Electric Organ Research Articles

Glia-mediated modulation of extracellular potassium concentration determines the sexually dimorphic output frequency of a model brainstem oscillator

Sexual dimorphism in behavior is widespread among animals, but the cellular mechanisms underlying neural control of this phenomenon are largely unknown. One behavior that has provided some important clues about how such sex differences might develop is the electric organ discharge of Apteronotus leptorhynchus. In this weakly electric fish, the mean discharge frequencies of males and females are 880 Hz and 740 Hz, respectively, with little overlap of the two frequency bands. The discharges are controlled, in a one-to-one fashion, by the neural oscillations of the pacemaker nucleus in the medulla oblongata. Experimental evidence has shown that the astrocytic syncytium associated with the neural network that generates these oscillations is significantly larger, and stronger coupled via gap junctions, in females than in males. In the present study, modeling of this network was performed to test the hypotheses that the sex-dependent differences in the structure and properties of the astrocytic syncytium mediate better buffering of extracellular potassium in females than in males, which in turn causes, via a lowering of the potassium equilibrium potential, a decrease in the oscillation frequency. Simulations of the neural activity of the pacemaker nucleus and its individual components demonstrated that under both spontaneous and induced conditions the oscillation frequency and the potassium equilibrium potential are strongly positively correlated. These simulations predict that sufficient separation of the electric organ discharge frequencies for establishment of the sexual dimorphism can be achieved by rather minor alterations in the concentration of the extracellular potassium concentration in the pacemaker nucleus.

Electroreception, electrogenesis and electric signal evolution.

Electroreception, the capacity to detect external underwater electric fields with specialised receptors, is a phylogenetically widespread sensory modality in fishes and amphibians. In passive electroreception, a capacity possessed by c. 16% of fish species, an animal uses low-frequency-tuned ampullary electroreceptors to detect microvolt-range bioelectric fields from prey, without the need to generate its own electric field. In active electroreception (electrolocation), which occurs only in the teleost lineages Mormyroidea and Gymnotiformes, an animal senses its surroundings by generating a weak (< 1 V) electric-organ discharge (EOD) and detecting distortions in the EOD-associated field using high-frequency-tuned tuberous electroreceptors. Tuberous electroreceptors also detect the EODs of neighbouring fishes, facilitating electrocommunication. Several other groups of elasmobranchs and teleosts generate weak (< 10 V) or strong (> 50 V) EODs that facilitate communication or predation, but not electrolocation. Approximately 1.5% of fish species possess electric organs. This review has two aims. First, to synthesise our knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and with emphasis on the proximate (morphological, physiological and genetic) bases of EOD and electroreceptor diversity. Second, to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms and to explore the ultimate (evolutionary) bases of signal and receptor diversity in their convergent electrogenic-electrosensory systems. Four sets of potential drivers or moderators of signal diversity are discussed. First, selective forces of an abiotic (environmental) nature for optimal electrolocation and communication performance of the EOD. Second, selective forces of a biotic nature targeting the communication function of the EOD, including sexual selection, reproductive interference from syntopic heterospecifics and selection from eavesdropping predators. Third, non-adaptive drift and, finally, phylogenetic inertia, which may arise from stabilising selection for optimal signal-receptor matching.

Stem-Cell-Driven Growth and Regrowth of the Adult Spinal Cord in Teleost Fish.

The spinal cord of the teleost fish Apteronotus leptorhynchus continues to grow during adulthood, in concert with the overall body growth. Immunohistological studies, combined with mathematical modeling, suggest that this growth is driven by proliferative activity of Sox2-expressing stem/progenitor cells (SPCs) and by cell drift due to population pressure. The SPCs exhibit high volumetric density in the caudal filament and the ependymal layer. Nevertheless, the majority of these cells are found in the parenchyma throughout the rostro-caudal axis of the spinal cord, albeit at much lower volumetric densities than in the ependymal layer. The SPCs give rise, via transit-amplifying cells, to neurons and glia. The relative number of neurons and glia is primarily regulated through apoptosis of supernumerary neurons. Quantitative analysis has demonstrated that the continued cell proliferation results in additive neurogenesis. This addition includes adult-born spinal electromotoneurons, thereby resulting in a continuous increase in the amplitude of the fish's electric organ discharge during adult life. Amputation of the caudal part of the spinal cord induces initially a degenerative response, dominated by massive apoptotic cell death in spinal cord tissue immediately rostral to the injury site, and distinguished by a partial loss of the electric organ discharge amplitude. This phase is followed by a regenerative response, characterized by absence of gliosis and by rapid stem-cell-driven tissue regrowth. Although the quality of the regenerated tissue is variable among individuals, the structural repair has led in every fish examined thus far to full recovery of the electric organ discharge amplitude.

Molecular phylogeny of the ghost knifefishes (Gymnotiformes: Apteronotidae)

Ghost knifefishes (Gymnotiformes: Apteronotidae) are weakly electric fishes that possess a high-frequency, neurogenic electric organ discharge. They are found throughout the humid Neotropics from Panama to Argentina and are most diverse and abundant in the channels of large lowland rivers. Apteronotidae is the most species-rich family of Neotropical electric knifefishes with 96 valid species in 15 genera. We present a phylogenetic hypothesis based on molecular sequence data from three mitochondrial genes (16S, coi, cytb) and four nuclear loci (glyt, rag2, ryr3, zic1). Our analysis includes sequence data for 203 samples in 54 species and 14 genera, making it the most densely-sampled and data-rich phylogeny of the Apteronotidae to date. Our results corroborate previous phylogenetic hypotheses with the placement of Orthosternarchus + Sternarchorhamphus sister to all other apteronotids, a non-monophyletic Apterontotus, and a sister relationship between Sternarchorhynchus and the Navajini. We also report several novel relationships, particularly within the Navajini and among several species of the nominal genus Apteronotus not previously included in phylogenetic analyses. We additionally provide a new classification for the family.

Organic Bio-Electronics: Bridging The Gap Between Natural and Artificial Materials for Bio-Electronics Applications

This paper aims to review current research and advancement in technology in organic bioelectronics and to reinvestigate the relationship between organic bioelectronics materials, properties, and application. A comprehensive literature review on organic bioelectronics and its dependent variables created a theoretical foundation for the paper. Using the review-centric theory, a model was developed and presented to encapsulate highly dynamic interaction of organic bioelectronics, synthetic and natural material sources that can be employed in present innovations and its implications on modern technologies. The model highlights the relationship between organic bioelectronics and its four main drivers namely, synthetic material (Piezoelectric energy harvesters), natural materials (electric organs), application (bio-devices, sensors, nanogenerators) and properties. Limitations to this research include; availability of raw materials in appropriate amounts, problems associated with interfacing natural with synthetic materials, maintenance of bioelectronics devices in living organisms and design methods for a variety of specific devices. The empirical data is limited to 4 dependent variables which do not present a conclusive theory about organic bioelectronics. In this review, we explored the possibility of interfacing synthetic material (PVDF) and a natural material (electric organ of Electrophorus electricus) by reviewing their properties, fabrication methods to create a composite that has application in a variety of bioelectronics devices.

Organic Bio-Electronics: Bridging The Gap Between Natural and Artificial Materials for Bio-Electronics Applications

This paper aims to review current research and advancement in technology in organic bioelectronics and to reinvestigate the relationship between organic bioelectronics materials, properties, and application. A comprehensive literature review on organic bioelectronics and its dependent variables created a theoretical foundation for the paper. Using the review-centric theory, a model was developed and presented to encapsulate highly dynamic interaction of organic bioelectronics, synthetic and natural material sources that can be employed in present innovations and its implications on modern technologies. The model highlights the relationship between organic bioelectronics and its four main drivers namely, synthetic material (Piezoelectric energy harvesters), natural materials (electric organs), application (bio-devices, sensors, nanogenerators) and properties. Limitations to this research include; availability of raw materials in appropriate amounts, problems associated with interfacing natural with synthetic materials, maintenance of bioelectronics devices in living organisms and design methods for a variety of specific devices. The empirical data is limited to 4 dependent variables which do not present a conclusive theory about organic bioelectronics. In this review, we explored the possibility of interfacing synthetic material (PVDF) and a natural material (electric organ of Electrophorus electricus) by reviewing their properties, fabrication methods to create a composite that has application in a variety of bioelectronics devices.

Neuronal Dynamics Underlying Communication Signals in a Weakly Electric Fish: Implications for Connectivity in a Pacemaker Network

Neuronal networks can produce stable oscillations and synchrony that are under tight control yet flexible enough to rapidly switch between dynamical states. The pacemaker nucleus in the weakly electric fish comprises a network of electrically coupled neurons that fire synchronously at high frequency. This activity sets the timing for an oscillating electric organ discharge with the lowest cycle-to-cycle variability of all known biological oscillators. Despite this high temporal precision, pacemaker activity is behaviorally modulated on millisecond time-scales for the generation of electrocommunication signals. The network mechanisms that allow for this combination of stability and flexibility are not well understood. In this study, we use an in vitro pacemaker preparation from Apteronotus leptorhynchus to characterize the neural responses elicited by the synaptic inputs underlying electrocommunication. These responses involve a variable increase in firing frequency and a prominent desynchronization of neurons that recovers within 5 oscillation cycles. Using a previously developed computational model of the pacemaker network, we show that the frequency changes and rapid resynchronization observed experimentally are most easily explained when model neurons are interconnected more densely and with higher coupling strengths than suggested by published data. We suggest that the pacemaker network achieves both stability and flexibility by balancing coupling strength with interconnectivity and that variation in these network features may provide a substrate for species-specific evolution of electrocommunication signals.

Representation of object's shape by multiple electric images in electrolocation.

Weakly electric fish generate an electric field by discharging an electric organ located on the tail region. An object near the fish modulates the self-generated electric field. The modulated field enables the fish to perceive objects even in complete darkness. The ability to perceive objects is provided by the electrosensory system of the fish. Electroreceptors distributed on the fish's skin surface can sense the modulated field, on the basis of transdermal voltage across the skin surface, called electric images. The fish can extract object's features such as lateral distance, size, shape, and electric property from an electric image. Although previous studies have demonstrated the relationship between electric-image features and object's distance and size, it remains unclear what features of an electric image represent the object's shape. We make here a hypothesis that shape information is not represented by a single image but by multiple images caused by the object's rotation or fish movement around the object. To test the hypothesis, we develop a computational model that can predict electric images produced by the rotation of differently shaped objects. We used five different shapes of resistive objects: a circle, a square, an equilateral triangle, a rectangle, and an ellipsoid. We show that differently shaped objects of a fixed arrangement generate similar Gaussian electric images, irrespective of their shapes. We also show that the features of an electric image such as the peak amplitude, half-maximum width, and peak position exhibit the angle-dependent variations characteristic to object rotation, depending on object shapes and lateral distances. Furthermore, we demonstrate that an integration effect of the peak amplitude and half-maximum width could be an invariant measure of object shape. These results suggest that the fish could perceive an object shape by combining those image features produced during exploratory behaviors around the object.

Spatial and temporal distribution of Gymnorhamphichthys rondoni (Gymnotiformes: Rhamphichthyidae) in a long-term study of an Amazonian terra firme stream, Leticia - Colombia

ABSTRACT Weakly electric fishes continually emit electric organ discharges (EOD) as a means of communication and localization of objects in their surroundings. Depending on water conductivity, the amplitude of the electric field generated is known to increase with decreases in electrical conductivity of the water. In Amazonian terra firme streams, water conductivity is extremely low and fluctuates constantly due to local and regional rains. In this context, the space between freely moving weakly electric fishes may be expected to decrease, on average, with an increase in water conductivity. To test this hypothesis, we recorded the positions at rest of the sand-dwelling fish Gymnorhamphichthys rondoni in a terra firme stream for several days in alternating months, over two years. Based on daily nearest neighbor distances among individual fish in a grid, we found a uniform temporal distribution pattern (which was not affected by water conductivity) indicative of site fidelity. Here we highlight the role of other factors that could influence resting site fidelity.

Distinctive mechanisms underlie the emission of social electric signals of submission in Gymnotus omarorum.

South American weakly electric fish (order Gymnotiformes) rely on a highly conserved and relatively fixed electromotor circuit to produce species-specific electric organ discharges (EODs) and a variety of meaningful adaptive EOD modulations. The command for each EOD arises from a medullary pacemaker nucleus composed of electrotonically coupled intrinsic pacemaker and bulbospinal projecting relay cells. During agonistic encounters, Gymnotus omarorum signals submission by interrupting its EOD (offs) and emitting transient high-rate barrages of low-amplitude discharges (chirps). Previous studies in Gymnotiformes have shown that electric signal diversity is based on the segregation of descending synaptic inputs to pacemaker or relay cells and differential activation of the neurotransmitter receptors -for glutamate or γ-aminobutyric acid (GABA) - of these cells. Therefore, we tested whether GABAergic and glutamatergic inputs to pacemaker nucleus neurons are involved in the emission of submissive electric signals in G. omarorum We found that GABA applied to pacemaker cells evokes EOD interruptions that closely resemble natural offs. Although in other species chirping is probably due to glutamatergic suprathreshold depolarization of relay cells, here, application of glutamate to these cells was unable to replicate the emission of this submissive signal. Nevertheless, chirp-like discharges were emitted after the enhancement of excitability of relay cells by blocking an IA-type potassium current and, in some cases, by application of vasotocin, a status-dependent modulator peptide of G. omarorum agonistic behavior. Modulation of the electrophysiological properties of pacemaker nucleus neurons in Gymnotiformes emerges as a novel putative mechanism endowing electromotor networks with higher functional versatility.

A new and improved electric fish finder with resources for printed circuit board fabrication

ABSTRACT We describe the circuit design, construction, and operation of a field-portable electric fish finder (an AC-coupled wide-band differential bio-amplifier with loudspeaker output). This device permits detection and monitoring of the electric organ discharges generated by neotropical gymnotiform fishes (as well as the mormyroid fishes of tropical Africa). Our design is modified from earlier versions to optimize detection performance and stability over a wider range of ambient water conductivity, including under conditions of extremely low conductivity (&lt; ca. 10 μScm-1). Our new electric fish finder design also incorporates complete waterproofing and longer battery autonomy. We provide Gerber and Eagle files made with the electronic design automation software ‘Autodesk Eagle’ to allow researchers to order printed circuit boards directly from commercial manufacturers.

Encoding phase spectrum for evaluating 'electric qualia'.

The most broadly expressed and studied aspect of sensory transduction is receptor tuning to the power spectral density of the incoming signals. Temporal cues expressed in the phase spectrum are relevant in African and American pulse-emitting electric fish showing electroreceptors sensing the signals carried by the self- and conspecific-generated electric organ discharges. This article concerns the role of electroreceptor phase sensitivity in American pulse Gymnotiformes. These fish show electroreceptors sharply tuned to narrow frequency bands. This led to the common thought that most electrosensory information is contained in the amplitude spectra of the signals. However, behavioral and modeling studies suggest that in their pulses, Gymnotiformes electroreceptors also encode cues embodied in the phase spectrum of natural stimuli. Here, we show that the two main types of tuberous primary afferents of Gymnotus omarorum differentially respond to cues embodied in the amplitude and phase spectra of self-generated electrosensory signals. One afferent type, pulse markers, is mainly driven by the amplitude spectrum, while the other, burst coders, is predominantly sensitive to the phase spectrum. This dual encoding strategy allows the fish to create a sensory manifold where patterns of 'electric color' generated by object impedance and other potential sources of 'colored' images (such as large nearby objects and other electric fish) can be represented.

Anatomy and homology of the accessory electric organs of the toothless knifefishes (Rhamphichthyoidea: Gymnotiformes).

We describe the anatomy and histology of the accessory electric organs of several knifefish taxa. Accessory electric organs are observed among Rhamphichthyoidea in the opercular, mental and humeral regions. Within this group, some species of Brachyhypopomus possess an accessory electric organ in the opercular region. Rhamphichthyinae and Steatogenys possess accessory electric organs in the mental region of the body that differs in many aspects, such as general electrocyte shape and its number of caudal ridges. Steatogenys, Hypopygus and Rhamphichthys possess an accessory electric organ in the humeral region that differs in position, electrocyte configuration and shape. Electrocytes of both humeral and mental accessory electric organs in Steatogenys share a number of common features (e.g., electrocyte shape and innervation pattern), which distinguishes them from the electric organs of related groups. Rhamphichthys has an accessory electric organ in the humeral (specifically subpectoral) region, which has not previously been reported in the literature and differs in arrangement and electrocyte shape from those previously described electric organs of other taxa. Homology of these accessory electric organs is discussed in the context of hypothesized relationships among rhamphichthyoid taxa, indicating that accessory electric organs originated multiple times with apparently no subsequent losses.

Mitogenomics of Central American weakly-electric fishes

Electric fishes are a diverse group of freshwater organisms with the ability to generate electric organ discharges (EODs) that are used for communication and electrolocation. This group (ca. 200 species) has originated in South America, and six species colonized the Central American Isthmus. Here, we assembled the complete mitochondrial genomes (mitogenomes) for three Central American electric fishes (i.e. Sternopygus dariensis, Brachyhypopomus occidentalis, and Apteronotus rostratus), and, based on these data, explored their phylogenetic position among Gymnotiformes. The three mitogenomes show the same gene order, as reported for other fishes, with a size ranging from 16,631 to 17,093 bp. We uncovered a novel 60 bp intergenic spacer (IGS) located between the COII and tRNALys genes, which appears to be unique to the Apteronotidae. Furthermore, phylogenetic relationships supported the traditional monophyly of Gymnotiformes, with the three species positioned within their respective family. In addition, the genus Apteronotus belongs to the early diverging lineage of the order. Finally, we found high sequence divergence (13%) between our B. occidentalis specimen and a sequence previously reported in GenBank, suggesting that the prior mitogenome of B. occidentalis represents a different South American species. Indeed, phylogenetic analyses using Cytochrome b gene across the genus placed the previously reported individual within B. bennetti. Our study provides novel mitogenome resources that will advance our understanding of the diversity and phylogenetic history of Neotropical fishes.

Jamming Avoidance Response Inspired by Wave-type Weakly Electric Fish

Weakly electric fish use the electric field to detect objects in the neighborhood or communicate with conspecifics. They generate electric field with their electric organ and the electroreceptors sense the distortion of electric field caused by nearby objects. They use a modulated frequency signal of the Electric Organ Discharge (EOD), and it can be disturbed by similar frequency signals that neighboring weakly electric fish emit. They have a particular behavior response to change their EOD frequencies to avoid signal jamming. It is called jamming avoidance response. Inspired by the behavior of wave-type weakly electric fish, we propose an engineering perspective of jamming avoidance response model with the amplitude-phase modulation graph. The time course of the amplitude-phase graph of the EOD signal provides a cue to detect the jamming signal. We argue that the temporal integration can determine the shift direction of the EOD as well as the amount of the frequency shift to be moved frequency for the jamming avoidance response. Alternatively, as a fast adapting measure, the cross product of point vectors in the amplitude-phase graph allows early decision for jamming avoidance. We demonstrate the methods with simulations and the real experiments in the underwater environment.

Harmonic and temporal structure of electric organ discharges of the wave-type in Amazonian knifefishes (Gymnotiformes)

Neotropical, nocturnal freshwater knifefishes of the families Sternopygidae and Apteronotidae are electroreceptive, and emit electric organ discharges (EODs) of the wave type for communication and active electrolocation. In a field-collected sample of an estimated 43 gymnotiform species, members of the former family displayed the same type of sinusoidal EOD waveform at frequencies of up to about 800 Hz, with the fundamental frequency, f1, the strongest harmonic in each. Members of the latter (Apteronotidae) displayed f1 frequencies of up to 1800 Hz, and a great diversity in EOD waveform. Apteronotid EODs often differed from those of sternopygids by more harmonics at stronger amplitudes, where f1 was not always the strongest harmonic. The frequency band at −10 dB increased with diminishing f1 amplitude. In contrast to apteronotids, all sternopygids showed the same phase relationship between their respective f1 and f2: a difference of an average 72°, which explains their single type of sinusoidal waveform. In apteronotids a great variety of phase relationships among harmonics was observed, in some their harmonics series cycled through 360° repeatedly. It is argued that the evolutionary driving force for the apteronotids — in contrast to sternopygids — was the greater potential for adaptive radiation.

The subtle art of electro-flirting in wild knifefish

![Graphic][1] What do James Brown and ghost knifefish ( Apteronotus ) have in common? They've both harnessed the power of electric organs in order to deliver declarations of adoration. As close relatives of the electric eel ( Electrophorus electricus ), it's probably not too shocking that

Electric pulse characteristics can enable species recognition in African weakly electric fish species

Communication is key to a wide variety of animal behaviours and multiple modalities are often involved in this exchange of information from sender to receiver. The communication of African weakly electric fish, however, is thought to be predominantly unimodal and is mediated by their electric sense, in which species-specific electric organ discharges (EODs) are generated in a context-dependent and thus variable sequence of pulse intervals (SPI). While the primary function of the electric sense is considered to be electrolocation, both of its components likely carry information regarding identity of the sender. However, a clear understanding of their contribution to species recognition is incomplete. We therefore analysed these two electrocommunication components (EOD waveform and SPI statistics) in two sympatric mormyrid Campylomormyrus species. In a set of five playback conditions, we further investigated which components may drive interspecific recognition and discrimination. While we found that both electrocommunication components are species-specific, the cues necessary for species recognition differ between the two species studied. While the EOD waveform and SPI were both necessary and sufficient for species recognition in C. compressirostris males, C. tamandua males apparently utilize other, non-electric modalities. Mapped onto a recent phylogeny, our results suggest that discrimination by electric cues alone may be an apomorphic trait evolved during a recent radiation in this taxon.

Electric Organ Discharges of Cyphomyrus petherici (Mormyridae, Osteoglossiformes) from the White Nile Basin.

The waveform and some characteristics of the electric organ discharges have been studied in 11 individuals of Cyphomyrus petherici, the only representative of the genus in the Nilotic fauna. The discharge is characterized by three to five phases with a prevalence of the second phase in terms of the relative amplitude and a wide variability of the total duration of discharge (from 212 to 558 μs). The comparison of the discharges of the species under study with those in the congeneric species and representatives of the genus Pollimyrus (which previously encompassed C. petherici) demonstrates a general similarity of the C. petherici discharges with those of Cyphomyrus, but not Pollimyrus. This is in agreement with the correspondence of the discharge characteristics observed in other mormyrids to the phylogenetic position and taxonomic status of the species.

Electrostatic Tuning of a Potassium Channel in Electric Fish

Molecular variation contributes to the evolution of adaptive phenotypes, though it is often difficult to understand precisely how. The adaptively significant electric organ discharge behavior of weakly electric fish is the direct result of biophysical membrane properties set by ion channels. Here, we describe a voltage-gated potassium-channel gene in African electric fishes that is under positive selection and highly expressed in the electric organ. The channel produced by this gene shortens electric organ action potentials by activating quickly and at hyperpolarized membrane potentials. The source of these properties is a derived patch of negatively charged amino acids in an extracellular loop near the voltage sensor. We demonstrate that this negative patch acts by contributing to the global surface charge rather than by local interactions with specific amino acids in the channel's extracellular face. We suggest a more widespread role for this loop in the evolutionary tuning of voltage-dependent channels.