Cutaneous electrical oscillation in a weakly electric fish, Gymnarchus niloticus

An African electric fish, Gymnarchus niloticus. ceases its electric organ discharge for a prolonged time in response to external electrical signals. During the cessation of electric organ discharges from the electric organ, a weak sinusoidal signal (approximately 0.1 mV cm(-1)) near the fish's previous discharge frequency was recorded near the body. The oscillatory potentials at all points on the body surface were synchronized and had a complex spatial distribution. The source of the potential was determined to be within the dermal tissue. Electroreceptive central neurons that responded to a moving target near the fish with normal electric organ discharges also responded to the same target when the electric organ discharge was interrupted and the potential from the skin existed. This result suggests that the fish may be able to electrolocate objects without the discharge from the electric organ.     

The African wave-type electric fish,Gymnarchus niloticus,lacks corollary discharge mechanisms for electrosensory gating

Gymnarchus niloticus, a wave-type African electric fish, performs its jamming avoidance response by relying solely upon afferent signals and does not use corollary discharges from the pacemaker nucleus in the medulla which generates the rhythmicity of electric organ discharges. This is in sharp contrast to the mode of sensory processing found in closely related African pulse-type electric fishes where afferent signals are gated by corollary discharges from the pacemaker for the distinction of exafferent and reafferent stimuli. Does Gymnarchus still possess a corollary discharge mechanism for other behavioral tasks but does not use it for the jamming avoidance response? In this study, I recorded from and labeled medullary neuronal structures that either generate or convey the pacemaker signal for electric organ discharges to examine whether this information is also sent directly to any sensory areas. The pacemaker nucleus was identified as the site of generation of the pacemaking signal. The pacemaker neurons project exclusively to the lateral relay nucleus which, in turn projects exclusively to the medial relay nucleus. Neurons in the medial relay nucleus send unbranched axons to the spinal electromotoneurons. These neurons are entirely devoted to drive the electric organ discharges, and no axon collaterals from these neurons were found to project to any sensory areas. This indicates that Gymnarchus does not possess the neuronal hardware for a corollary discharge mechanism.     

Interruption of pacemaker signals by a diencephalic nucleus in the African electric fish, Gymnarchus niloticus

The African electric fish Gymnarchus niloticus rhythmically emits electric organ discharges (EODs) for communication and navigation. The EODs are generated by the electric organ in the tail in response to the command signals from the medullary pacemaker complex, which consists of a pacemaker nucleus (PN), two lateral relay nuclei (LRN) and a medial relay nucleus (MRN). The premotor structure and its modulatory influences on the pacemaker complex have been investigated in this paper. A bilateral prepacemaker nucleus (PPn) was found in the area of the dorsal posterior nucleus (DP) of the thalamus by retrograde labeling from the PN. No retrogradely labeled neurons outside the pacemaker complex were found after tracer injection into the LRN or MRN. Accordingly, anterogradely labeled terminal fibers from PPn neurons were found only in the PN. Iontophoresis of l-glutamate into the region of the PPn induced EOD interruptions. Despite the exclusive projection of the PPn neurons to the PN, extracellular and intracellular recordings showed that PN neurons continue their firing while MRN neurons ceased their firing during EOD interruption. This mode of EOD interruption differs from those found in any other weakly electric fishes in which EOD cessation mechanisms have been known.     

Emergence of temporal-pattern sensitive neurons in the midbrain of weakly electric fish Gymnarchus niloticus.

Sensitivity of neurons in the torus semicircularis of a weakly electric fish, Gymnarchus niloticus, to two stimulus parameters that are critical for its behavior the jamming avoidance response was examined. The first parameter is the sign of frequency difference between discharge frequencies of fish's own electric organ and that of a neighbor's. The second parameter is the spatial orientation of neighbor's electric field. Whereas neuronal ambiguity of frequency coding for different orientations of neighbor's electric field is predicted, unambiguous JAR occurs at the behavioral level. Most neurons in the torus semicircularis showed sensitivity to the sign of frequency difference. Although a small number of neurons showed preference to a consistent sign of the frequency difference, the coding of the sign of frequency differences was found to be ambiguous with a highly variable pattern of responses for different orientations in most of neurons.     

Independently evolved jamming avoidance responses employ identical computational algorithms: a behavioral study of the African electric fish,Gymnarchus niloticus

An African electric fish, Gymnarchus, and a South American electric fish, Eigenmannia, are believed to have evolved their electrosensory systems independently. Both fishes, nevertheless, gradually shift the frequency of electric organ discharge away when they encounter a neighbor of a similar discharge frequency. Computational algorithms employed by Gymnarchus for this jamming avoidance response have been identified in this study for comparison with those of extensively studied Eigenmannia.

1. Gymnarchus determines whether it should raise or lower its discharge frequency based solely upon the signal mixture of its own reafferent and the exafferent signal from a neighbor, and does not internally refer to the pacemaker command signal which drives its own discharge.
2. The signal mixture is analyzed in terms of the time courses of amplitude modulation and phase modulation at each area of the body surface.
3. Phase of the signal mixture at each area is compared with that of another area for the detection of phase modulation.
4. Unambiguous information necessary for the jamming avoidance response is extracted by integrating information from all body areas each of which yields ambiguous information.
5. These computational features are identical to those of Eigenmannia, suggesting that the neural circuit for jamming avoidance responses may have evolved from preexisting mechanisms for electrolocation in both fishes.

     

Development of electric organs of Gymnarchus niloticus (fam. Gymnarchidae). I. Origin and histogenesis of electroplates

The development of the electric organs of Gymnarchus niloticus has been studied and the origin and histogenesis of an electroplate worked out. A segmental origin of the electroplate is reported for the first time for this fish. Light has been thrown on many hitherto obscure phenomena, viz., growth of core girth, loss of transverse striations on the myofibrillar elements, differentiation of electroplate polarities, shortening in length of the electroplate etc. The transverse striations of the myofibrillar bundle of the electroplate primordium progressively disappear with development owing to splitting apart of the constituent myofilaments and consequent loss of their parallel order, and not to degeneration of the myofibrillar bundle. The excessive growth of the core girth of the electroplates is caused by the deposition of some kind of interfibrillar substance probably secreted by the peripheral cytoplasm.     

Special cutaneous receptor organs of fish. 3. The ampullary organs of Eigenmannia

Ampullary receptor organs of the South American weakly electric gymnotid fish Eigenmannia virescens consist of a pore at the surface of the skin, a canal through the epidermis, and the expanded basal end of the canal in the corium. The cavity of the organ contains a jelly that is filled with fine fibers. The canal wall consists of three to six layers of flattened cells that appear to be derived from the adjacent skin. Along the lumen of the organ the cells are joined by tight junctions. Usually there are four spherical receptor cells in the base of the organ. They are innervated by single neural terminals. These organs are compared to tuberous receptor organs found in the same species, and the functional significance of the fine structure observed in these cells is discussed.     

II. Ultrastructure of the type B sense organ of the specific lateral line system of Gymnarchus niloticus

Summary The type B cutaneous receptor represents one of the three kinds of specific organs of the lateral line system of Gymnarchus niloticus (Szabo and Barets, 1963). Electron microscopic observations reveal that the elementary unit (Fig. 18) of the type B organ consists of a well organized assembly of different epithelial elements grouped around each sensory cell. Several such units compose a type B organ innervated by a single myelinated nerve fiber.The cytoplasm of the sensory cell is characterised by a deep invagination lined by long and densely packed microvilli covered by a jelly-like substance. This jelly substance of allongated stylet form is situated in an intraepidermal cavity, overlaid by vacuolised epithelial cells oriented perpendicularly toward the external epidermal surface.Certain morphological characteristics of the organ B allows the conclusion that this organ is one of the possible electroreceptors of the Gymnarchus niloticus.This work was supported by grant No. 659535 of the Direction de Recherches et Moyens d'Essais (D.R.M.E.) to Dr. Szabo.This work was carried out on the electronmicroscope of the Service de Microscopie Electronique du Laboratoire de Médecine Experimentale (RCA) et du Laboratoire d'Histologie Normale et Pathologique du Système Nerveux (Siemens).With the technical assistance of Miss L. Seguin and Mr. C. Pennarun.     

The electroreceptive ampullary organs of urodeles

The system of lateral-line organs in urodeles was examined by the use of various light- and electron-microscopical techniques. The results show that, in addition to the well-known mechanoreceptive neuromast organs, a second type of receptor can be identified. This second type of organ was presumably seen by earlier workers, but they seemingly failed to point out the distinction between the two organs. The presently described organs are anatomically similar to the ampullary organs of various anamniotic species such as Brachiopterygii, sturgeons, lungfish, and silurids. In all these species the ampullary organs display only one afferent fiber but no efferent innervation and are situated around an ampullary enlargement in or below the epidermis as in urodeles. All ampullary receptors including those of urodeles are very sensitive to weak electrical fields. Similar to the situation in teleosts, the ampullae of urodeles show numerous microvilli but no kinocilia. All other nonteleostean ampullary receptors appear to possess only kinocilia as apical specializations but no microvilli. Current evidence suggests that the electroreceptive ampullary organs are as phylogenetically old as all other vertebrate sensory systems; they are now known to be relatively common among anamniotic vertebrates. Since all ampullary receptors share many common characteristics, it is assumed that they were derived from one phylogenetic precursor but have evolved certain peculiarities in each species not shared by other ampullary receptors.     

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.     

Zum Frequenzverhalten von Gymnarchus niloticus Cuv. (Mormyriformes,Teleostei)

Zusammenfassung Bei fünf Tieren der Art Gymnarchus niloticusCuv. wurden die Entladungen ihres elektrischen Organs untersucht. Vier Tiere sendeten ohne Unterbrechung; lediglich ein Tier unterbrach während eines Zeitraumes von etwa 27 Std seine Aktivität ohne erkennbare Einflüsse aus der Umwelt im Mittel 8–9 mal in der Stunde für durchschnittlich 18,5 sec.Durch Einwirkungen äußerer elektrischer Felder wird ein Aussetzen der Tätigkeit des elektrischen Organs hervorgerufen. Bei einem homogenen elektrischen Wechselfeld veränderlicher Frequenz lag die Schwelle für diese Reaktion für Frequenzen von 50–800 Hz bei etwa 20 mV_ss/cm. Bei höheren Frequenzen liegt die Reaktionsschwelle wesentlich höher.

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Summary Investigations on the continuity of the electric discharges of five specimen of the species Gymnarchus niloticusCuv. have been carried out. Four specimen did not interrupt their emission, one specimen paused within a time interval of 27 hours 8 to 9 times per hour with an average value of 18,5 sec without perceptible influences from the environment.Externally applied electric fields cause an interruption of the emission of the electric organ. For an homogenous electric field of variable frequency the threshold of this reaction has been found to be about 20 mV_pp/cm for frequencies from 50 to 800 Cps. For higher frequencies the threshold proved to be essentially higher.

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Die Verfasser danken dem Bundesministerium der Verteidigung für die Bereitstellung der erforderlichen Mittel.

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Jetzt: Zoophysiologisches Institut der Universität Tübingen.     

Structural and functional effects of heavy metals on the nervous system,including sense organs,of fish

• 1.1. Today, fish in the environment are inevitably exposed to chemical pollution. Although most hazardous substances are present at concentrations far below the lethal level, they may still cause serious damage to the life processes of these animals.
• 2.2. Fish depend on an intact nervous system, including their sense organs, for mediating relevant behaviour such as food search, predator recognition, communication and orientation.
• 3.3. Unfortunately, the nervous system is most vulnerable and injuries to its elements may dramatically change the behaviour and consequently the survival of fish.
• 4.4. Heavy metals are well known pollutants in the aquatic environment. Their interaction with relevant chemical stimuli may interfere with the communication between fish and environment.
• 5.5. The affinity for a number of ligands and macromolecules makes heavy metals most potent neurotoxins.
• 6.6. The present Mini-Review highlights some aspects of how trace concentrations of mercury, copper and lead affect the integrity of the fish nervous system; structurally, physiologically and biochemically.

     

Retreat site selection and social organization in captive electric fish, Apteronotus leptorhynchus

Gymnotiform fish use their electric organ discharge for electrolocation and communication. They are active nocturnally and seek retreat sites during the day. We examined retreat site selection in Apteronotus leptorhynchus by assessing their preference for retreat tubes that differed in opacity and dimension. Isolated fish preferred opaque to clear tubes, long and narrow diameter tubes to short, wide diameter tubes, and open-ended to closed tubes. We also assessed how groups of fish distributed themselves in tubes according to sex and electric organ discharge frequency under four conditions: (1) unlimited tube availability, (2) limited tube availability, (3) variation in tube opacity, and (4) variation in tube dimension. When tube availability was unlimited, fish generally preferred to occupy tubes alone. However, females, but not males, often cohabited tubes with consexuals. When tube availability was limited, females were more often than males found outside of tubes. When tubes varied by opacity and dimension, fish clustered most commonly in preferred tube types (opaque and long tubes). Males with the highest electric organ discharge frequencies usually occupied the most preferred tube type. Thus, fish have clear preferences in selecting retreat sites and groups of fish reveal their dominance relationships when presented with variation in retreat sites.