tuberous and ampullary organs) of 3 species of gymnotid fish: Apteronotus leptorhynchus, Eigenmannia virescens and Sternopygus sp. Immunohistochemical data have revealed that substance P is never present in the afferent fibers but is specifically localized in the electroreceptors of the three species examined. Substane P immunoreactivity is strictly localized in the sensory cells of the ampullary organs of all three species and in those of the tuberous organs of Apteronotus leptorhynchus and Sternopygus sp. In contrast, weak substance P immunoreactivity was observed only in certain tuberous sensory cells of Eigenmannia. Substance P immunoreactivity was also found in the accessory cells of certain organs: it was detected in the two types of accessory cells of the tuberous organs of Eigemmannia virescens, in the accessory cells type 2 of the tuberous organs of Sternopygus sp., and in all accessory cells of ampullary organs of Sternopygus sp. and Apteronotus leptorhynchus. In Sternopygus sp., positive staining was only evident if the substance P antibody was used at low concentration. Immunoreactivity for substance P in the sensory cells suggests that it has a transmitter or modulator function in these electroreceptors; the presence of substance P in the accessory cells remains to be explained.     

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)     

Immunohistochemical demonstration of calbindin-D 28K (CABP28K) in the spinal cord motoneurons of teleost fish

Summary The distribution and localization of the calciumbinding protein, calbindin-D 28K (CaBP28K), in the spinal cord motoneurons of larvae of the teleost fish, Apteronotus leptorhynchus (Gymnotidae) and Pollimyrus isidori (Mormyridae), and in the adult goldfish, Carassius auratus (Cyprinidae), were determined by means of immunohistochemistry. Sections of whole larvae and goldfish spinal cord were reacted with a polyclonal antibody to rat renal CaBP28K. CaBP28K was located by the PAP technique (Sternberger). It was found in the soma, dendrites, axons and axon terminals of spinal motoneurons but not in those of electromotoneurons of Apteronotus leptorhynchus, whereas it occurred in both motoneurons and electromotoneurons of the larval electric organ of Pollimyrus isidori. In these species CaBP28K was also present in the electromotoneuron axon terminals that make synaptic contacts with the pedicles of the electrocytes. In adult Carassius auratus, CaBP28K was found in the soma, dendrites and axons of certain spinal motoneurons. The results indicate that, in teleosts, the motoneurons containing CaBP28K may represent a well-defined population within the spinal cord; the role of this protein in these cells remains to be determined.