Collective sensing in electric fish.

A number of organisms, including dolphins, bats and electric fish, possess sophisticated active sensory systems that use self-generated signals (for example, acoustic or electrical emissions) to probe the environment1,2. Studies of active sensing in social groups have typically focused on strategies for minimizing interference from conspecific emissions2-4. However, it is well known from engineering that multiple spatially distributed emitters and receivers can greatly enhance environmental sensing (for example, multistatic radar and sonar)5-8. Here we provide evidence from modelling, neural recordings and behavioural experiments that the African weakly electric fish Gnathonemus petersii utilizes the electrical pulses of conspecifics to extend its electrolocation range, discriminate objects and increase information transmission. These results provide evidence for a new, collective mode of active sensing in which individual perception is enhanced by the energy emissions of nearby group members.

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

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

Evolution of a novel regulatory mechanism of hypoxia inducible factor in hypoxia-tolerant electric fishes.

Hypoxia is a significant source of metabolic stress that activates many cellular pathways involved in cellular differentiation, proliferation, and cell death. Hypoxia is also a major component in many human diseases and a known driver of many cancers. Despite the challenges posed by hypoxia, there are animals that display impressive capacity to withstand lethal levels of hypoxia for prolonged periods of time and thus offer a gateway to a more comprehensive understanding of the hypoxic response in vertebrates. The weakly electric fish genus Brachyhypopomus inhabits some of the most challenging aquatic ecosystems in the world, with some species experiencing seasonal anoxia, thus providing a unique system to study the cellular and molecular mechanisms of hypoxia tolerance. In this study, we use closely related species of Brachyhypopomus that display a range of hypoxia tolerances to probe for the underlying molecular mechanisms via hypoxia inducible factors (HIFs)-transcription factors known to coordinate the cellular response to hypoxia in vertebrates. We find that HIF1⍺ from hypoxia tolerant Brachyhypopomus species displays higher transactivation in response to hypoxia than that of intolerant species, when overexpressed in live cells. Moreover, we identified two SUMO-interacting motifs near the oxygen-dependent degradation and transactivation domains of the HIF1⍺ protein that appear to boost transactivation of HIF1, regardless of the genetic background. Together with computational analyses of selection, this shows that evolution of HIF1⍺ are likely to underlie adaptations to hypoxia tolerance in Brachyhypopomus electric fishes, with changes in two SUMO-interacting motifs facilitating the mechanism of this tolerance.

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

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

Model organisms and systems in neuroethology: one hundred years of history and a look into the future.

The Journal of Comparative Physiology lived up to its name in the last 100 years by including more than 1500 different taxa in almost 10,000 publications. Seventeen phyla of the animal kingdom were represented. The honeybee (Apis mellifera) is the taxon with most publications, followed by locust (Locusta migratoria), crayfishes (Cambarus spp.), and fruitfly (Drosophila melanogaster). The representation of species in this journal in the past, thus, differs much from the 13 model systems as named by the National Institutes of Health (USA). We mention major accomplishments of research on species with specific adaptations, specialist animals, for example, the quantitative description of the processes underlying the axon potential in squid (Loligo forbesii) and the isolation of the first receptor channel in the electric eel (Electrophorus electricus) and electric ray (Torpedo spp.). Future neuroethological work should make the recent genetic and technological developments available for specialist animals. There are many research questions left that may be answered with high yield in specialists and some questions that can only be answered in specialists. Moreover, the adaptations of animals that occupy specific ecological niches often lend themselves to biomimetic applications. We go into some depth in explaining our thoughts in the research of motion vision in insects, sound localization in barn owls, and electroreception in weakly electric fish.

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) in in 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.

Vasotocin but not isotocin is involved in the emergence of the dominant-subordinate status in males of the weakly electric fish, Gymnotus omarorum.

The establishment of the dominant-subordinate status implies a clear behavioral asymmetry between contenders that arises immediately after the resolution of the agonistic encounter and persists during the maintenance of stable dominance hierarchies. Changes in the activity of the brain social behavior network (SBN) are postulated to be responsible for the establishment and maintenance of the dominant-subordinate status. The hypothalamic nonapeptides of the vasopressin (AVP) and oxytocin (OT) families are known to modulate the activity of the SBN in a context-dependent manner across vertebrates, including status-dependent modulations. We searched for status-dependent asymmetries in AVP-like (vasotocin, AVT) and OT-like (isotocin, IT) cell number and activation immediately after the establishment of dominance in males of the weakly electric fish, Gymnotus omarorum, which displays the best understood example of non-breeding territorial aggression among teleosts. We used immunolabeling (FOS, AVT, and IT) of preoptic area (POA) neurons after dyadic agonistic encounters. This study is among the first to show in teleosts that AVT, but not IT, is involved in the establishment of the dominant-subordinate status. We also found status-dependent subregion-specific changes of AVT cell number and activation. These results confirm the involvement of AVT in the establishment of dominance and support the speculation that AVT is released from dominants' AVT neurons.

Reproductive biology of the electric lanternfish Electrona risso (Myctophidae) and the bigscale fishes Melamphaes polylepis and Scopelogadus mizolepis (Melamphaidae).

This study was the first to investigate the key reproductive traits of the electric lantern fish Electrona risso (Myctophidae, n = 918) and the bigscale fishes (Melamphaidae) Melamphaes polylepis (n = 260) and Scopelogadus mizolepis (n = 649). Specimens of these mesopelagic species were collected in March and April 2015 in the eastern Central Atlantic (0-24° N, 20-26° W). Sex ratio was not significantly different from 1:1 in E. risso and M. polylepis but significantly skewed toward female dominance in S. mizolepis. Reproductive phases were determined macroscopically and by histological analyses on selected individuals. Female length at 50% maturity (L50 ) was 55.1 mm standard length (LS ) in E. risso, with an observed female maximum length (Lmax ) of 81.2 mm LS . M. polylepis females had an L50 of 40.2 mm LS and an Lmax of 86.7 mm LS . S. mizolepis had an L50 of 46 mm LS and an Lmax of 97.9 mm LS . The three species show histological features of iteroparity, but the E. risso population appears to occur in two year-classes and experience only one spawning season per lifetime in the study region. All three species are batch-spawners. A batch fecundity of 2668 eggs was estimated from one E. risso individual, with a relative batch fecundity of 369 eggs g-1 gonad-free body mass. M. polylepis had a batch fecundity of 1027 eggs and a relative batch fecundity of 149 eggs g-1 (n = 3). S. polylepis had a batch fecundity of 1545 eggs and a relative batch fecundity of 215 eggs g-1 (n = 21). The median gonado-somatic index during the actively spawning phase of E. risso was 4.5, significantly lower than that of M. polylepis (7.5) and S. mizolepis (7.1). No regressing or regenerating phases were observed in this study. Batch-spawning in all three species is suggested to be advantageous to cope with intra-annual variability in food supply and other risks for offspring survival. With what appears to be in effect a (facultative) semelparous strategy in combination with a short life span in E. risso, interannual differences would have a great effect on population dynamics of this species. Knowledge is still lacking on temporal aspects of reproduction such as the duration of the spawning season and the frequency of spawning, as well as age and growth.

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

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

Androgen receptors rapidly modulate non-breeding aggression in male and female weakly electric fish (Gymnotus omarorum).

The South American weakly electric fish, Gymnotus omarorum, displays territorial aggression year-round in both sexes. To examine the role of rapid androgen modulation in non-breeding aggression, we administered acetate cyproterone (CPA), a potent inhibitor of androgen receptors, to both male and females, just before staged agonistic interactions. Wild-caught fish were injected with CPA and, 30 min later, paired in intrasexual dyads. We then recorded the agonistic behavior which encompasses both locomotor displays and emission of social electric signals. We found that CPA had no discernible impact on the levels of aggression or the motivation to engage in aggressive behavior for either sex. However, CPA specifically decreased the expression of social electric signals in both males and female dyads. The effect was status-dependent as it only affected subordinate electrocommunication behavior, the emission of brief interruptions in their electric signaling ("offs"). This study is the first demonstration of a direct and rapid androgen effect mediated via androgen receptors on non-breeding aggression. Elucidating the mechanisms involved in non-breeding aggression in this teleost model allows us to better understand potentially conserved or convergent neuroendocrine mechanisms underlying aggression in vertebrates.

Living life with an electric touch.

The electric organ discharges (EODs) produced by weakly electric fish have long been a source of scientific intrigue and inspiration. The study of these species has contributed to our understanding of the organization of fixed action patterns, as well as enriching general imaging theory by unveiling the dual impact of an agent's actions on the environment and its own sensory system during the imaging process. This Centenary Review firstly compares how weakly electric fish generate species- and sex-specific stereotyped electric fields by considering: (1) peripheral mechanisms, including the geometry, channel repertoire and innervation of the electrogenic units; (2) the organization of the electric organs (EOs); and (3) neural coordination mechanisms. Secondly, the Review discusses the threefold function of the fish-centered electric fields: (1) to generate electric signals that encode the material, geometry and distance of nearby objects, serving as a short-range sensory modality or 'electric touch'; (2) to mark emitter identity and location; and (3) to convey social messages encoded in stereotypical modulations of the electric field that might be considered as species-specific communication symbols. Finally, this Review considers a range of potential research directions that are likely to be productive in the future.

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

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

Unraveling the complex phylogeographic history of freshwater fishes in Lower Central America: A study of the electric fish Brachyhypopomus occidentalis.

Lower Central America (LCA) has a complex biogeographic history shaped by the rise of the Isthmus of Panama and the global climatic oscillations of the Pleistocene. These events have been crucial in structuring biodiversity in LCA, but their consequences for the distribution and partitions of genetic diversity across the region remain to be elucidated. We combined complete mitochondrial genomes and nuclear ultraconserved elements (UCEs) to study the phylogeographic history and population genetic structure of the electric fish Brachyhypopomus occidentalis in LCA. Our results are consistent with the known phylogeographic history of B. occidentalis in LCA, but we update this history in several important ways that help illuminate the phylogeographic history of freshwater fishes in the region. We provide: i) support for three waves of colonization, two of which occurred prior to the final closure of the Panama Isthmus; ii) a more precise understanding of each colonization event, with evidence for a larger footprint of the first event, as well as genetic exchange across the continental divide in subsequent events; and iii) evidence for high levels of previously unrecognized population genetic structure across LCA. This updated model of colonization and diversification of B. occidentalis consists of three waves of dispersal and colonization, which triggered the evolution of geographic breaks in both nuclear and mitochondrial genomes across LCA. These processes are tightly linked to the dynamic uplift of the Isthmus, recent volcanic activity in the region, and the sea-level oscillations of the Pleistocene. These results improve previous phylogeographic inferences regarding the distribution and diversification of freshwater fishes in LCA, and generate testable hypotheses to guide future research exploring the factors shaping biodiversity in the region.

Brain and circulating steroids in an electric fish: Relevance for non-breeding aggression.

Steroids play a crucial role in modulating brain and behavior. While traditionally it is thought that the brain is a target of sex steroids produced in endocrine glands (e.g. gonads), the brain itself produces steroids, known as neurosteroids. Neurosteroids can be produced in regions involved in the regulation of social behaviors and may act locally to regulate social behaviors, such as reproduction and aggression. Our model species, the weakly electric fish Gymnotus omarorum, displays non-breeding aggression in both sexes. This is a valuable natural behavior to understand neuroendocrine mechanisms that differ from those underlying breeding aggression. In the non-breeding season, circulating sex steroid levels are low, which facilitates the study of neurosteroids. Here, for the first time in a teleost fish, we used liquid chromatography-tandem mass spectrometry (LC-MS/MS) to quantify a panel of 8 steroids in both plasma and brain to characterize steroid profiles in wild non-breeding adult males and females. We show that: 1) systemic steroid levels in the non-breeding season are similar in both sexes, although only males have detectable circulating 11-ketotestosterone, 2) brain steroid levels are sexually dimorphic, as females display higher levels of androstenedione, testosterone and estrone, and only males had detectable 11-ketotestosterone, 3) systemic androgens such as androstenedione and testosterone in the non-breeding season are potential precursors for neuroestrogen synthesis, and 4) estrogens, which play a key role in non-breeding aggression, are detectable in the brain (but not the plasma) in both sexes. These data are consistent with previous studies of G. omarorum that show non-breeding aggression is dependent on estrogen signaling, as has also been shown in bird and mammal models. Overall, our results provide a foundation for understanding the role of neurosteroids, the interplay between central and peripheral steroids and potential sex differences in the regulation of social behaviors.

Evolution of androgen receptors contributes to species variation in androgenic regulation of communication signals in electric fishes.

Hormones and receptors coevolve to generate species diversity in hormone action. We compared the structure and function of androgen receptors (ARs) across fishes, with a focus on ARs in ghost knifefishes (Apteronotidae). Apteronotids, like many other teleosts, have two ARs (ARα and ARß). ARß is largely conserved, whereas ARα sequences vary considerably across species. The ARα ligand binding domain (LBD) has evolved under positive selection, and differences in the LBD across apteronotid species are associated with diversity in androgenic regulation of behavior. The Apteronotus leptorhynchus ARα LBD differs substantially from that of the Apteronotus albifrons ARα or the ancestral AR. Structural modeling and transactivation assays demonstrated that A. leptorhynchus ARα cannot bind androgens. We propose a model whereby relative expression of ARα versus ARß in the brain, coupled with loss of androgen binding by ARα in A. leptorhynchus might explain reversals in androgenic regulation and sex differences in electrocommunication behavior.

BECS-II: an updated bio-inspired electrocommunication system for small underwater robots.

Some weakly electric fish can use electric signals to interact and communicate with each other in dark and complex underwater environments where traditional underwater communication fails. In our previous work, we developed a bio-inspired electrocommunication system (BECS) that serves as an effective alternative to traditional methods in this challenging underwater scenario performing communication at a speed of approximately 1200 bps (bits per second) within approximately 3 m. In this study, a novel underwater wireless communication system (BECS-II) is proposed to upgrade the BECS with much better performance. We first propose theoretical and simulation models for electrocommunication, including the effects of the angular frequency and electrode impedance. A custom-made digital communication system is employed in BECS-II to improve the anti-interference ability and channel capacity of the BECS. In addition, a novel circuit optimization strategy was used to develop a customized circuit to enhance the transmitting and receiving capabilities of the BECS-II. Dual-frequency communication is proposed to meet the communication demands of different tasks by taking inspiration from the task allocation and evolution mechanisms of weakly electric fish. The experimental results showed that BECS-II outperformed BECS in high-frequency mode at both the communication speed (approximately 20 kbps) and distance (approximately 10 m), whereas in low-frequency mode, it extended the communication range by transmitting data up to a distance of approximately 20 m at a speed of approximately 200 bps. A substantial increase in the communication distance can expand the robot motion space in a group and improve group flexibility.

Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.

Studies on population coding implicitly assume that spikes from the presynaptic cells arrive simultaneously at the integrating neuron. In natural neuronal populations, this is usually not the case-neuronal signaling takes time and populations cover a certain space. The spread of spike arrival times depends on population size, cell density and axonal conduction velocity. Here we analyze the consequences of population size and axonal conduction delays on the stimulus encoding performance in the electrosensory system of the electric fish Apteronotus leptorhynchus. We experimentally locate p-type electroreceptor afferents along the rostro-caudal body axis and relate locations to neurophysiological response properties. In an information-theoretical approach we analyze the coding performance in homogeneous and heterogeneous populations. As expected, the amount of information increases with population size and, on average, heterogeneous populations encode better than the average same-size homogeneous population, if conduction delays are compensated for. The spread of neuronal conduction delays within a receptive field strongly degrades encoding of high-frequency stimulus components. Receptive field sizes typically found in the electrosensory lateral line lobe of A. leptorhynchus appear to be a good compromise between the spread of conduction delays and encoding performance. The limitations imposed by finite axonal conduction velocity are relevant for any converging network as is shown by model populations of LIF neurons. The bandwidth of natural stimuli and the maximum meaningful population sizes are constrained by conduction delays and may thus impact the optimal design of nervous systems.

Ontogeny reveals the origin of Gemminger bones in Mormyridae.

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

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.

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

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