Electric Organ Discharge Rate Research Articles

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

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

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

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

Understanding daily rhythms in weakly electric fish: the role of melatonin on the electric behavior of Brachyhypopomus gauderio.

Living organisms display molecular, physiological and behavioral rhythms synchronized with natural environmental cycles. Understanding the interaction between environment, physiology and behavior requires taking into account the complexity of natural habitats and the diversity of behavioral and physiological adaptations. Brachyhypopomus gauderio is characterized by the emission of electric organ discharges (EOD), with a very stable rate modulated by social and environmental cues. The nocturnal arousal in B. gauderio coincides with a melatonin-dependent EOD rate increase. Here, we first show a daily cycle in both the EOD basal rate (EOD-BR) and EOD-BR variability of B. gauderio in nature. We approached the understanding of the role of melatonin in this natural behavior through both behavioral pharmacology and in vitro assays. We report, for the first time in gymnotiformes, a direct effect of melatonin on the pacemaker nucleus (PN) inin vitro preparation. Melatonin treatment lowered EOD-BR in freely moving fish and PN basal rate, while increasing the variability of both. These results show that melatonin plays a key role in modulating the electric behavior of B. gauderio through its effect on rate and variability, both of which must be under a tight temporal regulation to prepare the animal for the challenging nocturnal environment.

Getting the news in milliseconds: The role of early novelty detection in active electrosensory exploration

The pulse emitting weakly electric fish Gymnotus omarorum shows stereotyped “novelty responses” consisting of a transient acceleration of the rhythm of a self-emitted electric organ discharge that carries electrosensory signals. Here we show that rapid increases in electric image amplitude cause a “novelty detection potential” in the first electrosensory relay. This sign precedes and its amplitude predicts, the amplitude of the subsequent behavioral novelty response. Current source density analyses indicates its origin ar the layers of the electrosensory lobe where the main output neurons occur. Two types of units, referred to as “ON” and “OFF”. Were recorded there in decerebrated fish. Firing probability of “OFF” units drastically decreased after a stepwise increase in electric image. By contrast, the very first novel stimuli after the increase evoked a sharp peak in firing rate of “ON” units followed by a very fast adaptation phase that contrasted with the slow adaptation observed in previous recordings of primary afferents. The amplitudes of this peak, the novelty detection potential, and the behavioral novelty responses, show the same dependence on the departure of the newest stimulus intensity from the weighted average of preceding ones suggesting that the signals encoded by “ON” neurons underlay the novelty detection potential, propagates through the hierarchical organization of the electromotor control, and finally contribute to accelerate the electric organ discharge rate. This suggests that detecting novelty at the very early processing stage of electrosensory signals is essential to adapt the electrosensory sampling rate to exploration requirements as they change dynamically.

Effects of hypoxia on aerobic metabolism and active electrosensory acquisition in the African weakly electric fish Marcusenius victoriae.

Environmental hypoxia has effected numerous and well-documented anatomical, physiological and behavioural adaptations in fishes. Comparatively little is known about hypoxia's impacts on sensing because it is difficult to quantify sensory acquisition in vivo. Weakly electric fishes, however, rely heavily on an easily-measurable sensory modality-active electric sensing-whereby individuals emit and detect electric organ discharges (EODs). In this study, hypoxia tolerance of a mormyrid weakly electric fish, Marcusenius victoriae, was assessed by examining both its metabolic and EOD rates using a critical threshold (pcrit ) paradigm. The routine metabolic rate was 1.42 mg O2 h-1 , and the associated critical oxygen tension was 14.34 mmHg. Routine EOD rate was 5.68 Hz with an associated critical tension of 15.14 mmHg. These metabolic indicators of hypoxia tolerance measured in this study were consistent with those in previous studies on M. victoriae and other weakly electric fishes. Furthermore, our results suggest that some aerobic processes may be reduced in favour of maintaining the EOD rate under extreme hypoxia. These findings underscore the importance of the active electrosensory modality to these hypoxia-tolerant fish.

The effect of normoxia exposure on hypoxia tolerance and sensory sampling in a swamp-dwelling mormyrid fish

Effects of energetic limitations on the performance of sensory systems are generally difficult to quantify. Weakly electric fishes provide an ideal model system to quantify the effects of metabolic stressors on sensory information acquisition, because they use an active-sensing strategy that permits easy measurement of the sensing effort. These fishes discharge an electric signal and sense perturbations of the resulting electric field. We used the mormyrid Petrocephalus degeni to quantify the relationship between routine metabolic rate and the rate of sensory sampling (rate of electric organ discharge, EOD) while under progressive hypoxia by quantifying the critical oxygen tension (PC-MR) and the critical electric organ discharge threshold (PC-EOD). PC-MR was significantly higher in fish acclimated to normoxia for over 40 days compared to animals tested within 1–5 days of capture from a hypoxic swamp, which suggests high costs of maintaining hypoxia tolerance; however, there was no acclimation effect on PC-EOD. All P. degeni reached their PC-EOD prior to their PC-MR. However, below the respective critical tension value, EOD rate decreased more gradually than the metabolic rate suggesting that the fish were increasing the proportion of their energy budget allocated to acquiring sensory information as dissolved-oxygen levels dropped. Trade-offs between sensory sampling and other physiological functions are also suggested by the increase in routine EOD rate with long-term normoxia acclimation, in contrast to metabolic rate, which showed no significant changes. These results highlight the relationship between sensory sampling and metabolic rate in response to progressive hypoxia and the plasticity of hypoxia tolerance.

Neural activity in a hippocampus-like region of the teleost pallium is associated with active sensing and navigation.

Most vertebrates use active sensing strategies for perception, cognition and control of motor activity. These strategies include directed body/sensor movements or increases in discrete sensory sampling events. The weakly electric fish, Gymnotus sp., uses its active electric sense during navigation in the dark. Electric organ discharge rate undergoes transient increases during navigation to increase electrosensory sampling. Gymnotus also use stereotyped backward swimming as an important form of active sensing that brings objects toward the electroreceptor dense fovea-like head region. We wirelessly recorded neural activity from the pallium of freely swimming Gymnotus. Spiking activity was sparse and occurred only during swimming. Notably, most units tended to fire during backward swims and their activity was on average coupled to increases in sensory sampling. Our results provide the first characterization of neural activity in a hippocampal (CA3)-like region of a teleost fish brain and connects it to active sensing of spatial environmental features.

Status-Dependent Vasotocin Modulation of Dominance and Subordination in the Weakly Electric Fish Gymnotus omarorum.

Dominant-subordinate status emerges from agonistic encounters. The weakly electric fish, Gymnotus omarorum, displays a clear-cut example of non-breeding territorial aggression. The asymmetry in the behavior of dominants and subordinates is outstanding. Dominants are highly aggressive and subordinates signal submission in a precise sequence of locomotor and electric traits: retreating, decreasing their electric organ discharge rate, and emitting transient electric signals. The hypothalamic neuropeptide arginine-vasotocin (AVT) and its mammalian homolog arginine-vasopressin, are key modulators of social behavior, known to adapt their actions to different contexts. By analyzing the effects of pharmacological manipulations of the AVT system in both dominants and subordinates, we show evidence of distinct status-dependent actions of AVT. We demonstrate an endogenous effect of AVT on dominants' aggression levels: blocking the V1a AVT receptor induced a significant decrease in dominants' attack rate. AVT administered to subordinates enhanced the expression of the electric signals of submission, without affecting subordinates' locomotor displays. This study contributes a clear example of status-dependent AVT modulation of agonistic behavior in teleosts, and reveals distinctive activation patterns of the AVT system between dominants and subordinates.

Vasotocin increases dominance in the weakly electric fish Brachyhypopomus gauderio

Animals establish social hierarchies through agonistic behavior. The recognition of the own and others social ranks is crucial for animals that live in groups to avoid costly constant conflicts. Weakly electric fish are valuable model systems for the study of agonistic behavior and its neuromodulation, given that they display conspicuous electrocommunication signals that are generated by a very well-known electromotor circuit. Brachyhypopomus gauderio is a gregarious electric fish, presents a polygynous breeding system, morphological and electrophysiological sexual dimorphism during the breeding season, and displays a typical intrasexual reproduction-related aggression. Dominants signal their social status by increasing their electric organ discharge (EOD) rate after an agonistic encounter (electric dominance). Subordinates only occasionally produce transient electric signals (chirps and offs). The hypothalamic neuropeptide arginine-vasotocin (AVT) and its mammalian homologue, arginine- vasopressin (AVP) are key modulators of social behavior across vertebrates. In this study, we focus on the role of AVT on dominance establishment in Brachyhypopomus gauderio by analyzing the effects of pharmacological manipulations of the AVT system in potential dominants. AVT exerts a very specific direct effect restricted only to EOD rate, and is responsible for the electric dominance. Unexpectedly, AVT did not affect the intensity of aggression in either contender. Nor was the time structure affected by AVT administration. We also present two interesting examples of the interplay between contenders by evaluating how AVT modulations, even when directed to one individual, affect the behavior of the dyad as a unit. First, we found that V1a AVT receptor antagonist Manning Compound (MC) induces a reversion in the positive correlation between dominants’ and subordinates’ attack rates, observed in both control and AVT treated dyads, suggesting that an endogenous AVT tone modulates aggressive interactions. Second, we confirmed that AVT administered to dominants induces an increase in the submissive transient electric signals in subordinates.

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.

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.

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.

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.

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.

Local vasotocin modulation of the pacemaker nucleus resembles distinct electric behaviors in two species of weakly electric fish

The neural bases of social behavior diversity in vertebrates have evolved in close association with hypothalamic neuropeptides. In particular, arginine-vasotocin (AVT) is a key integrator underlying differences in behavior across vertebrate taxa. Behavioral displays in weakly electric fish are channeled through specific patterns in their electric organ discharges (EODs), whose rate is ultimately controlled by a medullary pacemaker nucleus (PN). We first explored interspecific differences in the role of AVT as modulator of electric behavior in terms of EOD rate between the solitary Gymnotus omarorum and the gregarious Brachyhypopomus gauderio. In both species, AVT IP injection (10μg/gbw) caused a progressive increase of EOD rate of about 30%, which was persistent in B. gauderio, and attenuated after 30min in G. omarorum. Secondly, we demonstrated by in vitro electrophysiological experiments that these behavioral differences can be accounted by dissimilar effects of AVT upon the PN in itself. AVT administration (1μM) to the perfusion bath of brainstem slices containing the PN produced a small and transient increase of PN activity rate in G. omarorum vs the larger and persistent increase previously reported in B. gauderio. We also identified AVT neurons, for the first time in electric fish, using immunohistochemistry techniques and confirmed the presence of hindbrain AVT projections close to the PN that might constitute the anatomical substrate for AVT influences on PN activity. Taken together, our data reinforce the view of the PN as an extremely plastic medullary central pattern generator that not only responds to higher influences to adapt its function to diverse contexts, but also is able to intrinsically shape its response to neuropeptide actions, thus adding a hindbrain target level to the complexity of the global integration of central neuromodulation of electric behavior.

Effects of methylmercury on electric organ discharges in the weak electric fish Gymnotus sylvius.

MeHg) is present in the environment because of natural and anthropogenic causes. MeHg can reach the central nervous system (CNS) and cause neurological damage in humans and animals. Electric organ discharges (EODs) in the weak electric fish Gymnotus sylvius are produced by the electric organ and modulated by the CNS. These discharges are used for electrolocation and communication. The purpose of the present study was to investigate the effects of dietary MeHg exposure on EOD rate in G. sylvius. An oscilloscope was used to record the EOD rate. Two treatments were investigated: chronic MeHg administration (4 µg/kg MeHg every 2 days, with a total of nine dietary exposures to MeHg) and acute MeHg administration (a single dose of 20 µg/kg MeHg). The control data for both treatments were collected every 2 days for 18 days, with a total of nine sessions (day 1 until day 18). Data of fish exposed to MeHg were collected every 2 days, totaling nine sessions (day 19 until day 36). Chronic treatment significantly increased the EOD rate in G. sylvius (p < .05), especially with the final treatment (day 32 until day 36). Acute treatment resulted in an initial increase in the EOD rate, which was maintained midway through the experiment (day 26 until day 30; p < .05). The present study provides the first insights into the effects of MeHg on EODs in weak electric fish. The EOD rate is a novel response of the fish to MeHg administration. Keywords: electric organ discharge (EOD), methylmercury, electroreception, novel response.

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.

A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: functional aspects revealed by glutamate stimulation

The cyclic enrichment of behavioral repertoires is a common event in seasonal breeders. Breeding males Brachyhypopomus gauderio produce electric organ discharge (EOD) rate modulations called chirps while females respond with interruptions. The electromotor system is commanded by a pacemaker nucleus (PN) which sets the basal rate and produces the rate modulations. We focused on identifying functional, seasonal and sexual differences in this nucleus in correlation to these differences in behavior. The in vivo response to glutamate injection in the PN was seasonal, sexually dimorphic and site specific. Non-breeding adults and breeding females injected in dorsal and ventral sites generated EOD rate increases and interruptions, respectively. Reproductive males added a conspicuous communication signal to this repertoire. They chirped repetitively when we injected glutamate in a very restricted area of the ventral-rostral nucleus, surprisingly one with a low number of relay cell somata. This study shows that the PN is functionally organized in regions in a caudal-rostral axis, besides the previously documented dorsal-ventral division. Functional regions are revealed by seasonal changes that annually provide this nucleus with the cellular mechanisms that allow the bursting activity underlying chirp production, only in males.

A central pacemaker that underlies the production of seasonal and sexually dimorphic social signals: anatomical and electrophysiological aspects

Our long-term goal is to approach the understanding of the anatomical and physiological bases for communication signal diversity in gymnotiform fishes as a model for vertebrate motor pattern generation. Brachyhypopomus gauderio emits, in addition to its electric organ discharge (EOD) at basal rate, a rich repertoire of rate modulations. We examined the structure of the pacemaker nucleus, responsible for the EOD rate, to explore whether its high output signal diversity was correlated to complexity in its neural components or regional organization. We confirm the existence of only two neuron types and show that the previously reported dorsal-caudal segregation of these neurons is accompanied by rostral-caudal regionalization. Pacemaker cells are grouped dorsally in the rostral half of the nucleus, and relay cells are mainly ventral and more abundant in the caudal half. Relay cells are loosely distributed from the center to the periphery of the nucleus in correlation to somata size. Our findings support the hypothesis that regional organization enables a higher diversity of rate modulations, possibly offering distinct target areas to modulatory inputs. Since no anatomical or electrophysiological seasonal or sexual differences were found, we explored these aspects from a functional point of view in a companion article.

Vasotocin actions on electric behavior: interspecific, seasonal, and social context-dependent differences

Social behavior diversity is correlated with distinctively distributed patterns of a conserved brain network, which depend on the action of neuroendocrine messengers that integrate extrinsic and intrinsic cues. Arginine vasotocin (AVT) is a key integrator underlying differences in behavior across vertebrate taxa. Weakly electric fish use their electric organ discharges (EODs) as social behavioral displays. We examined the effect of AVT on EOD rate in two species of Gymnotiformes with different social strategies: Gymnotus omarorum, territorial and highly aggressive, and Brachyhypopomus gauderio, gregarious and aggressive only between breeding males. AVT induced a long-lasting and progressive increase of EOD rate in isolated B. gauderio, partially blocked by the V1a AVT receptor antagonist (Manning compound, MC), and had no effects in G. omarorum. AVT also induced a long-lasting increase in the firing rate (prevented by MC) of the isolated medullary pacemaker nucleus (PN) of B. gauderio when tested in an in vitro preparation, indicating that the PN is the direct effector of AVT actions. AVT is involved in the seasonal, social context-dependent nocturnal increase of EOD rate that has been recently described in B. gauderio to play a role in mate selection. AVT produced the additional nocturnal increase of EOD rate in non-breeding males, whereas MC blocked it in breeding males. Also, AVT induced a larger EOD rate increase in reproductive dyads than in agonistic encounters. We demonstrated interspecific, seasonal, and context-dependent actions of AVT on the PN that contribute to the understanding of the mechanisms the brain uses to shape sociality.