The captivating effect of electric organ discharges: species, sex, and orientation are embedded in every single received image

Some fish communicate using pulsatile, stereotyped electric organ discharges (EODs) that exhibit species- and sex-specific time courses. To ensure reproductive success, they must be able to discriminate conspecifics from sympatric species in the muddy waters they inhabit. We have previously shown that they use the electric field lines as a tracking guide to approach conspecifics (electrotaxis) in both Gymnotus and Brachyhypopomus genera. Here we show that the social species Brachyhypopomus gauderio uses electrotaxis to arrive abreast a conspecific, coming from behind. Stimulus image analysis shows that, even in a uniform field, every single EOD causes an image in which the gradient and the local field time courses contain enough information to allow the fish to evaluate conspecific sex, and to find the path to reach it. Using a forced-choice test we show that sexually mature individuals orient themselves along a uniform field in the direction encoded by the time course characteristic of the opposite sex. This indicates that these fish use the stimulus image profile as a spatial guidance clue to find a mate. Embedding species, sex, and orientation cues is a particular example of how species can encode multiple messages in the same self-generated communication signal carrier, allowing for other signal parameters (e.g., EOD timing) to carry additional, often circumstantial, messages. This ‘multiple messages’ EOD embedding approach expressed in this species is likely to be a common and successful strategy widespread across evolutionary lineages and among varied signaling modalities.

Derived loss of signal complexity and plasticity in a genus of weakly electric fish

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. Signal mimicry, mate recognition, and sexual selection are potential factors maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.

Glutamatergic Control Of A Pattern-Generating Central Nucleus In A Gymnotiform Fish

The activity of central pattern-generating networks (CPGs) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. Gymnotus omarorum, a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. G. omarorum emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication, under the command of an electromotor CPG. This nucleus is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. Descending influences target CPG neurons to produce adaptive behavioral electromotor responses to different environmental challenges. We used electrophysiological and pharmacological techniques in brainstem slices of G. omarorum to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptor subtypes. We also show that glutamatergic control of the CPG likely involves two types of synapses contacting pacemaker cells, one type containing both AMPAR-NMDAR receptors and the other one only-NMDAR. Fast neurotransmitter control of vertebrate CPGs seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs. The prospect of common neural designs to control CPG activity in vertebrates is discussed.

The weakly electric fish, Apteronotus albifrons, actively avoids experimentally induced hypoxia

Anthropogenic environmental degradation has led to an increase in the frequency and prevalence of aquatic hypoxia (low dissolved oxygen concentration, DO), which may affect habitat quality for water-breathing fishes. The weakly electric black ghost knifefish, Apteronotus albifrons, is typically found in well-oxygenated freshwater habitats in South America. Using a shuttle-box design, we exposed juvenile A. albifrons to a stepwise decline in DO from normoxia (> 95% air saturation) to extreme hypoxia (10% air saturation) in one compartment and chronic normoxia in the other. On average, A. albifrons actively avoided the hypoxic compartment below 22% air saturation. Hypoxia avoidance was correlated with upregulated swimming activity. Following avoidance, fish regularly ventured back briefly into deep hypoxia. Hypoxia did not affect the frequency of their electric organ discharges. Our results show that A. albifrons is able to sense hypoxia at non-lethal levels and uses active avoidance to mitigate its adverse effects.

Spike-frequency dependent coregulation of multiple ionic conductances in fast-spiking cells forces a metabolic tradeoff

ABSTRACTHigh-frequency action potentials (APs) allow rapid information acquisition and processing in neural systems, but create biophysical and metabolic challenges for excitable cells. The electric fish Eigenmannia virescens images its world and communicates with high-frequency (200-600 Hz) electric organ discharges (EODs) produced by synchronized APs generated at the same frequency in the electric organ cells (electrocytes). We cloned three previously unidentified Na+-activated K+ channel isoforms from electroctyes (eSlack1, eSlack2, and eSlick1). In electrocytes, mRNA transcript levels of the rapidly-activating eSlick, but not the slower eSlack1 or eSlack2, correlated with EOD frequency across individuals. In addition, transcript levels of an inward-rectifier K+ channel, a voltage-gated Na+ channel, and Na+,K+-ATPases also correlated with EOD frequency while a second Na+ channel isoform did not. Computational simulations showed that maintaining electrocyte AP waveform integrity as firing rates increase requires scaling conductances in accordance with these mRNA expression correlations, causing AP metabolic costs to increase exponentially.

Derived loss of signal complexity and plasticity in a genus of weakly electric fish

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. We discuss potential the roles of signal mimicry, species recognition, and sexual selection in maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.

Glutamatergic Control Of A Pattern-Generating Central Nucleus In A Gymnotiform Fish

ABSTRACTThe activity of pattern-generating networks (CPG) may change under the control exerted by various neurotransmitters and modulators to adapt its behavioral outputs to different environmental demands. Although the mechanisms underlying this control have been well established in invertebrates, most of their synaptic and cellular bases are not yet well understood in vertebrates. Gymnotus omarorum, a pulse-type gymnotiform electric fish, provides a well-suited vertebrate model to investigate these mechanisms. G. omarorum emits rhythmic and stereotyped electric organ discharges (EODs), which function in both perception and communication. The EOD is considered the behavioral output of an electromotor CPG which, modulated by descending influences, organizes adaptive electromotor behaviors in response to environmental and social challenges. The CPG is composed of electrotonically coupled intrinsic pacemaker cells, which pace the rhythm, and bulbospinal projecting relay cells that contribute to organize the pattern of the muscle-derived effector activation that produce the EOD. We used electrophysiological and pharmacological techniques in brainstem slices of G. omarorum to investigate the underpinnings of the fast transmitter control of its electromotor CPG. We demonstrate that pacemaker, but not relay cells, are endowed with ionotropic and metabotropic glutamate receptors subtypes. We also show, for the first time in gymnotiformes, that glutamatergic control of the CPG likely involves both AMPA-NMDA receptors transmitting and only-NMDA segregated synapses contacting pacemaker cells. Our data shed light on the fast neurotransmitter control of a vertebrate CPG that seems to exploit the kinetics of the involved postsynaptic receptors to command different behavioral outputs.NEW & NOTEWORTHYUnderpinnings of neuromodulation of pattern-generating central networks (CPG) have been well characterized in many species. The effects of fast neurotransmitter systems remain, however, poorly understood. This research uses in vitro electrophysiological and pharmacological techniques to show that the neurotransmitter control of a vertebrate CPG in gymnotiform fish involve the convergence of only-NMDA and AMPA-NMDA glutamatergic synapses onto neurons that pace the rhythm. These inputs may organize different behavioral outputs according to their distinct functional properties.

The weakly electric fish, Apteronotus albifrons, avoids hypoxia before it reaches critical levels

Anthropogenic environmental degradation has led to an increase in the frequency and prevalence of aquatic hypoxia (low dissolved-oxygen concentration, DO), which may affect habitat quality for water-breathing fishes. The weakly electric black ghost knifefish, Apteronotus albifrons, is typically found in well-oxygenated freshwater habitats in South America. Using a shuttle-box design, we exposed juvenile A. albifrons to a stepwise decline in DO from normoxia (>95% air saturation) to extreme hypoxia (10% air saturation) in one compartment and chronic normoxia in the other. Below 22% air saturation, A. albifrons actively avoided the hypoxic compartment. Hypoxia avoidance was correlated with upregulated swimming activity. Following avoidance, fish regularly ventured back briefly into deep hypoxia. Hypoxia did not affect the frequency of their electric organ discharges. Our results show that A. albifrons is able to sense hypoxia at non-lethal levels and uses active avoidance to mitigate its adverse effects.SummaryThe weakly electric knifefish, Apteronotus albifrons, avoids hypoxia below 22% air saturation. Avoidance correlates with increased swimming activity, but not with a change in electric organ discharge frequency.