Pulse-type Electric Fish Research Articles

Waveform sensitivity of electroreceptors in the pulse-type weakly electric fish Gymnotus omarorum.

As in most sensory systems, electrosensory images in weakly electric fish are encoded in two parallel pathways, fast and slow. From work on wave-type electric fish, these fast and slow pathways are thought to encode the time and amplitude of electrosensory signals, respectively. The present study focuses on the primary afferents giving origin to the slow path of the pulse-type weakly electric fish Gymnotus omarorum We found that burst duration coders respond with a high-frequency train of spikes to each electric organ discharge. They also show high sensitivity to phase-frequency distortions of the self-generated local electric field. We explored this sensitivity by manipulating the longitudinal impedance of a probe cylinder to modulate the stimulus waveform, while extracellularly recording isolated primary afferents. Resistive loads only affect the amplitude of the re-afferent signals without distorting the waveform. Capacitive loads cause large waveform distortions aside from amplitude changes. Stepping from a resistive to a capacitive load in such a way that the stimulus waveform was distorted, without changing its total energy, caused strong changes in latency, inter-spike interval and number of spikes of primary afferent responses. These burst parameters are well correlated suggesting that they may contribute synergistically in driving downstream neurons. This correlation also suggests that each receptor encodes a single parameter in the stimulus waveform. The finding of waveform distortion sensitivity is relevant because it may contribute to: (a) enhance electroreceptive range in the peripheral 'electrosensory field', (b) a better identification of living prey at the 'foveal electrosensory field' and (c) detect the presence and orientation of conspecifics. Our results also suggest a revision of the classical view of amplitude and time encoding by fast and slow pathways in pulse-type electric fish.

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.

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.

Enhanced attention precedes self-initiated locomotion in an electric fish

Volition is generally considered as a defining human faculty; but the outcome of a voluntary decision can be predicted by brain activity even before subject’s conscious awareness [1], and similar phenomena are observed in many species. Preparatory neural activities for voluntary movements involve movement planning and decision making [2], and active movements accompany heightened attention [3]. We show that enhanced attention precedes self-initiated movements in an animal model that exhibits a readily observable and quantifiable sensory acquisition rate. In addition to demonstrating preparatory increases in sensory sampling, our results reveal close similarities between the sensory sampling and the neural activity suggest associated with voluntary decision making [4]. Cortical activity precedes self-initiated movements by several seconds in mammals; this observation has led into inquiries on the nature of volition [1]. Preparatory neural activity is known to be associated with decision making and movement planning [2]. Self-initiated locomotion has been linked to active sensing indicative of enhanced attention [3]; 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 sensory sampling variability increased before, and declined after voluntary movement onset as previously observed for the neural variability associated with decision-making in primates [4]. In contrast, stimulus onset quenched the sampling variability similar to that previously reported in neural variability [5]. Spontaneous movements occurred randomly without a characteristic timescale, and no significant temporal correlation was found between successive movement intervals.

Automatic Realistic Real Time Stimulation/Recording in Weakly Electric Fish: Long Time Behavior Characterization in Freely Swimming Fish and Stimuli Discrimination

Weakly electric fish are unique model systems in neuroethology, that allow experimentalists to non-invasively, access, central nervous system generated spatio-temporal electric patterns of pulses with roles in at least 2 complex and incompletely understood abilities: electrocommunication and electrolocation. Pulse-type electric fish alter their inter pulse intervals (IPIs) according to different behavioral contexts as aggression, hiding and mating. Nevertheless, only a few behavioral studies comparing the influence of different stimuli IPIs in the fish electric response have been conducted. We developed an apparatus that allows real time automatic realistic stimulation and simultaneous recording of electric pulses in freely moving Gymnotus carapo for several days. We detected and recorded pulse timestamps independently of the fish’s position for days. A stimulus fish was mimicked by a dipole electrode that reproduced the voltage time series of real conspecific according to previously recorded timestamp sequences. We characterized fish behavior and the eletrocommunication in 2 conditions: stimulated by IPIs pre-recorded from other fish and random IPI ones. All stimuli pulses had the exact Gymontus carapo waveform. All fish presented a surprisingly long transient exploratory behavior (more than 8 h) when exposed to a new environment in the absence of electrical stimuli. Further, we also show that fish are able to discriminate between real and random stimuli distributions by changing several characteristics of their IPI distribution.

Spatial memory shapes active sensory sampling in pulse-type electric fish

Event Abstract Back to Event Spatial memory shapes active sensory sampling in pulse-type electric fish James J. Jun1, 2, 3*, Erik Harvey-Girard2, Andre Longtin1, 3 and Leonard Maler2, 3 1 University of Ottawa, Department of Physics, Canada 2 University of Ottawa, Department of Cellular and Molecular Medicine, Canada 3 University of Ottawa, Center for Neural Dynamics, Canada An animal's past experiences influence its behavior and its focus of its attention as it investigates its environment. Active sensing behavior therefore implies that an animal could use its past experiences to choose an optimal search strategy and modulate its sensory sampling rate accordingly. Weakly electric fish are nocturnal and navigate using an active electric sense by generating an electric organ discharge (EOD) and detecting distortions in its electric field caused by environmental features. Some electric fish (pulse-type) species generate brief EOD pulses (~1 ms) at a varying rate; the EOD rate rapidly rises when fish encounters a novel sensory stimuli. This phenomenon is known as a novelty response and the fish’s sensory sampling rate, in the dark, is simply equal to its EOD rate. We studied the South American pulse-type weakly electric fish Gymnotus sp. to test whether they can be trained, without visual cues, to learn a spatial location of food using electrosensory-detectable landmarks and, if so, whether they can use their past experiences to minimize their search area and modulate their EOD rate when hunting for food. A live mealworm was tied and presented at a fixed location with stable plastic landmarks until the fish was trained to find the food by traveling the shortest path; we determined the EOD rate as a function of landmark location and analyzed how it changed over learning trials. We presented four peripheral landmarks within a circular arena (1.5 m in diameter, Fig. 1) for all groups, and a central landmark adjacent to the mealworm for a cue-learning group; the other group was assumed to rely path integration for locating the prey. During probe trials (after learning was complete), we took out only the food and determined the fish’s trajectory and recorded its EOD rate as a function of location. During perturbation trials, we rearranged the landmarks by translation, expansion, or mirroring, and observed the most frequently visited location and associated EOD rate. Finally, fish were relocated and re-learned the food location by entering the same arena from a different entrance which was rotated 90 degrees from the original entrance. We found that fish revisited the missing food location with high spatial accuracy. The most visited location was within ~1 cm of the missing food location for the cue-learning group, and within ~5 cm for the path-integration group. Fish specifically increased their EOD rate near the missing food or changed landmark locations. The location of search was influenced by the geometric arrangement of landmarks. Translation of the landmarks caused the most visited location to be displaced by an equal amount for the cue-learning group, but the displacement of the most visited location followed less closely for the path-integration group. After the relocation, fish re-learned the food location from an alternate entrance and achieved the shortest path more quickly than in the initial learning phase. Our studies show that Gymnotus sp. can choose its search trajectory and modulate its sensory sampling rate based on its past experiences of landmarks and path-integration. Figure 1 Acknowledgements The authors acknowledge Lee Hunton, Declan Lu for their help with experimental setup and Chris Anderson for data collection. Authors also thank Dr. Gary Marsat and Dr. Erik Harvey-Girard for helpful discussions.

Precision measurement of electric organ discharge timing from freely moving weakly electric fish

Physiological measurements from an unrestrained, untethered, and freely moving animal permit analyses of neural states correlated to naturalistic behaviors of interest. Precise and reliable remote measurements remain technically challenging due to animal movement, which perturbs the relative geometries between the animal and sensors. Pulse-type electric fish generate a train of discrete and stereotyped electric organ discharges (EOD) to sense their surroundings actively, and rapid modulation of the discharge rate occurs while free swimming in Gymnotus sp. The modulation of EOD rates is a useful indicator of the fish's central state such as resting, alertness, and learning associated with exploration. However, the EOD pulse waveforms remotely observed at a pair of dipole electrodes continuously vary as the fish swims relative to the electrodes, which biases the judgment of the actual pulse timing. To measure the EOD pulse timing more accurately, reliably, and noninvasively from a free-swimming fish, we propose a novel method based on the principles of waveform reshaping and spatial averaging. Our method is implemented using envelope extraction and multichannel summation, which is more precise and reliable compared with other widely used threshold- or peak-based methods according to the tests performed under various source-detector geometries. Using the same method, we constructed a real-time electronic pulse detector performing an additional online pulse discrimination routine to enhance further the detection reliability. Our stand-alone pulse detector performed with high temporal precision (<10 μs) and reliability (error <1 per 10(6) pulses) and permits longer recording duration by storing only event time stamps (4 bytes/pulse).

Brain androgen receptor expression correlates with seasonal changes in the behavior of a weakly electric fish, Brachyhypopomus gauderio

Seasonal breeders are superb models for understanding natural relationships between reproductive behavior and its neural bases. We investigated the cellular bases of hormone effects in a weakly pulse-type electric fish with well-defined hormone-sensitive communication signals. Brachyhypopomus gauderio males emit social electric signals (SESs) consisting of rate modulations of the electric organ discharge during the breeding season. This discharge is commanded by a medullary pacemaker nucleus (PN), composed of pacemaker and relay neurons. We analyzed the contribution of androgen receptor (AR) expression to the seasonal generation of SESs, by examining the presence of ARs in the PN in different experimental groups: breeding, non-breeding, and testosterone (T)-implanted non-breeding males. AR presence and distribution in the CNS was assessed through western blotting and immunohistochemistry using the PG-21 antibody, which was raised against the human AR. We found AR immunoreactivity, for the first time in a pulse-type Gymnotiform, in several regions throughout the brain. In particular, this is the first report to reveal the presence of AR in both pacemaker and relay neurons within the Gymnotiform PN. The AR immunoreactivity was present in breeding males and could be induced in T-implanted non-breeding males. This seasonal and T-induced AR expression in the PN suggests that androgens may play an important role in the generation of SESs by modulating intrinsic electrophysiological properties of pacemaker and relay neurons.

Noise autocorrelation and jamming avoidance performance in pulse type electric fish

The amplitude and the autocorrelation level of the noise affecting the interval between successive electric organ discharges were estimated in isolated fish and in socially interacting fish of the species Gymnotus carapo. Both quantities increased in the fish with the slower discharging rate of the pair during the interaction, and we aim to assess whether they have some functional implication for the efficiency of the jamming avoidance response performed by the fish having the faster discharging rate of the pair. For this purpose, the noisy variability of the intervals around its mean value was simulated using autoregressive models estimated from experimental recordings of isolated and interacting fish. The simulation was implemented using two autoregressive models, each representing one fish of the pair. The jamming avoidance response was included by adding transient interval shortenings to the train simulating the fish of the pair that discharges at a faster rate whenever the two trains were close to discharge simultaneously. The number of double coincidences (i.e., simultaneous discharges occurring in two successive firing cycles) of the two simulated trains was used to measure the efficiency of the jamming avoidance. This quantity was evaluated separately as a function of the autocorrelation level and amplitude of the simulated variability, in realizations with and without jamming avoidance response. Only if jamming avoidance response was included in the simulation have we found that (i) the number of coincidences decreased with the increasing of the autocorrelation and (ii) the increase in the amplitude determined a growth of the coincidence number at a rate that is inversely proportional to the autocorrelation level. We argue that the persistent correlations of the fish variability constitute an adaptation that improves the efficiency of transient interval shortenings as a jamming avoidance strategy. The long autocorrelation time prevents the disruption of the jamming avoidance performance due to increases in the variability amplitude.

Relative dominance among males is expressed in the electric organ discharge characteristics of a weakly electric fish

The spectral characteristics of the electric organ discharge (EOD) of a species of pulse-type electric fish, Hypopomus occidentalis, can rapidly change during aggressive interactions. Pairs of animals were matched in aggressive displacement tests to score for dominace. The winning males displayed a reduction in the peak-power frequency of their EODs within 2 days. In addition, a correlation was found between the maintenance of dominant status and the display of the largest-amplitude EOD. Thus, in an interacting group of this species, a male with an EOD characterized by a lowest peak-power frequency and largest-amplitude holds the dominant status. Mechanisms are discussed as to how aggressive behavioural interactions may rapidly effect physiological changes in the EOD.

Time domain processing of electric organ discharge waveforms by pulse-type electric fish.

We explored coastal streams, rivers, and swamps in the Guianas of South America and found eleven species of gymnotiform fishes with pulse discharges. Each species has a characteristic electric organ discharge (EOD) waveform of 0.5-5 ms duration; at least two species appear to have a natural sex difference in their EODs which is apparent when comparing large adult males and females. Three sensory coding mechanisms are proposed to explain how electric fish might be able to determine species and sex identity from such short electrical pulses. Spectral Coding: electroreceptors tuned to different frequencies encode the spectrum of the EOD as a cross-fiber stimulation pattern. Temporal Coding: EODs are encoded as a volley of nerve spikes patterned in the time domain. Scan Sampling: a receiver detects a signaler's EOD as an amplitude modulation or 'beat' set up by the combination of its own discharge with the signaler's. The receiver uses the modulation envelope to assess the signaler's EOD waveform. To distinguish between these three coding mechanisms, we tested the ability of one pulse gymnotiform, Hypopomus beebei, to discriminate one electric waveform from another by comparing the acceleration of the discharge rate to different stimuli. Stimuli are presented under two conditions: when the stimulus pulse train is free-running compared to the fish's pulse train, and when the stimulus train is phase-locked to the fish's discharge pulse train. Under the former condition scan sampling may be used; under the latter it will be impossible. Hypopomus discriminates the polarity of a single period sinusoidal stimulus under scanning conditions but does not discriminate under clamped conditions. Hypopomus gives the strongest response to single period sine waves of 670 Hz and weaker responses to sinusoids of lower and higher frequencies. Free-running and phase-locked stimuli evoke similar responses. Under free-running conditions, Hypopomus discriminates a series of EOD-like stimuli that have been phase-shifted by varying amounts, but under phase-locked conditions does not. Scan sampling is presented as a possible waveform recognition mechanism for pulse-discharging gymnotiform fishes.

Sex differences in the waveform of the pulse-type electric fish,Pollimyrus isidori (Mormyridae)

This paper reports the finding of a sexual dimorphism in the electric organ discharge of the weakly electric fishPollimyms isidori. The difference in the head-positive components of the waveform (Fig. 1) was found in 95% of adults. Juvenile fish always possessed ‘female’ type discharges. Fourier analysis (Fig. 3) revealed significant sex differences in the power spectra of the discharges, indicating that specific phase information is perhaps unnecessary for sexual identification. The results are discussed with reference to our current knowledge of coding of electrocommunication signals in the electrosensory system.