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PubMed2000

Modeling inhibitory plasticity in the electrosensory system of mormyrid electric fish.

Mathematical analyses and computer simulations are used to study the adaptation induced by plasticity at inhibitory synapses in a cerebellum-like structure, the electrosensory lateral line lobe (ELL) of mormyrid electric fish. Single-cell model results are compared with results obtained at the system level in vivo. The model of system level adaptation uses detailed temporal learning rules of plasticity at excitatory and inhibitory synapses onto Purkinje-like neurons. Synaptic plasticity in this system depends on the time difference between pre- and postsynaptic spikes. Adaptation is measured by the ability of the system to cancel a reafferent electrosensory signal by generating a negative image of the predicted signal. The effects of plasticity are tested for the relative temporal correlation between the inhibitory input and the sensory input, the gain of the sensory signal, and the presence of shunting inhibition. The model suggests that the presence of plasticity at inhibitory synapses improves the function of the system if the inhibitory inputs are temporally correlated with a predictable electrosensory signal. The functional improvements include an increased range of adaptability and a higher rate of system level adaptation. However, the presence of shunting inhibition has little effect on the dynamics of the model. The model quantifies the rate of system level adaptation and the accuracy of the negative image. We find that adaptation proceeds at a rate comparable to results obtained from experiments in vivo if the inhibitory input is correlated with electrosensory input. The mathematical analysis and computer simulations support the hypothesis that inhibitory synapses in the molecular layer of the ELL change their efficacy in response to the timing of pre- and postsynaptic spikes. Predictions include the rate of adaptation to sensory stimuli, the range of stimulus amplitudes for which adaptation is possible, the stability of stored negative images, and the timing relations of a temporal learning rule governing the inhibitory synapses. These results may be generalized to other adaptive systems in which plasticity at inhibitory synapses obeys similar learning rules.

Action Potentials↗
PubMed1993

Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines.

Electrosensory neurons in the torus semicircularis (midbrain) of the weakly electric fish Eigenmannia vary considerably in their dendritic structure and responses to modulations of the amplitude of electric organ discharges. We investigated possible relations between these properties by recording intracellularly and labeling individual neurons while modulating stimulus amplitude over rates of approximately 2-20 Hz. Morphologically distinct cell types generally differed in their responses to these stimuli. The amplitude envelope of the stimulus was nicely reflected in fluctuations of the membrane potential of heavily spined neurons. The amplitude of these stimulus-related depolarizations decreased markedly as the stimulus modulation rate was increased. For aspiny or sparsely spined neurons, however, the amplitude of stimulus-related depolarizations either increased or remained constant over this range of modulation rates. In these cells, the amplitude envelope of the stimulus was not well represented in the membrane potential. Instead, fast EPSPs were observed that varied in number over time in accordance with the amplitude envelope of the stimulus. Aspiny neurons in the tectum also coded the amplitude envelope of stimuli with poor fidelity. The amplitude of stimulus-related depolarizations, however, decreased as the rate of modulation of stimulus amplitude was increased, consistent with the notion that tectal neurons receive afferent input from the spiny toral neurons. Spiny neurons appear, therefore, to act as low-pass filters of temporal information in sensory signals. Aspiny cells, however, code high temporal frequencies. These data support the hypothesis that dendritic spines contribute to the low-pass filtering of inputs to neurons.

Afferent Pathways↗
PubMed1995

Phylogenetic analysis of the South American electric fishes (order Gymnotiformes) and the evolution of their electrogenic system: a synthesis based on morphology, electrophysiology, and mitochondrial sequence data.

The order Gymnotiformes (South American electric fishes) is a fascinating assemblage of freshwater fishes that share the unusual ability to produce and sense electric fields used for electrolocation and social communication. In the last few decades, the electrogenic and electrosensory systems (EES) of these fish have served as an excellent model to study motor and sensory physiology in vertebrates. In an attempt to the evolution of characters associated with the EES in the group, we applied maximum-parsimony (MP), minimum-evolution (ME), and maximum-likelihood (ML) methods to analyze 302 aligned bases of the mitochondrial 12S rRNA and 416 bases of the mitochondrial 16S rRNA of 19 gymnotiform genera representing all six recognized families. Six catfish genera (order Siluriformes) were also sequenced and used as outgroups. The phylogenetic hypothesis resultant from molecular data analysis differs in some respects from previous hypotheses based on morphological studies. Our results were most informative within the family level, as we were unable to elucidate the relationships among deeper branches in this order with sufficient confidence by using molecular data alone. The phylogenetic information of both mitochondrial DNA segments appears to be affected by functional constraints, and the resultant topologies were sensitive to different weighting schemes and the algorithm used. Nonetheless, we found unanimous support for the following phylogenetic relationships: (1) the family Sternopygidae is an unnatural group, and Sternopygus is the sole representative of a unique lineage within the order; (2) the family Hypopomidae is not monophyletic; and (3) the order Gymnotiformes is composed of at least six natural clades: Sternopygus, family Apteronotidae, a new clade consisting of the remaining sternopygids, families Hypopomidae + Rhamphicthyidae, family Electrophoridae, and family Gymnotidae. By combining molecular, morphological, and physiological information, we propose a new hypothesis for the phylogeny of this group and suggest a new family Eigenmanniidae n. (order Gymnotiformes).

Animals↗
PubMed1978

Postsynaptic potentials in pacemaker cells: a correlation of behavior in command cells of an electric fish.

Intracellular recordings were made from pacemaker-command cells of the electric organ discharge (EOD) of the weakly electric fish Eigenmannia virescens. The fish was immobilized with gallamine triethiodide (Flaxedil) which silenced the EOD. A simulated EOD of this fish (ca. 300 Hz) and a sine wave simulating a neighbor, a few Hz higher (+deltaF) or lower (-deltaF) were introduced into the bath to elicit the "jamming avoidance response" (JAR), monitored through the pacemaker potential. We observed that accompanying the JAR there is a minute hyperpolarizing postsynaptic potential (hpsp) superimposed on the pacemaker potential. A shift in the phase of the hpsp occurs with a change in the sign of deltaF, and therefore of the JAR. Assuming that the behaviorally correlated hpsp is inhibitory, it suggests that mutual inhibition may play a role in regulating the synchronous firing frequency of command neurons, which are electrically coupled with one-another. Scheich and Bullock (1974) proposed a neuronal scheme for the JAR in which they suggest that two systems (P and T) operate together in the nervous system. The T system affects the pacemaker cells at a precise, variable phase of the pacemaker cycle. Although the present results indeed reveal a shift in the hpsp with a change in the sign of deltaF, the actual significance of this shift remains to be evaluated. The unexpected direction of the shift suggests either that the hpsp is excitatory at the phases when it occurs, or that effectiveness of inhibition decreases at later phases in this case instead of increasing as in other cases, or that the hpsp opposes the JAR. The parallel P system is probably more important in explaining the JAR, acting by a DC level control rather than a phase control.

Action Potentials↗
PubMed1999

Predation enhances complexity in the evolution of electric fish signals.

Theories of sexual selection assume that predation is a restrictive, simplifying force in the evolution of animal display characters and many empirical studies have shown that predation opposes excessive elaboration of sexually selected traits. In an unexpected turnaround, I show here that predation pressure on neotropical, weakly electric fish (order Gymnotiformes) seems to have selected for greater signal complexity, by favouring characters that have enabled further signal elaboration by sexual selection. Most gymnotiform fish demonstrate adaptations that lower detectability of their electrolocation/communication signals by key predators. A second wave phase added to the ancestral monophasic signal shifts the emitted spectrum above the most sensitive frequencies of electroreceptive predators. By using playback trials with the predatory electric eel (Electrophorus electricus), I show that these biphasic signals are less detectable than the primitive monophasic signals. But sexually mature males of many species in the family Hypopomidae extend the duration of the second phase of their electric signal pulses and further amplify this sexual dimorphism nightly during the peak hours of reproduction. Thus a signal element that evolved for crypsis has itself been modified by sexual selection.

Animals↗
PubMed1987

The optic tectum of the gymnotiform electric fish, Eigenmannia: labeling of physiologically identified cells.

A total of 47 tectal neurons of the weakly electric fish, Eigenmannia, were studied physiologically and labelled by intracellular injection of Lucifer Yellow. With the exception of two cell types, all cells could be classified in accordance with the Golgi studies of Sas and Maler. The dominant stimulus modality of neurons was correlated with their laminar location. Neurons of the stratum opticum only responded to visual stimuli, such as modulations of the light level or the motion of an object. They showed, however, no directional preferences for motion. Neurons of the stratum griseum centrale were predominantly driven by electrosensory stimuli, most often those associated with the movement of an object, and generally were very sensitive to the direction of motion. Integration of different sensory modalities was found in neurons with dendrites invading laminae with different sensory inputs. In addition, small axons of interneurons appear to relay information across laminae. Large multipolar neurons in the deep tectum responded to the motion of objects, often preferring a particular direction of motion. Some of these large multipolar neurons of the deep tectum also discriminated the sign of the frequency difference between a mimic of a neighbor's sinusoidal electric organ discharge and the animal's own signal. These neurons are potential candidates for the control of the jamming avoidance response. These neurons were morphologically indistinguishable from large multipolar neurons of the deep tectum that either responded to moving objects or to acoustical stimuli. Individual large cells of the deep tectum project to various targets (Fig. 1) and probably contribute to the control of different behavioral responses. This suggests that the nature of such responses would then depend upon the constitution of sets of neurons recruited by a given stimulus situation, and the role of individual tectal neurons would neither be particularly specific nor very significant.

Animals↗
PubMed2000

Phylogenetic relationships of mormyrid electric fishes (Mormyridae; Teleostei) inferred from cytochrome b sequences.

The Mormyridae are African osteoglossomorph freshwater fishes of great interest because of their electric organs. They have become an important model in studies of electrophysiology and behavior but their phylogenetic relationships are poorly known. Phylogenetic relationships among mormyrids were determined by comparing cytochrome b sequences (588 bp) of 27 species belonging to 15 genera. Results showed that the Petrocephalus species (subfamily Petrocephalinae) are the sister-group of all other mormyrids (subfamily Mormyrinae). The monophyly of the Mormyrinae was supported, as well as three original intra-Mormyrinae clades. Three genera, Marcusenius, Pollimyrus, and Brienomyrus, were found to be polyphyletic with high support. Some of these polyphylies are tentatively explained. The results confirmed that the lateral ethmoid bone was lost several times within the Mormyrinae. These findings emphasize the necessity of systematic studies and taxonomic revision of the Mormyridae. The tree obtained from the mitochondrial data showed a single rise of each electrocyte type except for electrocyte with penetrating stalk ("Pa"). Constraining the single occurrence of electrocyte type Pa did not require an excessive number of extra steps (1.86%).

Animals↗
PubMed1999

Neural circuitry for communication and jamming avoidance in gymnotiform electric fish.

Over the past decade, research on the neural basis of communication and jamming avoidance in gymnotiform electric fish has concentrated on comparative studies of the premotor control of these behaviors, on the sensory processing of communication signals and on their control through the endocrine system, and tackled the question of the degree to which these behaviors share neural elements in the sensory-motor command chain by which they are controlled. From this wealth of investigations, we learned, first, how several segregated premotor pathways controlling a single central pattern generator, the medullary pacemaker nucleus, can provide a large repertoire of behaviorally relevant motor patterns. The results suggest that even small evolutionary modifications in the premotor circuitry can yield extensive changes in the behavioral output. Second, we have gained some insight into the concerted action of the brainstem, the diencephalon and the long-neglected forebrain in sensory processing and premotor control of communication behavior. Finally, these studies shed some light on the behavioral significance of multiple sensory brain maps in the electrosensory lateral line lobe that long have been a mystery. From these latter findings, it is tempting to interpret the information processing in the electrosensory system as a first step in the evolution towards the 'distributed hierarchical' organization commonly realized in sensory systems of higher vertebrates.

Animal Communication↗
PubMed1987

Oculomotor system of the weakly electric fish Gnathonemus petersii.

The peripheral and central aspects of the extraocular system were studied in the weakly electric fish Gnathonemus petersii. All six extraocular muscles show a similar composition of large and small fibers grouped characteristically in the proximal and distal regions respectively. The exit of the three extraocular nerves from the brain is similar to that in other vertebrates. However, the intracephalic and intracranial course of the trochlear nerve is unusual, partly because of the extraordinary hypertrophy of the cerebellum. The three nerves course rostrally on the ventral brain surface; the trochlear nerve penetrates the orbital cavity separately from the two other nerves. The fiber-diameter spectrum of each extraocular nerve is bimodal; unmyelinated fibers were not observed in any of the nerves. The location of the extraocular motor nuclei was established by retrograde axonal transport of HRP or cobaltic-lysine complex. The oculomotor nucleus is situated ventral to the posterior pole of the magnocellular mesencephalic nucleus and the trochlear nucleus is found caudal and dorsal to this. The abducens nucleus is situated at the level of the octavolateral efferent nucleus and consists of a single group of cells on each side of the ventral tegmentum. The oculomotor nucleus of G. petersii shows a somatotopic organization. The superior rectus muscle receives a contralateral innervation whereas the inferior rectus and oblique muscles and the internal rectus muscles receive an ipsilateral innervation. The superior oblique muscle is innervated by contralateral trochlear motoneurons and the external rectus by ipsilateral abducens motoneurons. The majority of extraocular motoneurons have piriform perikarya and long beaded dendrites that extend laterally in the oculomotor and abducens nuclei and rostrally in the trochlear nucleus. The terminal dendritic portions of trochlear motoneurons widely overlap with oculomotor dendrites and perikarya. In all three nuclei the axon originates opposite to the main dendrite. Collaterals of the hairpin-bend abducens axons could be identified in a few cases. The oculomotor system of G. petersii appears basically similar to that of other teleosts; the differences observed concern mainly the structure of the abducens nucleus, the intracranial and intracephalic course of the trochlear nerve, and the relatively small number of axons in each nerve.

Abducens Nerve↗
PubMed1993

Directional characteristics of tuberous electroreceptors in the weakly electric fish, Hypopomus (Gymnotiformes).

This paper is an electrophysiological study of the directionality of the tuberous electroreceptors of weakly electric fish. We recorded from two classes of tuberous electroreceptors known for pulse gymnotiforms: Burst Duration Coders (BDCs), and Pulse Markers (PMs). Both code for stimulus amplitude, although the dynamic range for BDCs is greater, and both exhibit strong directional preferences. Polar plots of spike number (for BDCs) or spike threshold (for PMs) versus electric field azimuth, are figure-8 shaped with two asymmetrical, elliptical lobes separated by 180 degrees. The best azimuth of these two types of receptors from a given body region correlate with each other and with measures of best azimuth for transepidermal current flow. The shape and asymmetry of the directionality profiles appear to be caused by filter dynamics of the receptors. Pulse Markers are located on the anterior part of the body surface while Burst Duration Coders are located all over. The best directions of receptors in the anterior third of the body vary systematically with location from 0 degrees to 180 degrees. This region is probably critical for determining the direction of local electric fields. Together these receptors provide the CNS with sufficient information to construct a map of horizontal plane electric field directions.

Adaptation, Physiological↗
PubMed1984

Cerebellar influence on the time structure of movement in the electric fish Eigenmannia.

To determine how cerebellar activity influences motor co-ordination, a simple motor act of an electric fish, Eigenmannia spp, was studied. Whenever the fish encounters an object of conductivity different from water, it bends the caudal two-thirds of its body towards the object. This behavior, called "probing", was analysed in the normal fish and in fish with a small cerebellar lesion. Probing could be described as a wave travelling along the body very similar to what one observes when shaking a rope of moderate elasticity. In normal fish, the wave starts at the tipe of the tail and proceeds towards the head, dying out after about two-thirds of the body length. A lesion in the corpus cerebelli causes this wave to start at the head and move towards the tail, though it is otherwise the same as in normal fish, i.e. it has the same frequency components as revealed by Fourier analysis. In addition to the change in probing, the lesioned fish also undulates its body while swimming whereas it is normally kept straight. This undulating wave turns out to be the same as that during probing where it is executed whilst the fish keeps itself on the spot with its locomotory apparatus, the anal fin, which is driven by muscles independent of the trunk muscles used for probing.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗
PubMedDate not supplied

Computational model of the jamming avoidance response in the electric fish Gymnotus carapo.

The unperturbed electric organ discharges of Gymnotus carapo fish are highly periodic with interpulse intervals around 40 ms. The 'jamming avoidance response' happens when fish interact and is a transitory interval shortening in the fish with the faster discharge that decreases the likelihood that pulses from it and the other fish will coincide. Our model's basic components match certain experimentally demonstrated facts. First, recurrence equations reproduce the periodic unperturbed discharges. Secondly, when an isolated pulse arrives, the two intervals following that with the pulse are shortened by amounts that decrease up to a minimum and then increase. Simulations demonstrated that this model reproduces satisfactorily the jamming avoidance response. Two additional conditions were demonstrably necessary: (i) one was that every pulse arrive within the hot cophase window (and not elsewhere); (ii) the other condition was that, along successive pulses, the respective cophases decrease by moderate amounts. In short, we conclude that the fish's jamming avoidance response can involve the simple computational rules implied by the proposed equations.

Animals↗
PubMed2004

AFLPs resolve phylogeny and reveal mitochondrial introgression within a species flock of African electric fish (Mormyroidea: Teleostei).

Estimating species phylogeny from a single gene tree can be especially problematic for studies of species flocks in which diversification has been rapid. Here we compare a phylogenetic hypothesis derived from cytochrome b (cyt b) sequences with another based on amplified fragment length polymorphisms (AFLP) for 60 specimens of a monophyletic riverine species flock of mormyrid electric fishes collected in Gabon, west-central Africa. We analyze the aligned cyt b sequences by Wagner parsimony and AFLP data generated from 10 primer combinations using neighbor-joining from a Nei-Li distance matrix, Wagner parsimony, and Dollo parsimony. The different analysis methods yield AFLP tree topologies with few conflicting nodes. Recovered basal relationships in the group are similar between cyt b and AFLP analyses, but differ substantially at many of the more derived nodes. More of the clades recovered with the AFLP characters are consistent with the morphological characters used to designate operational taxonomic units in this group. These results support our hypothesis that the mitochondrial gene tree differs from the overall species phylogeny due at least in part to mitochondrial introgession among lineages. Mapping the two forms of electric organ found in this group onto the AFLP tree suggests that posteriorly innervated electrocytes with nonpenetrating stalks have independently evolved from anteriorly innervated, penetrating-stalk electrocytes at least three times.

Animal Communication↗
PubMed1998

Detection of multiple stimulus features forces a trade-off in the pyramidal cell network of a gymnotiform electric fish's electrosensory lateral line lobe.

Modification of an existing neural structure to support a second function will produce a trade-off between the two functions if they are in some way incompatible. The trade-off between two such sensory functions is modeled here in pyramidal neurons of the gymnotiform electric fish's medullar electrosensory lateral line lobe (ELL). These neurons detect two electric stimulus features produced when a nearby object interferes with the fish's autogenous electric field: (1) amplitude modulation across a cell's entire receptive field and (2) amplitude variation within a cell's receptive field produced by an object's edge. A model of sensory integration shows that detection of amplitude modulation and enhancement of spatial contrast involve an inherent mechanistic trade-off and that the severity of the trade-off depends on the particular algorithm of sensory integration. Electrophysiology data indicate that of the two algorithms for sensory integration modeled here for the gymnotiform fish Brachyhypopomus pinnicaudatus, the algorithm with the better trade-off function is used. Further, the intrinsic trade-off within single cells has been surmounted by the replication of ELL into multiple electrosensory map segments, each specialized to emphasize different sensory features.

Animals↗
PubMed1977

Neuronal mechanisms for object discrimination in the weakly electric fish Eigenmannia virescens.

The peripheral sensory basis for object discrimination was investigated in the weakly electric fish Eigenmannia virescens. Single unit recordings were made from the primary afferent fibres in the posterior branch of the anterior lateral line nerve while the local electric field (self-generated and stimulated) was modified by external resistance and capacitance shunts. Both fibre types (probability and phase coders) responded differentially to capacitance and resistance shunts of equivalent impedence. The degree of response differentiation between the two shunting conditions varied with the intensity of the electrical stimulus at the receptor. These data suggest that the primary electroreceptors can discriminatively encode the two electrical characteristics of 'objects'. However, since the response of primary electroreceptors also varied with the spatial orientation of the shunting electrodes, central structures must play an important role in object discrimination.

Action Potentials↗
PubMed1997

Connections of the basal forebrain of the weakly electric fish, Eigenmannia virescens.

The organization of the ventral nucleus of the ventral telencephalon (Vv) was examined in the weakly electric fish, Eigenmannia virescens. This nucleus, which is considered the teleost homologue to the basal forebrain nuclei of other vertebrates, was subdivided into dorsal and ventral subdivisions, based upon cytoarchitectonic, immunohistochemical, and connectional criteria. Afferent projections were observed from the medial olfactory bulb as well as the terminal nerve ganglion. Telencephalic afferents to the Vv were very restricted, consisting of the supracommissural and the dorsal intermediate nuclei of the ventral telencephalon, the nucleus taenia, and the medial region of the posterior nucleus of the dorsal telencephalon. However, the major afferents to the Vv were diencephalic, particularly those originating from the rostral preoptic area and other hypothalamic nuclei. Additional afferents included the posterior tubercular nucleus, the locus coeruleus, the medial perilemniscal nucleus, and the periventricular nucleus of the posterior tuberculum. Relatively weak projections were observed from the ventral thalamus and the dorsal posterior thalamic nucleus. As described previously, the diencephalic complex of the central posterior thalamic nucleus/prepacemaker nucleus (CP/PPn), which also has cells that innervate the pacemaker circuitry controlling the production of an electric organ discharge, projects to the Vv. Terminal fields of the Vv were observed to be coextensive with afferent cell groups in the preoptic area, lateral and caudal hypothalamic nuclei, and thalamus. An additional efferent target of the Vv was the pretectal nucleus electrosensorius. That many cell groups that are connected with the Vv are also connected with the CP/PPn, particularly the preoptic and hypothalamic nuclei, suggests that the electrocommunicatory system is intimately linked with basal forebrain limbic pathways.

Animals↗
PubMed1977

The role of the electrosensory system in postural control of the weakly electric fish Eigenmannia virescens.

The role of the electrosensory inputs in postural control was examined in the weakly electric fish Eigenmannia virescens. These fish exhibit tonic postural tilt in response to a tilted plexiglas substrate in both transverse and longitudinal planes (rolling and head-up pitching responses, respectively), but not to electrically "transparent" agar substrate. The fish's pitching and rolling responses were abolished when the electrosensory inputs from the trunk were bilaterally eliminated even though the fish's visual and mechanosensory lateral-line systems remained intact. Unilateral lesion abolished the rolling response but not the pitching response. These results demonstrate the functional role of the electrosensory system in postural control, in addition to its known role in social communication and in object location, and the underlying neuronal mechanism is discussed.

Animals↗
PubMed2004

Influence of temperature and reproductive state upon the jamming avoidance response in the pulse-type electric fish Brachyhypopomus pinnicaudatus.

The electric organ discharge (EOD) in Brachyhypopomus pinnicaudatus is modified by temperature and reproductive state. We studied the influence of these variables upon a complex behavior, the jamming avoidance response (JAR). Experiments were performed in non-reproductive fish and in two groups of fish after the induction of reproductive state (by nature or by acclimation at 28 degrees C). JARs were elicited at 20 and 30 degrees C by free-run electric stimuli with different deltaLs (interval difference between stimulus and EOD). In non-reproductive fish, JARs induced by stimuli with +deltaLs showed temperature sensitivity, with smaller responses at 30 degrees C. Conversely, similar JARs were obtained at both temperatures in reproductive fish. These observations were replicated in curarized preparations. Stimuli with -deltaLs were almost ineffective in non-reproductive fish at 30 degrees C, whereas adequate JARs were shown by reproductive fish. Phase-locked stimuli were used to evaluate the duration of the low-threshold electrosensory periods preceding and following the EOD. In non-reproductive fish, the temperature step induced a shortening of these periods. The opposite effect was observed in reproductive fish, probably explaining the differences in JAR capability. A prolongation of the low-threshold periods would favor the perception of electrocommunication signals during courtship. JAR changes would be a consequence of this adaptation.

Animals↗