Electric organ discharges and electric images during electrolocation.
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Weakly electric fish use active electrolocation - the generation and detection of electric currents - to explore their surroundings. Although electrosensory systems include some of the most extensively understood circuits in the vertebrate central nervous system, relatively little is known quantitatively about how fish electrolocate objects. We believe a prerequisite to understanding electrolocation and its underlying neural substrates is to quantify and visualize the peripheral electrosensory information measured by the electroreceptors. We have therefore focused on reconstructing both the electric organ discharges (EODs) and the electric images resulting from nearby objects and the fish's exploratory behaviors. Here, we review results from a combination of techniques, including field measurements, numerical and semi-analytical simulations, and video imaging of behaviors. EOD maps are presented and interpreted for six gymnotiform species. They reveal diverse electric field patterns that have significant implications for both the electrosensory and electromotor systems. Our simulations generated predictions of the electric images from nearby objects as well as sequences of electric images during exploratory behaviors. These methods are leading to the identification of image features and computational algorithms that could reliably encode electrosensory information and may help guide electrophysiological experiments exploring the neural basis of electrolocation. (+info)
Prey capture in the weakly electric fish Apteronotus albifrons: sensory acquisition strategies and electrosensory consequences.
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Sensory systems are faced with the task of extracting behaviorally relevant information from complex sensory environments. In general, sensory acquisition involves two aspects: the control of peripheral sensory surfaces to improve signal reception and the subsequent neural filtering of incoming sensory signals to extract and enhance signals of interest. The electrosensory system of weakly electric fish provides a good model system for studying both these aspects of sensory acquisition. On the basis of infrared video recordings of black ghost knifefish (Apteronotus albifrons) feeding on small prey (Daphnia magna) in the dark, we reconstruct three-dimensional movement trajectories of the fish and prey. We combine the reconstructed trajectory information with models of peripheral electric image formation and primary electrosensory afferent response dynamics to estimate the spatiotemporal patterns of transdermal potential change and afferent activation that occur during prey-capture behavior. We characterize the behavioral strategies used by the fish, with emphasis on the functional importance of the dorsal edge in prey capture behavior, and we analyze the electrosensory consequences. In particular, we find that the high-pass filter characteristics of P-type afferent response dynamics can serve as a predictive filter for estimating the future position of the prey as the electrosensory image moves across the receptor array. (+info)
Design features for electric communication.
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How do the communication discharges produced by electric fish evolve to accommodate the unique design features for the modality? Two design features are considered: first, the limited range of signaling imposed on the electric modality by the physics of signal transmission from dipole sources; and second, the absence of signal echoes and reverberations for electric discharges, which are non-propagating electrostatic fields. Electrostatic theory predicts that electric discharges from fish will have a short range because of the inverse cube law of geometric spreading around an electrostatic dipole. From this, one predicts that the costs of signaling will be high when fish attempt to signal over a large distance. Electric fish may economize in signal production whenever possible. For example, some gymnotiform fish appear to be impedance-matched to the resistivity of the water; others modulate the amplitude of their discharge seasonally and diurnally. The fact that electric signals do not propagate, but exist as electrostatic fields, means that, unlike sound signals, electric organ discharges produce no echoes or reverberations. Because temporal information is preserved during signal transmission, receivers may pay close attention to the temporal details of electric signals. As a consequence, electric organs have evolved with mechanisms for controlling the fine structure of electric discharge waveforms. (+info)
Mechanisms for generating temporal filters in the electrosensory system.
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Temporal patterns of sensory information are important cues in behaviors ranging from spatial analyses to communication. Neural representations of the temporal structure of sensory signals include fluctuations in the discharge rate of neurons over time (peripheral nervous system) and the differential level of activity in neurons tuned to particular temporal features (temporal filters in the central nervous system). This paper presents our current understanding of the mechanisms responsible for the transformations between these representations in electric fish of the genus Eigenmannia. The roles of passive and active membrane properties of neurons, and frequency-dependent gain-control mechanisms are discussed. (+info)
Physiology of electrosensory lateral line lobe neurons in Gnathonemus petersii.
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In mormyrid electric fish, sensory signals from electroreceptors are relayed to secondary sensory neurons in a cerebellum-like structure known as the electrosensory lateral line lobe (ELL). Efferent neurons and interneurons of the ELL also receive inputs of central origin, including electric organ corollary discharge signals, via parallel fibers and via fibers from the juxtalobar nucleus. To understand the cellular mechanisms of the integration of sensory inputs and central inputs in the ELL, the intracellular activity and ionic properties of the efferent projection neurons and interneurons were examined in an in vitro slice preparation.We focus here on the electrophysiological properties of the efferent neurons of the ELL network, the large fusiform cells and large ganglion cells, and on a class of gamma-aminobutyric acid (GABA)-ergic interneurons known as medium ganglion (MG) cells. In response to current injection through a recording pipette, both types of efferent neuron fire a large narrow spike followed by a large hyperpolarizing afterpotential. The MG cells fire a complex spike which consists of small narrow spikes and a large broad spike. Although the forms of the action potentials in efferent neurons and in MG cells are different, all spikes are mediated by tetrodotoxin (TTX)-sensitive Na+ conductances and spike repolarization is mediated by tetraethylammonium (TEA+)-sensitive K+ conductances. In the presence of TEA+, substitution of Ba2+ for Ca2+ in the bath revealed the presence of a high-voltage-activated Ca2+ conductance. Stimulation of parallel fibers conveying descending input to the ELL molecular layer in vitro evokes an excitatory postsynaptic potential (EPSP), generally followed by an inhibitory postsynaptic potential (IPSP), in the efferent neurons. In MG cells, the same stimulation evokes an EPSP, often followed by a small IPSP. Synaptic transmission at parallel fiber synapses is glutamatergic and is mediated via both N-methyl-d-aspartate (NMDA)- and (AMPA)-type glutamate receptors. The inhibitory component of the parallel fiber response is GABAergic. It is probably mediated via the stellate neurons and the MG cells, which are themselves GABAergic interneurons intrinsic to the ELL network.A hypothetical neural circuit of the intrinsic connections of the ELL, based on the known morphology of projection neurons and medium ganglion interneurons, is presented. This circuit includes an excitatory and an inhibitory submodule. The excitatory submodule is centered on a large fusiform cell and appears to relay the sensory input as a positive 'ON' image of an object. The inhibitory submodule is centered on a large ganglion cell and relays a negative 'OFF' image to the next higher level. We suggest that MG cells exert an inhibitory bias on efferent neuron types and that the ELL network output is modulated by the dynamically plastic integration of central descending signals with sensory input. (+info)
Molecular biology of the apteronotus NMDA receptor NR1 subunit.
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The complete sequences and expression patterns of the NR1 (aptNR1) subunit of the N-methyl-d-aspartate (NMDA) receptor and its alternative splice isoforms have been determined for the weakly electric fish Apteronotus leptorhynchus. The deduced amino acid sequence of aptNR1 is approximately 88 % identical to the NR1 sequences of other vertebrate. Two of the three alternative splice cassettes previously described for mammalian NR1s, N1 and C1, are present in aptNR1, but the third cassette, C2, is not found. In addition, two teleost-specific splice cassettes occur on the N-terminal side of the C1 sequence. The cellular patterns of aptNR1 expression, including the patterns of N1 and C1 splicing, have been mapped using the in situ hybridization technique. High levels of aptNR1 mRNA were detected throughout the central nervous system including most neurons of the electrosensory system, with the highest levels in electrosensory lateral line lobe pyramidal cells. Expression of the N1 splice isoform was higher in more caudal regions of the brain, and expression of the C1 splice isoform was higher in more rostral regions. The N1 splice isoform was present in almost all NR1-positive cells, in contrast to the C1 splice isoform which was restricted to a subset of NR1-positive cells. These results demonstrate that the NR1 subunit of the NMDA receptor is evolutionarily conserved across species and that regulation of alternative RNA splicing modulates the properties of NR1 in different neurons of the central nervous system of A. leptorhynchus. (+info)
Plasticity of feedback inputs in the apteronotid electrosensory system.
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Weakly electric fish generate an electric field surrounding their body by means of an electric organ typically located within the trunk and tail. Electroreceptors scattered over the surface of the body encode the amplitude and timing of the electric organ discharge (EOD), and central components of the electrosensory system analyze the information provided by the electroreceptor afferents. The electrosensory system is used for electrolocation, for the detection and analysis of objects near the fish which distort the EOD and for electrocommunication. Since the electric organ is typically located in the tail, any movement of this structure relative to the rest of the body alters the EOD field, resulting in large changes in receptor afferent activity. The amplitude of these reafferent stimuli can exceed the amplitudes of near-threshold electrolocation signals by several orders of magnitude. This review summarizes recent studies of the South American weakly electric fish Apteronotus leptorhynchus aimed at determining how the animals differentiate self-generated or reafferent electrosensory stimuli from those that are more behaviorally relevant. Cells within the earliest stages of central electrosensory processing utilize an adaptive filtering technique which allows the system preferentially to attenuate reafferent as well as other predictable patterns of sensory input without degrading responses to more novel stimuli. Synaptic plasticity within the system underlies the adaptive component of the filter and enables the system to learn to reject new stimulus patterns if these become predictable. A Ca2+-mediated form of postsynaptic depression contributes to this synaptic plasticity. The filter mechanism seen in A. leptorhynchus is surprisingly similar to adaptive filters described previously in mormyrid weakly electric fish and in elasmobranchs, suggesting that this mechanism may be a common feature of sensory processing systems. (+info)
Synaptic plasticity in the mormyrid electrosensory lobe.
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The mormyrid electrosensory lateral line lobe (ELL) is one of several different sensory structures in fish that behave as adaptive sensory processors. These structures generate negative images of predictable features in the sensory inflow which are added to the actual inflow to minimize the effects of predictable sensory features. The negative images are generated through a process of association between centrally originating predictive signals and sensory inputs from the periphery. In vitro studies in the mormyrid ELL show that pairing of parallel fiber input with Na+ spikes in postsynaptic cells results in synaptic depression at the parallel fiber synapses. The synaptic plasticity observed at the cellular level and the associative process of generating negative images of predicted sensory input at the systems level share a number of properties. Both are rapidly established, anti-Hebbian, reversible, input-specific and tightly restricted in time. These common properties argue strongly that associative depression at the parallel fiber synapse contributes to the adaptive generation of negative images in the mormyrid ELL. (+info)