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At least 19 recordsLinked to original sources

Active electrolocation of objects in weakly electric fish

Weakly electric fish produce electric signals (electric organ discharges, EODs) with a specialised electric organ creating an electric field around their body. Objects within this field alter the EOD-induced current at epidermal electroreceptor organs, which are distributed over almost the entire body surface. The detection, localisation and analysis of objects performed by monitoring self-produced electric signals is called active electrolocation. Electric fish employ active electrolocation to detect objects that are less than 12 cm away and have electric properties that are different from those of the surrounding water. Within this range, the mormyrid Gnathonemus petersii can also perceive the distance of objects. Depth perception is independent of object parameters such as size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters of the electric image that the object projects onto the fish's skin. Electric fish can not only locate objects but can also analyse their electrical properties. Fish are informed about object impedance by measuring local amplitude changes at their receptor organs evoked by an object. In addition, all electric fish studied so far can independently determine the capacitative and resistive components of objects that possess complex impedances. This ability allows the fish to discriminate between living and non-living matter, because capacitance is a property of living organisms. African mormyrids and South American gymnotiforms use different mechanisms for capacitance detection. Mormyrids detect capacitance-evoked EOD waveform distortions, whereas gymnotiforms perform time measurements. Gymnotiforms measure the temporal phase shift of their EODs induced at body parts close to the object relative to unaffected body parts further away.

Journal Article

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.

Animals

Effects of denervation upon receptor cell survival and basal cell proliferation in tuberous electroreceptor organs of a weakly electric fish.

Weakly electric fish generate electric fields for the purposes of electrolocation and communication. These fields are detected by specialized receptor organs: the tuberous organs. In the present study we investigated the effects of denervation upon receptor cell survival and progenitor (basal) cell proliferation rate. The left, infraorbital, anterior lateral line nerve of brown ghosts (Apteronotus leptorhynchus) was sectioned, and the proximal stump was dipped in ricin to prevent regrowth. In groups of four, the animals were given two daily injections of the cell proliferation marker bromodeoxyuridine (BrdU) for 2 days at 1, 2, 3, or 4 weeks following denervation. At the completion of the BrdU injection schedule, a piece of cheek skin, rostroventral to the eye, was removed from the left (denervated) and the right (intact) sides and processed for light microscopy or immunocytochemistry. Our results show: (1) there is progressive receptor cell death and tuberous organ degeneration following denervation; (2) basal cell proliferation increases steadily with time after denervation and tuberous organ degeneration; and (3) despite denervation, some proliferating basal cells differentiate into receptor cells, but these new receptor cells eventually die. These results suggest that innervation is essential for tuberous electroreceptor cell survival and that the rate at which basal cells proliferate is regulated by receptor cell health, locally released factors, or both.

Animals

A quantitative analysis of passive electrolocation behavior in electric fish.

Weakly electric fish of the families Gymnotidae and Hypopomidae (Gymnotiformes) are able to locate the electric discharges from conspecifics or from dipole electrodes, and they demonstrate this by making rapid, well-directed approaches toward these electrical sources. A video tracking system was used to follow the movements of electric fish in a large tank and an analytic method was used for computing the direction and magnitude of the electric field anywhere within the cylindrical test tank. Using a static analysis method, we describe the posture of test fish relative to the electric fields during their approaches to stationary or moving electrical stimuli. Using a dynamic analysis, we examine the movements of the fish including the sign and magnitude of velocity and bending in response to electric fields. Electric fish seek to maintain a zero error angle between their body orientation and the local electric field. They do so by bending their body in the direction of the local electric field. The response has a delay of approximately 0.5 s. Swimming in reverse inverts the direction of the bend. These fish also use 'V-turns' to redirect their swim directions when encountering rapidly-changing electric fields.

Animals

Sensory coding and corollary discharge effects in mormyrid electric fish.

Weakly electric fish use their electrosensory systems for electrocommunication, active electrolocation and low-frequency passive electrolocation. In electric fish of the family Mormyridae, these three purposes are mediated by separate classes of electroreceptors: electrocommunication by Knollenorgan electroreceptors, active electrolocation by Mormyromast electroreceptors and low-frequency passive electrolocation by ampullary electroreceptors. The primary afferent fibres from each class of electroreceptors terminate in a separate central region. Thus, the mormyrid electrosensory system has three anatomically and functionally distinct subsystems. This review describes the sensory coding and initial processing in each of the three subsystems, with an emphasis on the Knollenorgan and Mormyromast subsystems. The Knollenorgan subsystem is specialized for the measurement of temporal information but appears to ignore both intensity and spatial information. In contrast, the Mormyromast subsystem is specialized for the measurement of both intensity and spatial information. The morphological and physiological characteristics of the primary afferents and their central projection regions are quite different for the two subsystems and reflect the type of information which the subsystems preserve. This review also describes the electric organ corollary discharge (EOCD) effects which are present in the central projection regions of each of the three electrosensory subsystems. These EOCD effects are driven by the motor command that drives the electric organ to discharge. The EOCD effects are different in each of the three subsystems and these differences reflect differences in both the pattern and significance of the sensory information that is evoked by the fish's own electric organ discharge. Some of the EOCD effects are invariant, whereas others are plastic and depend on previous afferent input. The mormyrid work is placed within two general contexts: (a) the measurement of time and intensity in sensory systems, and (b) the various roles of motor command (efferent) signals and self-induced sensory (reafferent) signals in sensorimotor systems.

Action Potentials

Neural substrates for species recognition in the time-coding electrosensory pathway of mormyrid electric fish.

Mormyrid electric fish have species- and sex-typical electric organ discharges (EODs). One class of tuberous electroreceptors, the knollenorgans, plays a critical role in electric communication; one function is species recognition of EOD waveforms. In this paper, we describe cell types in the knollenorgan central pathway, which appear responsible for analysis of the temporal patterns of spikes encoded by the knollenorgans in response to EOD stimuli. Secondary sensory neurons in the nucleus of the electrosensory lateral line lobe (NELL) act as relays of peripheral responses. They fire a single phase-locked spike to an outside positive-going voltage step. Axons from the NELL project to the toral nucleus exterolateralis pars anterior (ELa). Immediately after they enter the ELa, they send collaterals to terminate on one to three ELa large cells and then continue in a lengthy neuronal pathway that traverses the ELa several times. After a path length of up to 5 mm, the NELL axon terminates on as many as 70 ELa small cells. Thus the large cells appear to be excited first, followed by the small cells, with the intervening length of the axon serving as a delay line. The large cells also respond with phase-locked spikes to voltage steps. Large cell axons extend for approximately 1 mm and terminate on several small cells within the ELa. The terminals are known to be GABAergic inputs and are presumed inhibitory. We propose that small cells receive direct inhibition from large cells and delayed excitation from NELL axons. The small cells may act as anti-co-incidence detectors to analyze the temporal structure of the EOD waveform.

Afferent Pathways

Different classes of glutamate receptors and GABA mediate distinct modulations of a neuronal oscillator, the medullary pacemaker of a gymnotiform electric fish.

Gymnotiform electric fish generate distinct communicatory signals by modulating the rate of their electric organ discharges (EODs). Each EOD is triggered by a command pulse from the medullary pacemaker nucleus (PN), which contains pacemaker cells and relay cells. The firing rate of this nucleus is modulated by inputs from the diencephalic prepacemaker nucleus (PPN). The NMDA receptor blocker APV and the kainate/quisqualate receptor blocker CNQX, administered to the PN, suppress different types of modulations, indicating that different classes of glutamate receptors mediate the generation of different modulations. A comparison of the 2 genera, Hypopomus and Eigenmannia, reveals that sustained modulations, such as smooth rises in the rate of pacemaker cell firing and the selective silencing of the relay cells (only observed in Hypopomus), are mediated by NMDA receptors, whereas the brief and rapid acceleration, called "chirp" or "decrement burst," is mediated by kainate/quisqualate receptors. Application of the GABA blocker bicuculline reveals that the 2 genera differ in the mechanism by which they slow the firing rate of their pacemaker. Whereas Hypopomus uses GABAergic inhibition to slow down and ultimately silence its pacemaker cells, Eigenmannia reduces tonic, APV-sensitive excitation originating from its PPN and lacks GABAergic inhibition in the PN.

2-Amino-5-phosphonovalerate

Tuberous electroreceptor organs form in denervated regenerating skin of a weakly electric fish.

Weakly electric fish use tuberous electroreceptor organs to detect their own electric fields. We investigated the role of innervation upon regeneration and differentiation of tuberous electroreceptor organs. The left, infraorbital, anterior lateral line nerve of brown ghosts (Apteronotus leptorhynchus) was sectioned, and the proximal stump was dipped in ricin to prevent regrowth. Immediately after denervation, a piece of cheek skin (approximately 0.5 cm2) was removed bilaterally to induce skin regeneration. After survival periods of 3, 4, or 5 weeks, regenerated skin from the left (denervated) and the right (reinnervated) sides was removed and processed for immunocytochemistry or electron microscopy. Tuberous electroreceptor organs were present in regenerated reinnervated, as well as regenerated denervated skin patches at all survival times. With increased time after skin removal, the number of fully differentiated organs increased in the reinnervated regenerated skin while the number of organs with degenerating receptor cells or entirely devoid of receptor cells increased in the denervated regenerated skin. These results suggest that innervation is not essential for tuberous electroreceptor organ development, but that it is necessary for complete sensory cell differentiation and long-term survival.

Animals

Central mechanisms of temporal analysis in the knollenorgan pathway of mormyrid electric fish

Mormyrid electric fish communicate using pulse-type electric organ discharges (EODs). The fine temporal structure of the waveforms of EODs varies widely throughout the 200 or more species of mormyrids. These signals carry information about the species, the sex and even the individual identity of the signaller. Behavioral experiments have shown that some species of fish are capable of using this information. Of the four known types of electroreceptors in mormyrid fish, the knollenorgan electroreceptor is the one most likely to be involved in the detection of conspecific EOD signals. Here, we review some recent advances in understanding how the central knollenorgan pathway might be analyzing the temporal structure of the EOD waveform. Fine temporal analysis appears to take place in the nucleus exterolateralis pars anterior (ELa), where tightly phase-locked inputs from the hindbrain drive a direct, excitatory input through a long axonal delay line and also drive an indirect, inhibitory input with negligible delay through the ELa large cell. These two inputs converge on ELa small cells, where they are hypothesized to interact in a 'delay-line/blanking' model. This initial temporal analysis is further refined in the nucleus exterolateralis pars posterior, where units tuned to ranges of pulse durations have been identified physiologically.

Journal Article

Temporal coding of species recognition signals in an electric fish.

An electric fish in the African family Mormyridae recognizes members of its own species by "listening" to electric organ discharges, which are species-specific signatures. Reactions of fish in the field and of individual electroreceptors to both normal and modified computer-synthesized discharges emphasize the importance of the waveform (time-domain cues) in species recognition.

Animal Communication

Regeneration of electroreceptors in weakly electric fish.

Weakly electric teleost fish possess two classes of electroreceptors: tuberous and ampullary organs. Ampullary organs are used for detecting prey, while tuberous organs detect the fish's own electric organ discharges (EODs) and those of conspecifics. EOD frequency varies among individuals within a species and a fish's tuberous receptors are sharply tuned to its own EOD frequency. In young, small fish both tuberous and ampullary afferents innervate only single organs. As fish grow new receptor cells are added to each organ and it divides into two daughter organs. This process continues resulting in numerous organs in a cluster; the afferent nerve innervates all the organs in a cluster. When a patch of skin is removed new skin grows back complete with new receptor organs of both classes. From our studies we have shown that: (1) new organs are found only in the presence of nerve fibres; (2) their morphological development during regeneration is similar to their normal development; (3) organs divide rapidly giving rise to daughter organs until each afferent fibre innervates the correct number of organs for a fish of its size; (4) receptor cells are broadly tuned below the EOD frequency of a given fish and they gradually increase their tuned frequency and sharpness of tuning until they become correctly tuned to that EOD frequency; (5) the correct matching of receptor tuning to EOD frequency occurs in fish in which the spinal cord has been severed or with lesions of the medullary pacemaker nucleus, thereby eliminating the EOD and any possible 'calibration' signal; and (6) basal and capsule cells of receptor organs in the intact skin around the wound divide after skin damage and are a possible source of precursor cells for new receptor organs.

Animals

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

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.

Animals

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, male 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 electronic 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.

Androgens

In vitro study of phase resetting and phase locking in a time-comparison circuit in the electric fish, Eigenmannia.

The electric fish Eigenmannia generates on oscillating weak electric field. The amplitude and timing information of this electric field is perceived by electroreceptors distributed on its skin. The pathway of timing information, consisting of spherical cells and giant cells, was studied in an in vitro preparation. The giant cells were identified to be endogenous oscillators and thus have the functional advantage of phase locking more easily to a periodic stimulus with a frequency in the range of the intrinsic frequency. Their spontaneous rhythmic activity was perturbed by delivering excitatory single pulses or periodic pulses via their synaptic inputs. The regular and irregular dynamics produced by periodic stimulation were discussed in the context of a mathematical analysis of the response to single pulses. Ambiguous representations of the timing of the stimulus pulse were observed and could be related to this analysis. Some spontaneously firing cells could be silenced with periodic excitatory stimulation in a narrow frequency and amplitude range. Some irregularly firing cells continued to fire periodically for several seconds after phase locking to a periodic stimulus. This study is the first description of an endogenous oscillator in a system devoted to the precise timing of sensory events.

Animals

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)

Animals

Phenotypic conversion of distinct muscle fiber populations to electrocytes in a weakly electric fish.

In most groups of electric fish, the electric organ (EO) derives from striated muscle cells that suppress many muscle phenotypic properties. This phenotypic conversion is recapitulated during regeneration of the tail in the weakly electric fish Sternopygus macrurus. Mature electrocytes, the cells of the electric organ, are considerably larger than the muscle fibers from which they derive, and it is not known whether this is a result of muscle fiber hypertrophy and/or fiber fusion. In this study, electron micrographs revealed fusion of differentiated muscle fibers during the formation of electrocytes. There was no evidence of hypertrophy of muscle fibers during their phenotypic conversion. Furthermore, although fish possess distinct muscle phenotypes, the extent to which each fiber population contributes to the formation of the EO has not been determined. By using myosin ATPase histochemistry and anti-myosin heavy chain (MHC) monoclonal antibodies (mAbs), different fiber types were identified in fascicles of muscle in the adult tail. Mature electrocytes were not stained by the ATPase reaction, nor were they labeled by any of the anti-MHC mAbs. In contrast, mature muscle fibers exhibited four staining patterns. The four fiber types were spatially arranged in distinct compartments with little intermixing; peripherally were two populations of type I fibers with small cross-sectional areas, whereas more centrally were two populations of type II fibers with larger cross-sectional areas. In 2- and 3-week regenerating blastema, three fiber types were clearly discerned. Most (> 95%) early-forming electrocytes had an MHC phenotype similar to that of type II fibers. In contrast, fusion among type I fibers was rare. Together, ultrastructural and immunohistochemical analyses revealed that the fusion of muscle fibers gives rise to electrocytes and that this fusion occurs primarily among the population of type II fibers in regenerating blastema.

Adenosine Triphosphatases

Comparative analysis of the jamming avoidance response in African and South American wave-type electric fishes.

African wave-type electric fish, Gymnarchus, and South American wave-type electric fish, Eigenmannia, have evolved electrosensory and electromotor systems independently. Nevertheless, they exhibit a similar electrical behavior, the jamming avoidance response (JAR). When two individuals with slightly different frequencies of electric organ discharge (EOD) meet, they shift discharge frequencies away from each other to avoid mutual jamming of their electrolocation systems. These two genera of electric fishes perform this behavior using an identical set of complex computational rules. Reflecting their independent evolution, however, neuronal implementation of the computational steps appears to take different forms. One of the essential computational steps, phase comparison, is performed in the hindbrain in Gymnarchus and in the midbrain in Eigenmannia. The comparison of these two species in this paper revealed an example of how different brain structures perform functionally similar tasks in independently evolved systems that have a similar overall behavioral function.

Action Potentials

Effects of 17alpha-methyltestosterone on sexually dimorphic characters in the weakly discharging electric fish, Brienomyrus niger (Günther, 1866) (Mormyridae): electric organ discharge, ventral body wall indentation, and anal-Fin ray bone expansion.

Adult males of African weakly discharging electric fish (family: Mormyridae) are distinguished from juveniles and adult females by a dorsally directed indentation of the posterior ventral body wall and by massive bone expansion of the bases of a select number of anal-fin rays. These sexually dimorphic structures seem to facilitate the anal-fin reflex that is displayed during courtship when the male envelopes its anal fin around the female's to form a common spawning pouch. Expanded bone could provide additional surface for muscle attachment and thus assist in part with the courtship sequence. Based on the fact that the expression of the male sexually dimorphic electric organ discharge (EOD) is under androgen control, and that the female EOD can be masculinized through testosterone administration, we hypothesized that androgens should also drive anal-fin ray bone expansion in male mormyrids and equally effect male-like changes in treated juveniles and adult females. Exogenous androgen treatment (17alpha-methyltestosterone) of adult female Brienomyrus niger resulted in a male-like EOD, and male-typical structural transformations (body wall indentation and anal-fin ray bone expansion). Some of these changes were immediate and receded following hormone withdrawal (EOD), while others developed more slowly and were apparently permanent (indentation and bone formation). 17alpha-Methyltestosterone administration affected only those targets in females that are normally involved in the male's reproductive behavior, i.e., its courtship signal (EOD) and two morphological features (body-wall indentation and bone expansion). Rays of the dorsal or caudal fins were never affected.

Animals