Electric Organ Discharge Research Articles

Behavioral and Single-Neuron Sensitivity to Millisecond Variations in Temporally Patterned Communication Signals.

In many sensory pathways, central neurons serve as temporal filters for timing patterns in communication signals. However, how a population of neurons with diverse temporal filtering properties codes for natural variation in communication signals is unknown. Here we addressed this question in the weakly electric fish Brienomyrus brachyistius, which varies the time intervals between successive electric organ discharges to communicate. These fish produce an individually stereotyped signal called a scallop, which consists of a distinctive temporal pattern of ∼8-12 electric pulses. We manipulated the temporal structure of natural scallops during behavioral playback and in vivo electrophysiology experiments to probe the temporal sensitivity of scallop encoding and recognition. We found that presenting time-reversed, randomized, or jittered scallops increased behavioral response thresholds, demonstrating that fish's electric signaling behavior was sensitive to the precise temporal structure of scallops. Next, using in vivo intracellular recordings and discriminant function analysis, we found that the responses of interval-selective midbrain neurons were also sensitive to the precise temporal structure of scallops. Subthreshold changes in membrane potential recorded from single neurons discriminated natural scallops from time-reversed, randomized, and jittered sequences. Pooling the responses of multiple neurons improved the discriminability of natural sequences from temporally manipulated sequences. Finally, we found that single-neuron responses were sensitive to interindividual variation in scallop sequences, raising the question of whether fish may analyze scallop structure to gain information about the sender. Collectively, these results demonstrate that a population of interval-selective neurons can encode behaviorally relevant temporal patterns with millisecond precision. The timing patterns of action potentials, or spikes, play important roles in representing information in the nervous system. However, how these temporal patterns are recognized by downstream neurons is not well understood. Here we use the electrosensory system of mormyrid weakly electric fish to investigate how a population of neurons with diverse temporal filtering properties encodes behaviorally relevant input timing patterns, and how this relates to behavioral sensitivity. We show that fish are behaviorally sensitive to millisecond variations in natural, temporally patterned communication signals, and that the responses of individual midbrain neurons are also sensitive to variation in these patterns. In fact, the output of single neurons contains enough information to discriminate stereotyped communication signals produced by different individuals.

Evidence for Non-neutral Evolution in a Sodium Channel Gene in African Weakly Electric Fish (Campylomormyrus, Mormyridae)

Voltage-gated sodium channels, Nav1, play a crucial role in the generation and propagation of action potentials and substantially contribute to the shape of their rising phase. The electric organ discharge (EOD) of African weakly electric fish (Mormyroidea) is the sum of action potentials fired from all electrocytes of the electric organ at the same time and hence voltage-gated sodium channels are one factor-together with the electrocyte's morphology and innervation pattern-that determines the properties of these EODs. Due to the fish-specific genome duplication, teleost fish possess eight copies of sodium channel genes (SCN), which encode for Nav1 channels. In mormyroids, SCN4aa is solely expressed in the electrocytes of the adult electric organ. In this study, we compared entire SCN4aa sequences of six species of the genus Campylomormyrus and identified nonsynonymous substitutions among them. SCN4aa in Campylomormyrus exhibits a much higher evolutionary rate compared to its paralog SCN4ab, whose expression is not restricted to the electric organ. We also found evidence for strong positive selection on the SCN4aa gene within Mormyridae and along the lineage ancestral to the Mormyridae. We have identified sites at which all nonelectric teleosts are monomorphic in their amino acid, but mormyrids have different amino acids. Our findings confirm the crucial role of SCN4aa in EOD evolution among mormyrid weakly electric fish. The inferred positive selection within Mormyridae makes this gene a prime candidate for further investigation of the divergent evolution of pulse-type EODs among closely related species.

Active sensing associated with spatial learning reveals memory-based attention in an electric fish

Active sensing behaviors reveal what an animal is attending to and how it changes with learning. Gymnotus sp, a gymnotiform weakly electric fish, generates an electric organ discharge (EOD) as discrete pulses to actively sense its surroundings. We monitored freely behaving gymnotid fish in a large dark "maze" and extracted their trajectories and EOD pulse pattern and rate while they learned to find food with electrically detectable landmarks as cues. After training, they more rapidly found food using shorter, more stereotyped trajectories and spent more time near the food location. We observed three forms of active sensing: sustained high EOD rates per unit distance (sampling density), transient large increases in EOD rate (E-scans) and stereotyped scanning movements (B-scans) were initially strong at landmarks and food, but, after learning, intensified only at the food location. During probe (no food) trials, after learning, the fish's search area and intense active sampling was still centered on the missing food location, but now also increased near landmarks. We hypothesize that active sensing is a behavioral manifestation of attention and essential for spatial learning; the fish use spatial memory of landmarks and path integration to reach the expected food location and confine their attention to this region.

Marcusenius desertus sp. nov. (Teleostei: Mormyridae), a mormyrid fish from the Namib desert

We critically compared Marcusenius specimens from the mouth of the Cunene River on the Namibia/Angola border, a harsh desert environment on the Atlantic Ocean coast virtually devoid of aerial insects with aquatic larvae which are an important food item, with Marcusenius multisquamatus Kramer & Wink, 2013 from the escarpment region of that same river, in a relatively rich and productive subtropical savannah environment. River mouth specimens were differentiated in morphology and electric organ discharges, as determined by ANOVA/MANOVA comparisons, principal component and discriminant analyses on morphological and electrophysiological characters, and genetics, including sequences of the mitochondrial cytochrome b gene, indicating reproductive isolation. Specimens from the river mouth differed from M. multisquamatus, their closest relatives, by having a shorter snout, a smaller eye diameter, and smaller nares separation. River mouth specimens were also differentiated from other, increasingly less-close relatives, such as M. altisambesi Kramer et al., 2007 from the Okavango River, Botswana, and from M. krameri Maake et al., 2014 from the Limpopo System, South Africa. We therefore designate the new species Marcusenius desertus sp. nov. for the Cunene River mouth population.

Modeling the Oscillating Dipole Properties of Electric Organ Discharge in the Weakly Electric Fish, Eigenmannia

One of the most studied weakly electric fish, Eigenmannia produces a continuous high frequency electric organ discharge (EOD) used to sense nearby objects and communicate with conspecifics. The EOD of an individual fish has a characteristic frequency (within the species range, 250-600 Hz) which it shifts when necessary to avoid jamming. The nearly dipolar oscillating electric field yields zero net current and is generated by parallel columns of identical, synchronously discharging electrocyte cells. Recent findings from whole fish respirometry (during high-frequency signaling over a range of frequencies) have renewed interest in the frequency-dependent energetics of the EODs (Lewis et al 2014 J Neurosci 34:197) but the modeling based on past analyses is missing some key features of the in-vivo electrolyte operation. We have constructed a model for the neurally-driven electrocyte action potentials (APs) that underlie the EOD. APs are initiated by brief post-synaptic cation influxes through AChR channels at each electrocyte's innervated posterior end. This yields a head positive current while the anterior end serves mainly as a capacitor whose discharge yields the head negative current of the oscillating dipole cycle. To maintain the appropriate [Na]in and [K]out levels, Na/K-ATPase pumps run continuously. Modeling the activity of this ATP consuming protein gives us access to electrocyte energetics and frequency-dependent EOD efficiency. Modeling the posterior-anterior current flows gives us access to the electric field patterns produced by the electrocytes.

Finite-element simulation study of an underwater active electrolocation system based on Cole-Cole model

The underwater active electrolocation method is a promising technology, which can be used to locating and navigation. This method is invented by simulating a kind of weakly electric fish detect target. This kind of fish can generate a low frequency electric field by its electric organ discharges (EOD), and can sense the electric field change in surrounding area by its electroreceptors. This function of weakly electric fish is called active electrolocation system. The weakly electric fish can detect the target in complete darkness by their active electrolocation system. In order to understand the active electrolocation system, it has been researched by biologists for almost 60 years. At recently two decades, the underwater active electrolocation system has been investigated by many engineers. All of these scientists focused on setting up the active electrolocation test platform by experiment or building the active electrolocation system model by theoretical analysis or the finite element emulation method. But the physical mechanism of the active electrolocation system of weakly electric fish still is a contentious issue. In previous experiments, the amplitude information-frequency characteristics (AIFC) for active electrolocation system has been studied, and the detect frequency dead zone (DFDZ) and frequency inflection point (FIP) phenomena of AIFC for active electrolocation system has been found. In this paper, to understand this special phenomenon, a finite element model based on the ideal electromagnetic theory was built to simulate the active electrolocation system. But the DFDZ and FIP phenomena of AIFC for active electolocation system cannot be really simulated by this model. Then, we assumed that DFDZ and FIP phenomena are induced by phenomenon (IP) effect at the boundary between the target and water in the process of detecting target. In order to validate this assumption, the Cole-Cole model was used to fits the IP effect, and a finite element model of coupling the Cole-Cole model and ideal electromagnetic theory was created. Large numbers of simulation calculations based on this new finite element model were carried out. The simulation calculations results of the new finite element model were found to be in line with the experimental results. The simulation calculations calculation results of the new model indicate that: (1) the underwater active electrolocation system can be simulated by the new finite element model of coupling the Cole-Cole model and ideal electromagnetic theory; (2) it is a reasonable fact that the DFDZ and FIP phenomena of AIFC for underwater active electrolocation system can be explained by the IP effect; (3) the frequency inflection point (FIP) is varies with the parameters of the Cole-Cole model, and it is also can be speculated that the parameters of the Cole-Cole model reflect the changing of the DFDZ and FIP phenomenon of AFIC for electrolocation system. In this paper, the IP effect is introduced to the model of underwater active eletrolocation system for the first time. It will be of great benefit to us to understand the physical mechanism for active electrolocation system of weakly electric fish and provided an active electrolocation system finite element model for simulation. And it may be helpful for designing the equipment of active electrolocation system.

The active electric sense of weakly electric fish: from electric organ discharge to sensory processing and behaviour

Sensory systems have been shaped by evolution to extract information that is relevant for decision making. In order to understand the mechanisms used by sensory systems for filtering the incoming stream of sensory input, it is important to have a quantitative understanding of the natural sensory scenes that are to be processed. Weakly electric fish lead a rather cryptic nocturnal life in often turbid tropical rainforest streams. They produce electric discharges and sense perturbations of their selfgenerated electric field for prey detection and navigation, and also use their active sense for communication in the context of courtship and aggression. The fact that they produce their electric signals throughout day and night permits the use of electrode arrays to track the movements of multiple individual fish and monitor their communication interactions, thus offering a window into their electrosensory world. This approach yields unprecedented access to information on the biology of these fishes and also on the statistical properties of the sensory scenes that are to be processed by their electrosensory system. The electrosensory system shares many organizational features with other sensory systems, in particular, the use of multiple topographic maps. In fact, the sensory surface (the skin) is represented in three parallel maps in the hindbrain, with each map covering the receptor organ array with six different cell types that project to the next higher level of processing. Thus, the electroreceptive body surface is represented a total of 18 times in the hindbrain, with each representation having its specific filter properties and degree of response plasticity. Thus, the access to the sensory world of these fish as well as the manifold filtering of the sensory input makes these fish an excellent model system for exploring the cell-intrinsic and network characteristics underlying the extraction of behaviourally relevant sensory information.

Ultrafast traveling wave dominates the electric organ discharge of Apteronotus leptorhynchus: an inverse modelling study.

Identifying and understanding the current sources that give rise to bioelectric fields is a fundamental problem in the biological sciences. It is very difficult, for example, to attribute the time-varying features of an electroencephalogram recorded from the head surface to the neural activity of specific brain areas; model systems can provide important insight into such problems. Some species of fish actively generate an oscillating (c. 1000 Hz) quasi-dipole electric field to communicate and sense their environment in the dark. A specialized electric organ comprises neuron-like cells whose collective signal underlies this electric field. As a step towards understanding the detailed biophysics of signal generation in these fish, we use an anatomically-detailed finite-element modelling approach to reverse-engineer the electric organ signal over one oscillation cycle. We find that the spatiotemporal profile of current along the electric organ constitutes a travelling wave that is well-described by two spatial Fourier components varying in time. The conduction velocity of this wave is faster than action potential conduction in any known neuronal axon (>200 m/s), suggesting that the spatiotemporal features of high-frequency electric organ discharges are not constrained by the conduction velocities of spinal neuron pathways.

Androgens regulate sex differences in signaling but are not associated with male variation in morphology in the weakly electric fish Parapteronotus hasemani

Sexually dimorphic signaling is widespread among animals and can act as an honest indicator of mate quality. Additionally, differences in signaling and morphology within a sex can be associated with different strategies for acquiring mates. Weakly electric fish communicate via self-generated electrical fields that transmit information about sex, reproductive state, and social status. The weakly electric knifefish Parapteronotus hasemani exhibits sexual dimorphism in body size as well as substantial within-male variation in body size and jaw length. We asked whether P. hasemani exhibits hormonally mediated sexual dimorphism in electrocommunication behavior. We also asked whether males with short versus long jaws differed significantly from each other in morphology, behavior, hormone levels, or reproductive maturity. Males produced longer chirps than females, but other signal parameters (electric organ discharge frequency; chirp rate and frequency modulation) were sexually monomorphic. Pharmacologically blocking androgen receptors in males reduced chirp duration, suggesting that this sexually dimorphic trait is regulated at least in part by the activational effects of androgens. Males sorted into two distinct morphological categories but did not differ in circulating 11-ketotestosterone or testosterone. Short-jawed males and long-jawed males also did not differ in any aspects of signaling. Thus, chirping and high levels of 11-ketotestosterone were reliably associated with reproductively active males but do not necessarily indicate male type or quality. This contrasts with other alternative male morph systems in which males that differ in morphology also differ in androgen profiles and signaling behavior.

Cross-tissue and cross-species analysis of gene expression in skeletal muscle and electric organ of African weakly-electric fish (Teleostei; Mormyridae)

BackgroundAfrican weakly-electric fishes of the family Mormyridae are able to produce and perceive weak electric signals (typically less than one volt in amplitude) owing to the presence of a specialized, muscle-derived electric organ (EO) in their tail region. Such electric signals, also known as Electric Organ Discharges (EODs), are used for objects/prey localization, for the identification of conspecifics, and in social and reproductive behaviour. This feature might have promoted the adaptive radiation of this family by acting as an effective pre-zygotic isolation mechanism. Despite the physiological and evolutionary importance of this trait, the investigation of the genetic basis of its function and modification has so far remained limited. In this study, we aim at: i) identifying constitutive differences in terms of gene expression between electric organ and skeletal muscle (SM) in two mormyrid species of the genus Campylomormyrus: C. compressirostris and C. tshokwe, and ii) exploring cross-specific patterns of gene expression within the two tissues among C. compressirostris, C. tshokwe, and the outgroup species Gnathonemus petersii.ResultsTwelve paired-end (100 bp) strand-specific RNA-seq Illumina libraries were sequenced, producing circa 330 M quality-filtered short read pairs. The obtained reads were assembled de novo into four reference transcriptomes. In silico cross-tissue DE-analysis allowed us to identify 271 shared differentially expressed genes between EO and SM in C. compressirostris and C.tshokwe. Many of these genes correspond to myogenic factors, ion channels and pumps, and genes involved in several metabolic pathways. Cross-species analysis has revealed that the electric organ transcriptome is more variable in terms of gene expression levels across species than the skeletal muscle transcriptome.ConclusionsThe data obtained indicate that: i) the loss of contractile activity and the decoupling of the excitation-contraction processes are reflected by the down-regulation of the corresponding genes in the electric organ’s transcriptome; ii) the metabolic activity of the EO might be specialized towards the production and turn-over of membrane structures; iii) several ion channels are highly expressed in the EO in order to increase excitability; iv) several myogenic factors might be down-regulated by transcription repressors in the EO.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1858-9) contains supplementary material, which is available to authorized users.

Thermal acclimation and thyroxine treatment modify the electric organ discharge frequency in an electric fish, Apteronotus leptorhynchus

In ectotherms, the rate of many neural processes is determined externally, by the influence of the thermal environment on body temperature, and internally, by hormones secreted from the thyroid gland. Through thermal acclimation, animals can buffer the influence of the thermal environment by adjusting their physiology to stabilize certain processes in the face of environmental temperature change. The electric organ discharge (EOD) used by weak electric fish for electrocommunication and electrolocation is highly temperature sensitive. In some temperate species that naturally experience large seasonal fluctuations in environmental temperature, the thermal sensitivity (Q10) of the EOD shifts after long-term temperature change. We examined thermal acclimation of EOD frequency in a tropical electric fish, Apteronotus leptorhynchus that naturally experiences much less temperature change. We transferred fish between thermal environments (25.3 and 27.8°C) and measured EOD frequency and its thermal sensitivity (Q10) over 11d. After 6d, fish exhibited thermal acclimation to both warming and cooling, adjusting the thermal dependence of EOD frequency to partially compensate for the small change (2.5°C) in water temperature. In addition, we evaluated the thyroid influence on EOD frequency by treating fish with thyroxine or the anti-thyroid compound propylthiouricil (PTU) to stimulate or inhibit thyroid activity, respectively. Thyroxine treatment significantly increased EOD frequency, but PTU had no effect. Neither thyroxine nor PTU treatment influenced the thermal sensitivity (Q10) of EOD frequency during acute temperature change. Thus, the EOD of Apteronotus shows significant thermal acclimation and responds to elevated thyroxine.

The secretogranin-II derived peptide secretoneurin modulates electric behavior in the weakly pulse type electric fish, Brachyhypopomus gauderio

Secretoneurin (SN) in the preoptic area and pituitary of mammals and fish has a conserved close association with the vasopressin and oxytocin systems, members of a peptide family that are key in the modulation of sexual and social behaviors. Here we show the presence of SN-immunoreactive cells and projections in the brain of the electric fish, Brachyhypopomus gauderio. Secretoneurin colocalized with vasotocin (AVT) and isotocin in cells and fibers of the preoptic area. In the rostral pars distalis of the pituitary, many cells were both SN and prolactin-positive. In the hindbrain, at the level of the command nucleus of the electric behavior (pacemaker nucleus; PN), some of SN-positive fibers colocalized with AVT. We also explored the potential neuromodulatory role of SN on electric behavior, specifically on the rate of the electric organ discharge (EOD) that signals arousal, dominance and subordinate status. Each EOD is triggered by the command discharge of the PN, ultimately responsible for the basal EOD rate. SN modulated diurnal basal EOD rate in freely swimming fish in a context-dependent manner; determined by the initial value of EOD rate. In brainstem slices, SN partially mimicked the in vivo behavioral effects acting on PN firing rate. Taken together, our results suggest that SN may regulate electric behavior, and that its effect on EOD rate may be explained by direct action of SN at the PN level through either neuroendocrine and/or endocrine mechanisms.

Food deprivation reduces and leptin increases the amplitude of an active sensory and communication signal in a weakly electric fish

Energetic demands of social communication signals can constrain signal duration, repetition, and magnitude. The metabolic costs of communication signals are further magnified when they are coupled to active sensory systems that require constant signal generation. Under such circumstances, metabolic stress incurs additional risk because energy shortfalls could degrade sensory system performance as well as the social functions of the communication signal. The weakly electric fish Eigenmannia virescens generates electric organ discharges (EODs) that serve as both active sensory and communication signals. These EODs are maintained at steady frequencies of 200–600Hz throughout the lifespan, and thus represent a substantial metabolic investment. We investigated the effects of metabolic stress (food deprivation) on EOD amplitude (EODa) and EOD frequency (EODf) in E. virescens and found that only EODa decreases during food deprivation and recovers after restoration of feeding. Cortisol did not alter EODa under any conditions, and plasma cortisol levels were not changed by food deprivation. Both melanocortin hormones and social challenges caused transient EODa increases in both food-deprived and well-fed fish. Intramuscular injections of leptin increased EODa in food-deprived fish but not well-fed fish, identifying leptin as a novel regulator of EODa and suggesting that leptin mediates EODa responses to metabolic stress. The sensitivity of EODa to dietary energy availability likely arises because of the extreme energetic costs of EOD production in E. virescens and also could reflect reproductive strategies of iteroparous species that reduce social signaling and reproduction during periods of stress to later resume reproductive efforts when conditions improve.

Neotropical electric fishes (Gymnotiformes) as model organisms for bioassays

Electric fishes (Gymnotiformes) inhabit Central and South America and form a relatively large group with more than 200 species. Besides a taxonomic challenge due to their still unresolved systematic, wide distribution and the variety of habitats they occupy, these fishes have been intensively studied due to their peculiar use of bioelectricity for electrolocation and communication. Conventional analysis of cells, tissues and organs have been complemented with the studies on the electric organ discharges of these fishes. This review compiles the results of 13 bioassays developed during the last 50 years, which used the quickness, low costs and functionality of the bioelectric data collection of Gymnotiformes to evaluate the effects of environmental contaminants and neuroactive drugs. journal homepage: www.jclmm.com

Individual discrimination of freely swimming pulse-type electric fish from electrode array recordings

Pulse-type weakly electric fishes communicate through electrical discharges with a stereotyped waveform, varying solely the interval between pulses according to the information being transmitted. This simple codification mechanism is similar to the one found in various known neuronal circuits, which renders these animals as good models for the study of natural communication systems, allowing experiments involving behavioral and neuroethological aspects. Performing analysis of data collected from more than one freely swimming fish is a challenge since the detected electric organ discharge (EOD) patterns are dependent on each animal׳s position and orientation relative to the electrodes. However, since each fish emits a characteristic EOD waveform, computational tools can be employed to match each EOD to the respective fish. In this paper we describe a computational method able to recognize fish EODs from dyads using normalized feature vectors obtained by applying Fourier and dual-tree complex wavelet packet transforms. We employ support vector machines as classifiers, and a continuity constraint algorithm allows us to solve issues caused by overlapping EODs and signal saturation. Extensive validation procedures with Gymnotus sp. showed that EODs can be assigned correctly to each fish with only two errors per million discharges.

Enhanced sensory sampling precedes self-initiated locomotion in an electric fish.

Cortical activity precedes self-initiated movements by several seconds in mammals; this observation has led into inquiries on the nature of volition. Preparatory neural activity is known to be associated with decision making and movement planning. Self-initiated locomotion has been linked to increased active sensory sampling; however, the precise temporal relationship between sensory acquisition and voluntary movement initiation has not been established. Based on long-term monitoring of sensory sampling activity that is readily observable in freely behaving pulse-type electric fish, we show that heightened sensory acquisition precedes spontaneous initiation of swimming. Gymnotus sp. revealed a bimodal distribution of electric organ discharge rate (EODR) demonstrating down- and up-states of sensory sampling and neural activity; movements only occurred during up-states and up-states were initiated before movement onset. EODR during voluntary swimming initiation exhibited greater trial-to-trial variability than the sound-evoked increases in EODR. The sampling variability declined after voluntary movement onset as previously observed for the neural variability associated with decision making in primates. Spontaneous movements occurred randomly without a characteristic timescale, and no significant temporal correlation was found between successive movement intervals. Using statistical analyses of spontaneous exploratory behaviours and associated preparatory sensory sampling increase, we conclude that electric fish exhibit key attributes of volitional movements, and that voluntary behaviours in vertebrates may generally be preceded by increased sensory sampling. Our results suggest that comparative studies of the neural basis of volition may therefore be possible in pulse-type electric fish, given the substantial homologies between the telencephali of teleost fish and mammals.

Sound production to electric discharge: sonic muscle evolution in progress in Synodontis spp. catfishes (Mochokidae).

Elucidating the origins of complex biological structures has been one of the major challenges of evolutionary studies. Within vertebrates, the capacity to produce regular coordinated electric organ discharges (EODs) has evolved independently in different fish lineages. Intermediate stages, however, are not known. We show that, within a single catfish genus, some species are able to produce sounds, electric discharges or both signals (though not simultaneously). We highlight that both acoustic and electric communication result from actions of the same muscle. In parallel to their abilities, the studied species show different degrees of myofibril development in the sonic and electric muscle. The lowest myofibril density was observed in Synodontis nigriventris, which produced EODs but no swim bladder sounds, whereas the greatest myofibril density was observed in Synodontis grandiops, the species that produced the longest sound trains but did not emit EODs. Additionally, S. grandiops exhibited the lowest auditory thresholds. Swim bladder sounds were similar among species, while EODs were distinctive at the species level. We hypothesize that communication with conspecifics favoured the development of species-specific EOD signals and suggest an evolutionary explanation for the transition from a fast sonic muscle to electrocytes.

Electric imaging through evolution, a modeling study of commonalities and differences.

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.

A phenomenological model for self-initiated movement in electric fish

Observing behaviourally unconstrained animals can lead to simple characterization of complex behaviour. We apply this principle to infer the neural dynamics of self-initiated movement in pulse-type electric fish, Gymnotus sp. Recent long-term monitoring of fish (~200 hours from 22 recording sessions, over 4 animals) in freely swimming conditions, devoid of external stimuli, reveals non-trivial structures in their pattern of electric organ discharge (EOD). Simultaneous recording of EODs and fish movement show that the EOD rate (EODR) and the activity level of the fish are bi-modally distributed, as well as highly correlated. These features thus effectively define behavioural attractor states corresponding to high and low levels of neural activity (up- and down-states, respectively). Trajectories in the EODR-activity plane consist of diffusional motion around the attractor states, interrupted by sharp transitions between states. The duration of each state is uncorrelated with that of the next up- or down-state, and is log-normally distributed with no characteristic time-scale. Based on this data, our goal is to develop a modelling framework to better understand the neural pathway responsible for self-initiated movement. However, because the physiological parameters defining this pathway are experimentally unconstrained, it would be premature at this point to develop a detailed biophysical model of this system. There is thus a preliminary need to, instead, characterize the key features of the data from a phenomenological perspective. To address this research gap, we attempt to fit a stochastic process, with the simplest combination of dynamical components, that most closely reproduces the statistics of the data. As a first step, we hypothesize that the first principal component of the data (EODR and activity level) follows an overdamped Brownian motion in a double-well potential with additive noise. Based on the approach of [1], we fit a 4th order polynomial for the potential function by associating the stationary solution of the Fokker-Planck equation with the measured histogram. For most recording sessions, the fits appropriately reproduce the histograms, but consistently underestimates the width of the up-state potential well. Once the potential function is determined, we generate an estimate for the noise intensity by calculating the mean escape time from small regions at the bottom of either well, and comparing it with its theoretical expression. We find, however, that this estimate is dependent on the well that was used to generate it, with all recording sessions showing a larger noise estimate for the up-state than for the down-state. Moreover, in most cases, the ratio of up- to down-state duration is underestimated by the fitted process, indicative of either too short up-states, or too long down-states compared to the data. These findings are consistent with the above discrepancy for the width of the up-state potential well, as well as with visual inspection of the data, which shows greater variability when fish are in up-states. Taken together, these observations strongly suggest that state-dependent noise is involved in the process generating the data, either in the form of multiplicative noise, or Poisson shot noise.

Differential neural responses to naturally occurring envelopes in the electrosensory system

Natural sensory stimuli frequently consist of a fine structure whose amplitude (i.e. envelope) varies more slowly. Previous studies have demonstrated that envelope signals are found across sensory systems and are necessary for perception. For example, envelope signals in the auditory system carry information pertaining to the perception of pitch fluctuations in communication vocalizations [1], while envelopes in the visual system are responsible for object grouping and the perception of illusory contours [2,3]. However, the neural mechanisms underlying the encoding of these envelope signals are poorly understood in general. Gymnotiform wave-type weakly electric fish constitute an attractive model system for studying envelope processing in the brain because of its well-characterized anatomy and physiology [4]. These fish generate around themselves a weak quasi-sinusoidal electric field through the electric organ discharge (EOD) [5]. Recent studies have shown that the beat amplitude (i.e. the envelope) can vary in time during different behavioral contexts and display differential frequency content: while envelopes caused by movement primarily contain low ( 1 Hz) temporal frequencies [7]. While it is known that electrosensory neurons can respond to envelopes [7], whether these neurons respond differentially to envelopes arising from movement and social interaction is unknown in part because their tuning to envelope frequencies has not been characterized. Here we used well established techniques [8] to record from electrosensory pyramidal neurons across different maps of the body surface within the electrosensory lateral line lobe (ELL) in response to envelope stimuli with different frequency content spanning the behaviorally relevant range (0.05-10 Hz). Using standard measures of linear systems identification techniques as well as more quantitative methods of information theory, we found that pyramidal neurons in different maps displayed differential responses to envelopes arising from different behavioral contexts. Our results suggest that information about envelopes arising from different behavioral contexts begins to be segregated at the level of the ELL and provide new insights as to how these behaviorally relevant stimuli are encoded in early sensory pathways.