The slow pathway in the electrosensory lobe of Gymnotus omarorum: field potentials and unitary activity.

This is a first communication on the self-activation pattern of the electrosensory lobe in the pulse weakly electric fish Gymnotus omarorum. Field potentials in response to the fish's own electric organ discharge (EOD) were recorded along vertical tracks (50µm step) and on a transversal lattice array across the electrosensory lobe (resolution 50µm×100µm). The unitary activity of 82 neurons was recorded in the same experiments. Field potential analysis indicates that the slow electrosensory path shows a characteristic post-EOD pattern of activity marked by three main events: (i) a small and early component at about 7ms, (ii) an intermediate peak about 13ms and (iii) a late broad component peaking after 20ms. Unit firing rate showed a wide range of latencies between 3 and 30ms and a variable number of spikes (median 0.28units/EOD). Conditional probability analysis showed monomodal and multimodal post-EOD histograms, with the peaks of unit activity histograms often matching the timing of the main components of the field potentials. Monomodal responses were sub-classified as phase locked monomodal (variance smaller than 1ms), early monomodal (intermediate variance, often firing in doublets, peaking range 10-17ms) and late monomodal (large variance, often firing two spikes separated about 10ms, peaking beyond 17ms). The responses of multimodal units showed that their firing probability was either enhanced, or depressed just after the EOD. In this last (depressed) subtype of unit the probability stepped down just after the EOD. Early inhibition and the presence of early phase locked units suggest that the observed pattern may be influenced by a fast feed forward inhibition. We conclude that the ELL in pulse gymnotiformes is activated in a complex sequence of events that reflects the ELL network connectivity.

Electric organ discharge diversity in the genus Gymnotus: anatomo-functional groups and electrogenic mechanisms.

Previous studies describe six factors accounting for interspecific diversity of electric organ discharge (EOD) waveforms in Gymnotus. At the cellular level, three factors determine the locally generated waveforms: (1) electrocyte geometry and channel repertoire; (2) the localization of synaptic contacts on electrocyte surfaces; and (3) electric activity of electromotor axons preceding the discharge of electrocytes. At the organismic level, three factors determine the integration of the EOD as a behavioral unit: (4) the distribution of different types of electrocytes and specialized passive tissue forming the electric organ (EO); (5) the neural mechanisms of electrocyte discharge coordination; and (6) post-effector mechanisms. Here, we reconfirm the importance of the first five of these factors based on comparative studies of a wider diversity of Gymnotus than previously investigated. Additionally, we report a hitherto unseen aspect of EOD diversity in Gymnotus. The central region of the EO (which has the largest weight on the conspecific-received field) usually exhibits a negative-positive-negative pattern where the delay between the early negative and positive peaks (determined by neural coordination mechanisms) matches the delay between the positive and late negative peaks (determined by electrocyte responsiveness). Because delays between peaks typically determine the peak power frequency, this matching implies a co-evolution of neural and myogenic coordination mechanisms in determining the spectral specificity of the intraspecific communication channel. Finally, we define four functional species groups based on EO/EOD structure. The first three exhibit a heterogeneous EO in which doubly innervated electrocytes are responsible for a main triphasic complex. Group I species exhibit a characteristic cephalic extension of the EO. Group II species exhibit an early positive component of putative neural origin, and strong EO auto-excitability. Group III species exhibit an early, slow, negative wave of abdominal origin, and variation in EO auto-excitability. Representatives of Group IV generate a unique waveform comprising a main positive peak followed by a small, load-dependent negative component.

Waveform generation in the weakly electric fish Gymnotus coropinae (Hoedeman): the electric organ and the electric organ discharge.

This article deals with the electric organ and its discharge in Gymnotus coropinae, a representative species of one of the three main clades of the genus. Three regions with bilateral symmetry are described: (1) subopercular (medial and lateral columns of complex shaped electrocytes); (2) abdominal (medial and lateral columns of cuboidal and fusiform electrocytes); and (3) main [four columns, one dorso-lateral (containing fusiform electrocytes) and three medial (containing cuboidal electrocytes)]. Subopercular electrocytes are all caudally innervated whereas two of the medial subopercular ones are also rostrally innervated. Fusiform electrocytes are medially innervated at the abdominal portion, and at their rostral and caudal poles at the main portion. Cuboidal electrocytes are always caudally innervated. The subopercular portion generates a slow head-negative wave (V(1r)) followed by a head-positive spike (V(3r)). The abdominal and main portions generate a fast tetra-phasic complex (V(2345ct)). Since subopercular components prevail in the near field and the rest in the far field, time coincidence of V(3r) with V(2) leads to different waveforms depending on the position of the receiver. This confirms the splitting hypothesis of communication and exploration channels based on the different timing, frequency band and reach of the regional waveforms. The following hypothesis is compatible with the observed anatomo-functional organization: V(1r) corresponds to the rostral activation of medial subopercular electrocytes and V(3r) to the caudal activation of all subopercular electrocytes; V(2), and part of V(3ct), corresponds to the successive activation of the rostral and caudal poles of dorso-lateral fusiform electrocytes; and V(345ct) is initiated in the caudal face of cuboidal electrocytes by synaptic activation (V(3ct)) and it is completed (V(45ct)) by the successive activation of rostral and caudal faces by the action currents evoked in the opposite face.

Active electroreception in Gymnotus omari: imaging, object discrimination, and early processing of actively generated signals.

Weakly electric fishes "electrically illuminate" the environment in two forms: pulse fishes emit a succession of discrete electric discharges while wave fishes emit a continuous wave. These strategies are present in both taxonomic groups of weakly electric fishes, mormyrids and gymnotids. As a consequence one can distinguish four major types of active electrosensory strategies evolving in parallel. Pulse gymnotids have an electrolocating strategy common with pulse mormyrids, but brains of pulse and wave gymnotids are alike. The beating strategy associated to other differences in the electrogenic system and electrosensory responses suggests that similar hardware might work in a different mode for processing actively generated electrosensory images. In this review we summarize our findings in pulse gymnotids' active electroreception and outline a primary agenda for the next research.

Lipids associated with the (Na+ - K+)ATPase of normal and denervated electric organs of Electrophorus electricus (L.).

The effect of denervation on the lipid metabolism and on the activity of (Na+ - K+)ATPase isoforms from the membrane fraction P3, which corresponds to the innervated electrocyte membrane, was evaluated. On a discontinuous sucrose gradient, normal P3 membranes exhibit a bimodal ("a" and "b bands) distribution of the (Na+ - K+)ATPase activity, which upon denervation changes to an unimodal ("c" band) distribution. Using these fractions, which have a higher (Na+ - K+)ATPase activity, we characterized the lipids at the hydrophobic protein surface boundary, (i.e., the bulk lipids that surround the protein). The results confirm that these lipids consist of phospholipids and cholesterol. The quantitative composition of the phospholipids is similar for both isoform fractions obtained from the discontinuous gradient of normal membranes, with phosphatidylcholine, phosphatidylethanolamine and phosphatidylserine representing about 90% of the total phospholipids. Sphingomyelin, phosphatidylinositol, diphosphatidylglycerol and phosphatidic acid were in the minority. However, in the single band obtained after denervation, the three major phospholipid components decreased to 70% of the total, and a significant increase in the other phospholipids and in cholesterol was observed. The high cholesterol content of the denervated fraction may confer membrane stabilization, as it is likely to cause a decrease in the membrane fluidity and consequently in the enzyme activity.

The spinal cord of Gymnotus carapo: the electromotoneurons and their projection patterns.

The electric organ of Gymnotus carapo lies parallel to the spinal cord and extends from the pectoral girdle to the tip of the tail. The spinal electromotoneurons are distributed in a relatively consistent pattern: there is a peak at 17% of the fish's length and an irregular distribution beyond 25%. Horseradish peroxidase injections into the electric organ not exceeding 5% of the fish's length labeled electromotoneuron arrays occupying 20% of the fish's length. Injections made in four discrete rostrocaudal electric organ regions resulted in labeled electromotoneurons distributed along four sequential but overlapping arrays. Since the caudal portion of the spinal cord lacks electromotoneurons, there is a shortened representation of the electric organ. The electromotoneuron population is not homogeneous: there are small neurons (somata 25-40 microns) and large neurons (somata 45-60 microns) unevenly distributed along the cord. Small neurons occur at more rostral spinal cord segments, while large neurons lie in more caudal segments. Both kinds of nerve cells coexist in the intermediate regions. Overlapping of subsequent neuronal arrays favors synchronized firing of electrocytes. The presence of two neuronal populations differing in size and projecting to opposite electrocyte faces may account for the timed excitation of the electrogenic surfaces. Taking into account these new findings a comprehensive explanation of the activation sequence along the spinal cord and the electric organ is proposed.

Postsynaptic distribution of acetylcholine receptors in electroplax of the torpedine ray, Narcine brasiliensis.

Other investigations have shown that many postsynaptic membranes which contain high densities of the nicotinic acetylcholine receptor appear to be unusually thick in electron micrographs. This peculiarity is believed to arise in part from the receptor protein itself. We show that in electroplax of Narcine brasiliensis, the thick membrane is found in juxtaneural postsynaptic regions, but not in deeper portions of junctional fold-like postsynaptic papillae or in extrasynaptic regions of the innervated face. Autoradiographic localization of receptor-bound [125I]alpha-bungarotoxin confirms that high densities of receptor are confined to juxtaneural regions. Narcine electric tissue thus provides a system for biochemical study of an acetylcholine receptor localization similar to that found at the mammalian or amphibian neuromuscular junction. Limited data suggest that similar postsynaptic distributions of receptor also occur in electroplax of several species of Torpedo.

Scanning electron microscopy of the electric tissue of Narcine brasiliensis.

The anatomy of electroplaques of Narcine brasiliensis has been studied by scanning electron microscopy. The ventral faces of the plaques are innervated with an abundance of branching nerves in close contact with the underlying (postsynaptic) membrane. Large numbers of troughs and evaginations of the postsynaptic membrane serve to increase its surface area. Fibroblasts are closely associated with the dorsal faces which appear covered with a matrix of fibrous material. Well-washed dorsal surfaces of single electroplaques are free of this matrix. The dorsal surface area is considerably increased by tubules extending into, and projections out of, the surface.