Electric Organ Research Articles

The effect of extracellular potassium concentration on the oscillation frequency of the pacemaker nucleus in the weakly electric fish Apteronotus leptorhynchus.

The weakly electric brown ghost knifefish (Apteronotus leptorhynchus) exhibits a pronounced sexual dimorphism in its electric behavior-males discharge at higher frequencies than females, with little overlap between the sexes. The frequency of these electric organ discharges is controlled by the frequency of the synchronized oscillations of the medullary pacemaker nucleus. Previous studies have suggested that sex-specific differences in the morphology and gene expression pattern of the astrocytic syncytium that envelopes the pacemaking neural network cause differences in its capacity to buffer the extracellular concentration of K+. This change in the K+ buffering capacity affects the K+ equilibrium potential of the neurons constituting the neural network, which in turn modulates the frequency of the pacemaker nucleus. In the present study, we have tested a critical element of this hypothesis by examining whether, and how, changes in the extracellular K+ concentration influence the frequency of the pacemaker nucleus oscillations. By using an in vitro preparation of the pacemaker nucleus, the results of this investigation demonstrate that exposure of this nucleus to acutely increased/decreased concentrations of K+ in the perfusate (while maintaining osmolarity) leads to concentration-dependent increases/decreases in the frequency of the synchronized oscillations generated by the pacemaker nucleus.

Species variation in steroid hormone-related gene expression contributes to species diversity in sexually dimorphic communication in electric fishes

Sexually dimorphic behaviors are often regulated by gonadal steroid hormones. Species diversity in behavioral sex differences may arise as expression of genes mediating steroid action in brain regions controlling these behaviors evolves. The electric communication signals of apteronotid knifefishes are an excellent model for comparatively studying neuroendocrine regulation of sexually dimorphic behavior. These fish produce and detect weak electric organ discharges (EODs) for electrolocation and communication. EOD frequency (EODf), controlled by the medullary pacemaker nucleus (Pn), is sexually dimorphic and regulated by androgens and estrogens in some species, but is sexually monomorphic and unaffected by hormones in other species. We quantified expression of genes for steroid receptors, metabolizing enzymes, and cofactors in the Pn of two species with sexually dimorphic EODf (Apteronotus albifrons and Apteronotus leptorhynchus) and two species with sexually monomorphic EODf (“Apteronotus” bonapartii and Parapteronotus hasemani). The “A.” bonapartii Pn expressed lower levels of androgen receptor (AR) genes than the Pn of species with sexually dimorphic EODf. In contrast, the P. hasemani Pn robustly expressed AR genes, but expressed lower levels of genes for 5α-reductases, which convert androgens to more potent metabolites, and higher levels of genes for 17β-hydroxysteroid dehydrogenases that oxidize androgens and estrogens to less potent forms. These findings suggest that sexual monomorphism of EODf arose convergently via two different mechanisms. In “A.” bonapartii, reduced Pn expression of ARs likely results in insensitivity of EODf to androgens, whereas in P. hasemani, gonadal steroids may be metabolically inactivated in the Pn, reducing their potential to influence EODf.

Large-area, self-healing block copolymer membranes for energy conversion

Membranes are widely used for separation processes in applications such as water desalination, batteries and dialysis, and are crucial in key sectors of our economy and society1. The majority of technologically exploited membranes are based on solid polymers and function as passive barriers, whose transport characteristics are governed by their chemical composition and nanostructure. Although such membranes are ubiquitous, it has proved challenging to maximize selectivity and permeability independently, leading to trade-offs between these pertinent characteristics2. Self-assembled biological membranes, in which barrier and transport functions are decoupled3,4, provide the inspiration to address this problem5,6. Here we introduce a self-assembly strategy that uses the interface of an aqueous two-phase system to template and stabilize molecularly thin (approximately 35 nm) biomimetic block copolymer bilayers of scalable area that can exceed 10 cm2 without defects. These membranes are self-healing, and their barrier function against the passage of ions (specific resistance of approximately 1 MΩ cm2) approaches that of phospholipid membranes. The fluidity of these membranes enables straightforward functionalization with molecular carriers that shuttle potassium ions down a concentration gradient with exquisite selectivity over sodium ions. This ion selectivity enables the generation of electric power from equimolar solutions of NaCl and KCl in devices that mimic the electric organ of electric rays.

Electrosensory and metabolic responses of weakly electric fish to changing water conductivity.

Weakly electric gymnotiform fishes use self-generated electric organ discharges (EODs) to navigate and communicate. The electrosensory range for these processes is a function of EOD amplitude, determined by the fish's electric organ (EO) output and the electrical conductivity of the surrounding water. Anthropogenic activity, such as deforestation, dams and industrial/agricultural runoff, are known to increase water conductivity in neotropical habitats, likely reducing the electrosensory range of these fish. We investigated whether fish modulate EO output as means of re-expanding electrosensory range after a rapid increase in water conductivity in the pulse-type Brachyhypopomus gauderio and the wave-type Eigenmannia virescens. Furthermore, because EOD production incurs significant metabolic costs, we assessed whether such compensation is associated with an increase in metabolic rate. Following the conductivity increase, B. gauderio increased EOD amplitude by 20.2±4.3% over 6days but with no associated increase in metabolic rate, whereas the EOD amplitude of E. virescens remained constant, accompanied by an unexpected decrease in metabolic rate. Our results suggest that B. gauderio uses a compensation mechanism that requires no metabolic investment, such as impedance matching, or a physiological trade-off wherein energy is diverted from other physiological processes to increase EO output. These divergent responses between species could be the result of differences in reproductive life history or evolutionary adaptations to different aquatic habitats. Continued investigation of electrosensory responses to changing water conditions will be essential for understanding the effects of anthropogenic disturbances on gymnotiforms, and potential physiological mechanisms for adapting to a rapidly changing aquatic environment.

The effect of current collectors on polymer-based energy-generating units inspired by the electric organs of eels

Bioinspired energy generation systems, particularly focusing on replicating the electrocytes, which are the cells of electric discharging organs of electric eels, have attracted much attention for battery cell development. Motivated by this trend, this study explores the effects of different current collectors (Au, Cu, Ni foils, and multilayer graphene-coated Ni foam) on the cell performance and open-circuit potentials of bioinspired energy-generating units. The results indicate that asymmetric current collectors, particularly the Cu-cell-Al configurations, yielded higher open circuit voltages and more stable power outputs over extended cycles. A polymer-based stacked energy unit between nickel current collectors achieved a high open circuit voltage of 230 mV and had a 75 % capacity decrease after 500 cycles. The developed devices, especially with asymmetric current collectors, provided a promising energy density (6541μWh.cm−2) and power density (50 mW.cm−2) while maintaining stability over thousands of cycles. In conclusion, flexible energy-generating units with potential applications in long-term energy needs were proposed in this study by incorporating electrochemical interactions to enhance the power output.

Characterization of the agonistic behavior of the weakly electric fish Gymnotus sylvius

AbstractElectric fish are good models in neuroethology as any behavior in electric fish involves both locomotor and electrical displays, which are experimentally accessible and controlled by well‐known neural circuits. The agonistic behavior within the genus Gymnotus has been evaluated in Gymnotus carapo and Gymnotus omarorum, providing an advantageous model system to address comparative analyses. Gymnotus sylvius is a weakly electric fish which occurs in sympatry with G. omarorum in freshwater environments of Argentina. Here, we describe the agonistic behavior of G. sylvius in laboratory conditions. All dyads engaged in intense fights, with a latency to the first attack of 8 ± 7.8 s and a contest phase of 42.71 ± 31.7 s. Individual initiative in the first attack predicted contest outcome with no apparent influence of body weight asymmetry between contenders. Contenders did not escalate in their aggression during the short contest; in turn, subordinates tended to retreat in response to dominants' attacks. Submission and dominance were expressed by electric signals: dominants increased their basal electric organ discharge (EOD) rate after contest resolution, resulting in a persistent EOD rate rank. Subordinates also emitted chirps and offs during the contest and post‐resolution phases without a clear temporal pattern. The agonistic behavior of G. sylvius presents some similarities with other species of the genus Gymnotus: EOD rank between dominants and subordinates, electric signals of submission, and the presence of attacks in the post‐resolution phase. On the other hand, it also presents differences: a shorter evaluation phase in G. sylvius, initiative as a determinant of outcome, a higher attack rate of dominants in G. sylvius, a different temporal pattern of chirps, and different mechanisms to separate EOD rate of dominants and subordinates. These facts open a promising road to analyze the evolution of different neuroendocrine strategies, operating on homologous neural pathways, to command the same behavior.

Elucidation of Rapid Synchronization on Electric Discharge by Use of Model Cell Systems Mimicking Electric Organs of Electric Eel

Elucidation of Rapid Synchronization on Electric Discharge by Use of Model Cell Systems Mimicking Electric Organs of Electric Eel

Gene and Allele-Specific Expression Underlying the Electric Signal Divergence in African Weakly Electric Fish.

In the African weakly electric fish genus Campylomormyrus, electric organ discharge signals are strikingly different in shape and duration among closely related species, contribute to prezygotic isolation, and may have triggered an adaptive radiation. We performed mRNA sequencing on electric organs and skeletal muscles (from which the electric organs derive) from 3 species with short (0.4 ms), medium (5 ms), and long (40 ms) electric organ discharges and 2 different cross-species hybrids. We identified 1,444 upregulated genes in electric organ shared by all 5 species/hybrid cohorts, rendering them candidate genes for electric organ-specific properties in Campylomormyrus. We further identified several candidate genes, including KCNJ2 and KLF5, and their upregulation may contribute to increased electric organ discharge duration. Hybrids between a short (Campylomormyrus compressirostris) and a long (Campylomormyrus rhynchophorus) discharging species exhibit electric organ discharges of intermediate duration and showed imbalanced expression of KCNJ2 alleles, pointing toward a cis-regulatory difference at this locus, relative to electric organ discharge duration. KLF5 is a transcription factor potentially balancing potassium channel gene expression, a crucial process for the formation of an electric organ discharge. Unraveling the genetic basis of the species-specific modulation of the electric organ discharge in Campylomormyrus is crucial for understanding the adaptive radiation of this emerging model taxon of ecological (perhaps even sympatric) speciation.

Ecologically mediated differences in electric organ discharge drive evolution in a sodium channel gene in South American electric fishes.

Active electroreception-the ability to detect objects and communicate with conspecifics via the detection and generation of electric organ discharges (EODs)-has evolved convergently in several fish lineages. South American electric fishes (Gymnotiformes) are a highly species-rich group, possibly in part due to evolution of an electric organ (EO) that can produce diverse EODs. Neofunctionalization of a voltage-gated sodium channel gene accompanied the evolution of electrogenic tissue from muscle and resulted in a novel gene (scn4aa) uniquely expressed in the EO. Here, we investigate the link between variation in scn4aa and differences in EOD waveform. We combine gymnotiform scn4aa sequences encoding the C-terminus of the Nav1.4a protein, with biogeographic data and EOD recordings to test whether physiological transitions among EOD types accompany differential selection pressures on scn4aa. We found positive selection on scn4aa coincided with shifts in EOD types. Species that evolved in the absence of predators, which likely selected for reduced EOD complexity, exhibited increased scn4aa evolutionary rates. We model mutations in the protein that may underlie changes in protein function and discuss our findings in the context of gymnotiform signalling ecology. Together, this work sheds light on the selective forces underpinning major evolutionary transitions in electric signal production.

Diet in phenotypically divergent sympatric species of African weakly electric fish (genus: Campylomormyrus)-A hybrid capture/HTS metabarcoding approach.

Ecological speciation within the mormyrid genus Campylomormyrus resulted in sympatric species exhibiting divergence in their feeding apparatus and electric organ discharge (EOD). This study documents the overall diet of the genus Campylomormyrus and examines the hypothesis that the Campylomormyrus radiation is caused by adaptation to different food sources. We performed diet assessment of five sympatric Campylomormyrus species (C. alces, C. compressirostris, C. curvirostris, C. tshokwe, C. numenius) and their sister taxon Gnathonemus petersii with markedly different snout morphologies and EODs using hybrid capture/HTS DNA metabarcoding of their stomach contents. Our approach allowed for high taxonomic resolution of prey items, including benthic invertebrates, allochthonous invertebrates and vegetation. Comparisons of the diet compositions using quantitative measures and diet overlap indices revealed that all species are able to exploit multiple food niches in their habitats, that is fauna at the bottom, the water surface and the water column. A major part of the diet is larvae of aquatic insects, such as dipterans, coleopterans and trichopterans, known to occur in holes and interstitial spaces of the substrate. The results indicate that different snout morphologies and the associated divergence in the EOD could translate into different prey spectra. This suggests that the diversification in EOD and/or morphology of the feeding apparatus could be under functional adaptation.

A chromosome-level genome of electric catfish (Malapterurus electricus) provided new insights into order Siluriformes evolution.

The online version contains supplementary material available at 10.1007/s42995-023-00197-8.

Electric organ discharge from electric eel facilitates DNA transformation into teleost larvae in laboratory conditions

Background Electric eels (Electrophorus sp.) are known for their ability to produce electric organ discharge (EOD) reaching voltages of up to 860 V. Given that gene transfer via intense electrical pulses is a well-established technique in genetic engineering, we hypothesized that electric eels could potentially function as a gene transfer mechanism in their aquatic environment. Methods To investigate this hypothesis, we immersed zebrafish larvae in water containing DNA encoding the green fluorescent protein (GFP) and exposed them to electric eel’s EOD. Results and Discussion Some embryos exhibited a mosaic expression of green fluorescence, in contrast to the control group without electrical stimulation, which showed little distinct fluorescence. This suggests that electric eel EOD has the potential to function as an electroporator for the transfer of DNA into eukaryotic cells. While electric eel EOD is primarily associated with behaviors related to sensing, predation, and defense, it may incidentally serve as a possible mechanism for gene transfer in natural environment. This investigation represents the initial exploration of the uncharted impact of electric eel EOD, but it does not directly establish its significance within the natural environment. Further research is required to understand the ecological implications of this phenomenon.

The effect of eugenol anesthesia on the electric organ discharge of the weakly electric fish Apteronotus leptorhynchus

Eugenol, the major active ingredient of clove oil, is widely used for anesthesia in fish. Yet virtually nothing is known about its effects on CNS functions, and thus about potential interference with neurophysiological experimentation. To address this issue, we employed a neuro-behavioral assay recently developed for testing of water-soluble anesthetic agents. The unique feature of this in-vivo tool is that it utilizes a readily accessible behavior, the electric organ discharge (EOD), as a proxy of the neural activity generated by a brainstem oscillator, the pacemaker nucleus, in the weakly electric fish Apteronotus leptorhynchus. A deep state of anesthesia, as assessed by the cessation of locomotor activity, was induced within less than 3 min at concentrations of 30–60 µL/L eugenol. This change in locomotor activity was paralleled by a dose-dependent, pronounced decrease in EOD frequency. After removal of the fish from the anesthetic solution, the frequency returned to baseline levels within 30 min. Eugenol also led to a significant increase in the rate of ‘chirps,’ specific amplitude/frequency modulations of the EOD, during the 30 min after the fish’s exposure to the anesthetic. At 60 µL/L, eugenol induced a collapse of the EOD amplitude after about 3.5 min in half of the fish tested. The results of our study indicate strong effects of eugenol on CNS functions. We hypothesize that these effects are mediated by the established pharmacological activity of eugenol to block the generation of action potentials and to reduce the excitability of neurons; as well as to potentiate GABAA-receptor responses.

Electric Eel‐Inspired Soft Electrocytes for Solid‐State Power Systems

AbstractAs the demand for power systems, including portable ones, is growing at an ever‐faster pace, many studies are approaching to discover innovative materials for current battery technology or replace the existing ones with new systems through mimicking living things or nature. Here, a soft, solid‐state power storage system featuring electric eel‐inspired artificial electric organs capable of converting the chemical potential of an ionic gradient into electricity is introduced. These organs are constructed through the assembly of low and high ion‐concentrated zwitterionic gel films with cation‐ and anion‐selective intermembranes, which generate a rechargeable open‐circuit voltage of ≈135 mV. Combined use of a chemically synthesized room‐temperature ionic liquid and a high‐boiling point organic solvent as ion‐conducting electrolyte allows electric organs to withstand extreme temperatures ranging from −20 and 100 °C, while the thin and stretchable constituent layers facilitate mechanical flexibility without compromising electrical performance. Scalable integration of electric organs in series and parallel configurations achieves high levels of voltage and current outputs, and employment of origami folding geometry enables on‐demand discharge upon self‐registered folding, paving the way for portable, high‐voltage energy sources in the fields of wearable electronics and soft robotics.

Supervised learning algorithm for analysis of communication signals in the weakly electric fish Apteronotus leptorhynchus

Signal analysis plays a preeminent role in neuroethological research. Traditionally, signal identification has been based on pre-defined signal (sub-)types, thus being subject to the investigator’s bias. To address this deficiency, we have developed a supervised learning algorithm for the detection of subtypes of chirps—frequency/amplitude modulations of the electric organ discharge that are generated predominantly during electric interactions of individuals of the weakly electric fish Apteronotus leptorhynchus. This machine learning paradigm can learn, from a ‘ground truth’ data set, a function that assigns proper outputs (here: time instances of chirps and associated chirp types) to inputs (here: time-series frequency and amplitude data). By employing this artificial intelligence approach, we have validated previous classifications of chirps into different types and shown that further differentiation into subtypes is possible. This demonstration of its superiority compared to traditional methods might serve as proof-of-principle of the suitability of the supervised machine learning paradigm for a broad range of signals to be analyzed in neuroethology.

The sensory effects of light on the electric organ discharge rate of Gymnotus omarorum.

Gymnotiformes are nocturnal fishes inhabiting the root mats of floating plants. They use their electric organ discharge (EOD) to explore the environment and to communicate. Here, we show and describe tonic and phasic sensory-electromotor responses to light distinct from indirect effects depending on the light-induced endogenous circadian rhythm. In the dark, principally during the night, inter-EOD interval histograms are bimodal: the main peak corresponds to the basal rate and a secondary peak corresponds to high-frequency bouts. Light causes a twofold tonic but opposing effect on the EOD histogram: (i) decreasing the main mode and (ii) blocking the high-frequency bouts and consequently increasing the main peak at the expense of removal of the secondary one. Additionally, light evokes phasic responses whose amplitude increases with intensity but whose slow time course and poor adaptation differentiate from the so-called novelty responses evoked by abrupt changes in sensory stimuli of other modalities. We confirmed that Gymnotus omarorum tends to escape from light, suggesting that these phasic responses are probably part of a global 'light-avoidance response'. We interpret the data within an ecological context. Fish rest under the shade of aquatic plants during the day and light spots due to the sun's relative movement alert the fish to hide in shady zones to avoid macroptic predators and facilitate tracking the movement of floating plant islands by wind and/or water currents.

Bidirectional Jump Point Search Path-Planning Algorithm Based on Electricity-Guided Navigation Behavior of Electric Eels and Map Preprocessing.

The electric eel has an organ made up of hundreds of electrocytes, which is called the electric organ. This organ is used to sense and detect weak electric field signals. By sensing electric field signals, the electric eel can identify changes in their surroundings, detect potential prey or other electric eels, and use it for navigation and orientation. Path-finding algorithms are currently facing optimality challenges such as the shortest path, shortest time, and minimum memory overhead. In order to improve the search performance of a traditional A* algorithm, this paper proposes a bidirectional jump point search algorithm (BJPS+) based on the electricity-guided navigation behavior of electric eels and map preprocessing. Firstly, a heuristic strategy based on the electrically induced navigation behavior of electric eels is proposed to speed up the node search. Secondly, an improved jump point search strategy is proposed to reduce the complexity of jump point screening. Then, a new map preprocessing strategy is proposed to construct the relationship between map nodes. Finally, path planning is performed based on the processed map information. In addition, a rewiring strategy is proposed to reduce the number of path inflection points and path length. The simulation results show that the proposed BJPS+ algorithm can generate optimal paths quickly and with less search time when the map is known.

Ontogeny reveals the origin of Gemminger bones in Mormyridae.

Mormyridae are well known and intensively studied for their weak electric organ discharges, which facilitate communication and orientation. The Gemminger bones of Mormyridae are located next to the electrical organ in the caudal peduncle; however, they have not attracted much interest until recently. Therefore, we investigated the diversity of Gemminger bones in mormyrids and studied their ontogenetic development in Mormyrus rume proboscirostris. Gemminger bones are paired, thin, elongated ossifications lying on the dorsal and ventral sides of the caudal peduncle, and usually reach anterior well below the dorsal and anal fin bases. Ontogeny revealed that they are not intermuscular ossifications, as suspected based on the anatomical position of this structure and the systematic position of the mormyrids. Instead, they are membrane ossifications that originate from the fin stays of the dorsal and anal fins.

Hormonal coordination of motor output and internal prediction of sensory consequences in an electric fish

Steroid hormones remodel neural networks to induce seasonal or developmental changes in behavior. Hormonal changes in behavior likely require coordinated changes in sensorimotor integration. Here, we investigate hormonal effects on a predictive motor signal, termed corollary discharge, that modulates sensory processing in weakly electric mormyrid fish. In the electrosensory pathway mediating communication behavior, inhibition activated by a corollary discharge blocks sensory responses to self-generated electric pulses, allowing the downstream circuit to selectively analyze communication signals from nearby fish. These pulses are elongated by increasing testosterone levels in males during the breeding season. We induced electric-pulse elongation using testosterone treatment and found that the timing of electroreceptor responses to self-generated pulses was delayed as electric-pulse duration increased. Simultaneous recordings from an electrosensory nucleus and electromotor neurons revealed that the timing of corollary discharge inhibition was delayed and elongated by testosterone. Furthermore, this shift in the timing of corollary discharge inhibition was precisely matched to the shift in timing of receptor responses to self-generated pulses. We then asked whether the shift in inhibition timing was caused by direct action of testosterone on the corollary discharge circuit or by plasticity acting on the circuit in response to altered sensory feedback. We surgically silenced the electric organ of fish and found similar hormonal modulation of corollary discharge timing between intact and silent fish, suggesting that sensory feedback was not required for this shift. Our findings demonstrate that testosterone directly regulates motor output and internal prediction of the resulting sensory consequences in a coordinated manner.

From Peptides to Receptors

—In the 1960s and 1970s, the Institute of Chemistry of Natural Compounds developed a topochemical approach for designing new biologically active peptide compounds, the applicability of which to the creation of inhibitors and effective substrates of proteolytic enzymes was shown by the author of this review under the direct supervision of V.T. Ivanov. The next task was to establish the conformation of protein neurotoxins from snake venoms and to study the topography of their binding to the target, the nicotinic acetylcholine receptor (nAChR) from the electric organ of the Torpedo marmorata ray. With selectively labeled derivatives containing one fluorescent or spin label on established amino acid residues, neurotoxin residues in contact with nAChR were identified for the first time. Later, in collaboration with the laboratory of V.T. Ivanov, new analogs of α-conotoxins (peptide neurotoxins from venomous Conus mollusks), were synthesized including their photoactivated derivatives, which showed the participation of all Torpedo nAChR subunits in the binding of α-conotoxins. In the final part, the review briefly presents the recent achievements of the Department of Molecular Neuroimmune Signaling (headed by V.I. Tsetlin) concerning the isolation and synthesis of new peptide and protein neurotoxins and the study of how they work.