A hormone-sensitive communication system in an electric fish

The electric communication system includes both special muscle-derived cells or electrocytes that produce species-typical electric signals, or electric organ discharges (EODs), and specialized sensory receptors, or electroreceptors, that encode the electric fields set up by EODs. Steroid hormones can influence the characteristic properties of both EODs and electroreceptors. Steroids appear to directly effect the anatomy and physiology of the electrocytes that generate an EOD. In contrast, the steroid effect on electroreceptors may be predominantly via an indirect mechanism whereby changes in the spectral characteristics of the EOD appear to induce changes in the spectral sensitivity of electroreceptors. Continued studies of electrosensory and electromotor systems will offer insights into the cellular bases for the development and evolution of steroid-sensitive pathways in the vertebrate nervous system.     

Acoustic communication in an electric fish,Pollimyrus isidori (Mormyridae)

It has been known since von Frisch's work in the 1930's that mormyrid electric fishes are quite sensitive to sound. We now describe a repertoire of natural sounds produced by the mormyrid, Pollimyrus isidori, during breeding and aggression; reception of communication sounds is probably a major function for mormyrid audition. In aquaria, Pollimyrus isidori produce 'grunts', 'moans', 'growls', 'pops' and 'hoots' at various phases during nesting, courtship, and territory defense. All five sounds are produced primarily at night. Territorial males produce grunts, moans and growls during courtship. Vocalizing is stimulated by the presence of a gravid female on the male's territory and decreases with the onset of spawning. Hoots and pops are given during agonistic behavior. Grunts are bursts of acoustic pulses, stereotyped for an individual, with the potential as individual signatures. The electric organ is silent during grunts and moans and is discharged at a reduced rate during growls. The courtship and spawning of Pollimyrus isidori is described.     

Regulation and modulation of electric waveforms in gymnotiform electric fish

Weakly electric gymnotiform fish specialize in the regulation and modulation of the action potentials that make up their multi-purpose electric signals. To produce communication signals, gymnotiform fish modulate the waveforms of their electric organ discharges (EODs) over timescales spanning ten orders of magnitude within the animal’s life cycle: developmental, reproductive, circadian, and behavioral. Rapid changes lasting milliseconds to seconds are the result of direct neural control of action potential firing in the electric organ. Intermediate-term changes taking minutes to hours result from the action of melanocortin peptides, the pituitary hormones that induce skin darkening and cortisol release in many vertebrates. Long-term changes in the EOD waveform taking days to weeks result from the action of sex steroids on the electrocytes in the electric organ as well as changes in the neural control structures in the brain. These long-term changes in the electric organ seem to be associated with changes in the expression of voltage-gated ion channels in two gene families. Electric organs express multiple voltage-gated sodium channel genes, at least one of which seems to be regulated by androgens. Electric organs also express multiple subunits of the shaker (Kv1) family of voltage-gated potassium channels. Expression of the Kv1 subtype has been found to vary with the duration of the waveform in the electric signal. Our increasing understanding of the mechanisms underlying precise control of electric communication signals may yield significant insights into the diversity of natural mechanisms available for modifying the performance of ion channels in excitable membranes. These mechanisms may lead to better understanding of normal function in a wide range of physiological systems and future application in treatment of disease states involving pathology of excitable membranes.     

Coping with flow: behavior, neurophysiology and modeling of the fish lateral line system

With the mechanosensory lateral line fish perceive water motions relative to their body surface and local pressure gradients. The lateral line plays an important role in many fish behaviors including the detection and localization of dipole sources and the tracking of prey fish. The sensory units of the lateral line are the neuromasts which are distributed across the surface of the animal. Water motions are received and transduced into neuronal signals by the neuromasts. These signals are conveyed by afferent nerve fibers to the fish brain and processed by lateral line neurons in parts of the brainstem, cerebellum, midbrain, and forebrain. In the cerebellum, midbrain, and forebrain, lateral line information is integrated with sensory information from other modalities. The present review introduces the peripheral morphology of the lateral line, and describes our understanding of lateral line physiology and behavior. It focuses on recent studies that have investigated: how fish behave in unsteady flow; what kind of sensory information is provided by flow; and how fish use and process this information. Finally, it reports new theoretical and biomimetic approaches to understand lateral line function.     

Postsynaptic potentials in pacemaker cells: A correlate of behavior in command cells of an electric fish

Intracellular recordings were made from pacemaker-command cells of the electric organ discharge (EOD) of the weakly electric fish Eigenmannia virescens. The fish was immobilized with gallamine triethiodide (Flaxedil) which silenced the EOD. A simulated EOD of this fish (ca. 300 Hz) and a sine wave simulating a neighbor, a few Hz higher (+ΔF) or lower (-ΔF) were introduced into the bath to elicit the “jamming avoidance response” (JAR), monitored through the pacemaker potential. We observed that accompanying the JAR there is a minute hyperpolarizing postsynaptic potential (hpsp) superimposed on the pacemaker potential. A shift in the phase of the hpsp occurs with a change in the sign of ΔF, and therefore of the JAR. Assuming that the behaviorally correlated hpsp is inhibitory, it suggests that mutual inhibition may play a role in regulating the synchronous firing frequency of command neurons, which are electrically coupled with one-another. Scheich and Bullock (1974) proposed a neuronal scheme for the JAR in which they suggest that two systems (P and T) operate together in the nervous system. The T system affects the pacemaker cells at a precise, variable phase of the pacemaker cycle. Although the present results indeed reveal a shift in the hpsp with a change in the sign of ΔF, the actual significance of this shift remains to be evaluated. The unexpected direction of the shift suggests either that the hpsp is excitatory at the phases when it occurs, or that effectiveness of inhibition decreases at later phases in this case instead of increasing as in other cases, or that the hpsp opposes the JAR. The parallel P system is probably more important in explaining the JAR, acting by a DC level control rather than a phase control.     

Postsynaptic potentials in pacemaker cells: a correlation of behavior in command cells of an electric fish

Intracellular recordings were made from pacemaker-command cells of the electric organ discharge (EOD) of the weakly electric fish Eigenmannia virescens. The fish was immobilized with gallamine triethiodide (Flaxedil) which silenced the EOD. A simulated EOD of this fish (ca. 300 Hz) and a sine wave simulating a neighbor, a few Hz higher (+deltaF) or lower (-deltaF) were introduced into the bath to elicit the "jamming avoidance response" (JAR), monitored through the pacemaker potential. We observed that accompanying the JAR there is a minute hyperpolarizing postsynaptic potential (hpsp) superimposed on the pacemaker potential. A shift in the phase of the hpsp occurs with a change in the sign of deltaF, and therefore of the JAR. Assuming that the behaviorally correlated hpsp is inhibitory, it suggests that mutual inhibition may play a role in regulating the synchronous firing frequency of command neurons, which are electrically coupled with one-another. Scheich and Bullock (1974) proposed a neuronal scheme for the JAR in which they suggest that two systems (P and T) operate together in the nervous system. The T system affects the pacemaker cells at a precise, variable phase of the pacemaker cycle. Although the present results indeed reveal a shift in the hpsp with a change in the sign of deltaF, the actual significance of this shift remains to be evaluated. The unexpected direction of the shift suggests either that the hpsp is excitatory at the phases when it occurs, or that effectiveness of inhibition decreases at later phases in this case instead of increasing as in other cases, or that the hpsp opposes the JAR. The parallel P system is probably more important in explaining the JAR, acting by a DC level control rather than a phase control.     

Sensory control of behavior in electric fish

The electrosensory system is ideally suited for the integration of behavioral and cellular approaches and, therefore, has led to the most detailed explanations of natural behaviors at the single-cell level. The electric sense shares basic principles in the coding of sensory information with more advanced sensory modalities and thus provides a convenient model system for studying neuronal mechanisms of information processing in general.     

Species recognition in mormyrid weakly electric fish

We investigated group cohesion in four species of African weakly electric fish (Brienomyrus niger, Gnathonemus petersii, Marcusenius cyprinoides and Pollimyrus isidori). The attraction among members of the same and different species served as the criterion for species recognition. To identify possible mechanisms underlying this ability, conspecifics were allowed to interact through a wide-meshed plastic screen with either a pair of confined conspecifics or a pair from a related species. Members of each of the four test species were optimally attracted to their own kind, but also responded selectively to the presence of the other species. These interspecific interactions ranged from attraction to avoidance. The difference in the fish's preference to aggregate in inter- and intraspecific interactions pointed to species-specific social cues that facilitate group cohesion in mormyrid fish. Since all four species respond to each other's electric organ discharge with changes in their own discharge rate, species recognition cannot be merely a function of electroreceptor characteristics but must involve the integration of electroreceptive and other sensory cues.     

Melanocortins regulate the electric waveforms of gymnotiform electric fish

The hypothalamic-pituitary-adrenal/interrenal axis couples serotonergic activity in the brain to the peripheral regulators of energy balance and response to stress. The regulation of peripheral systems occurs largely through the release of peptide hormones, especially the melanocortins (adrenocorticotropic hormone [ACTH] and alpha melanocyte stimulating hormone [α-MSH]), and beta-endorphin. Once in circulation, these peptides regulate a wide range of processes; α-MSH in particular regulates behaviors and physiologies with sexual and social functions. We investigated the role of the HPI and melanocortin peptides in regulation of electric social signals in the gymnotiform electric fish, Brachyhypopomus pinnicaudatus. We found that corticotropin releasing factor, thyrotropin-releasing hormone, and α-MSH, three peptide hormones of the HPI/HPA, increased electric signal waveform amplitude and duration when injected into free-swimming fish. A fourth peptide, a synthetic cyclic-α-MSH analog attenuated the normal circadian and socially-induced EOD enhancements in vivo. When applied to the electrogenic cells (electrocytes) in vitro, only α-MSH increased the amplitude and duration of the electrocyte discharge similar to the waveform enhancements seen in vivo. The cyclic-α-MSH analog had no effect on its own, but blocked or attenuated α-MSH-induced enhancements in the single-cell discharge parameters, demonstrating that this compound functions as a silent antagonist at the electrocyte. Overall, these results strongly suggest that the HPI regulates the EOD communication signal, and demonstrate that circulating melanocortin peptides enhance the electrocyte discharge waveform.     

Central auditory neurophysiology of a sound-producing fish: the mesencephalon of Pollimyrus isidori (Mormyridae)

This paper describes the auditory neurophysiology of the mesencephalon of P. isidori, a soundproducing mormyrid fish. Mormyrids have a specialized pressure-sensitive auditory periphery, and anatomical studies indicate that acoustic information is relayed to the mesencephalic nucleus MD. Fish were stimulated with tone bursts and clicks, and responses of MD neurons were recorded extracellularly. Auditory neurons had best frequencies (BF) and best sensitivities (BS) that fell within the range of frequencies and levels of the natural communication sounds of these fish. BSs were in the range of 0 to — 35 dB (re. 1.0 dyne/cm²). Many of the neurons were tuned (Q_{10 dB}: 2–6), and had BFs in the range of 100–300 Hz where the animal's sounds have their peak energy. A range of different physiological cell types were encountered, including phasic, sustained, and complex neurons. Some of the sustained neurons showed strong phase-locking to tones. Many neurons exhibited non-monotonic rate-level functions. Frequencies flanking the BF often caused a reduction in spontaneous activity suggesting inhibition. Many neurons showed excellent representation of click-trains, and some showed a temporal representation of inter-click-intervals with errors less than 1 ms.Abbreviations BF best frequency - BS best sensitivity - ELa anterior exterolateral toral nucleus - ELp posterior exterolateral toral nucleus - EOCD electric organ command discharge - FFT fast Fourier transform - HRP horseradish peroxidase - ICI inter-clickinterval - MD mediodorsal toral nucleus (=auditory nucleus) - OR onset response rate - PSTH peri-stimulus-time-histogram - R synchronization coefficient - RA response area - SS steady state response rate     

Comparative genomics provides evidence for an ancient genome duplication event in fish

There are approximately 25 000 species in the division Teleostei and most are believed to have arisen during a relatively short period of time ca. 200 Myr ago. The discovery of 'extra' Hox gene clusters in zebrafish (Danio rerio), medaka (Oryzias latipes), and pufferfish (Fugu rubripes), has led to the hypothesis that genome duplication provided the genetic raw material necessary for the teleost radiation. We identified 27 groups of orthologous genes which included one gene from man, mouse and chicken, one or two genes from tetraploid Xenopus and two genes from zebrafish. A genome duplication in the ancestor of teleost fishes is the most parsimonious explanation for the observations that for 15 of these genes, the two zebrafish orthologues are sister sequences in phylogenies that otherwise match the expected organismal tree, the zebrafish gene pairs appear to have been formed at approximately the same time, and are unlinked. Phylogenies of nine genes differ a little from the tree predicted by the fish-specific genome duplication hypothesis: one tree shows a sister sequence relationship for the zebrafish genes but differs slightly from the expected organismal tree and in eight trees, one zebrafish gene is the sister sequence to a clade which includes the second zebrafish gene and orthologues from Xenopus, chicken, mouse and man. For these nine gene trees, deviations from the predictions of the fish-specific genome duplication hypothesis are poorly supported. The two zebrafish orthologues for each of the three remaining genes are tightly linked and are, therefore, unlikely to have been formed during a genome duplication event. We estimated that the unlinked duplicated zebrafish genes are between 300 and 450 Myr. Thus, genome duplication could have provided the genetic raw material for teleost radiation. Alternatively, the loss of different duplicates in different populations (i.e. 'divergent resolution') may have promoted speciation in ancient teleost populations.     

Morphological convergence of pharyngeal jaw structure in durophagous perciform fish

This study investigated the ecomorphology of pharyngeal jaw structure and durophagy in three families of marine teleosts: the Sciaenidae, Haemulidae and Carangidae. Regressions of the bone and muscle mass of pharyngeal jaws were generated to elucidate the differences associated with eating hard-bodied and soft-bodied prey; within-family comparisons revealed significant differences in masses of bones and muscles involved with processing the former. Generally, the durophagous species − Trachinotus carolinus (Carangidae), Pogonias cromis (Sciaenidae) and Anisotremus surinamensis (Haemulidae) − had heavier and stronger pharyngeal toothplates and larger protractor pectoralis muscles, with masses of these musculoskeletal elements ranging from five times to nearly an order of magnitude larger than those of their soft-prey feeding relatives. Pogonias cromis and T. carolinus demonstrate convergence in the ontogeny and morphological modification of the pharyngeal toothplates and protractor pectoralis muscles that enhance crushing ability. In the Haemulidae, moderate size increases in a few pharyngeal jaw elements (and larger overall body size in A. surinamensis ) are sufficient for durophagy. Morphospace analysis of six species from the three families illustrates the strong functional association between the biomechanical properties of prey and the relative sizes of biting and transport mechanisms.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80 , 147−165.     

Marine electric fields and fish orientation

1. Two methods for short-span measurements of DC electric fields in the sea are described. 2. The results indicate a difference between local electric fields (up to 150 muV/m) caused by bottom structures and regional electric fields (up to 60 muV/m) due to electromagnetic processes. 3. The possible relevance of these phenomena to electro-sensitive fishes is discussed.     

Omnidirectional sensory and motor volumes in electric fish

Active sensing organisms, such as bats, dolphins, and weakly electric fish, generate a 3-D space for active sensation by emitting self-generated energy into the environment. For a weakly electric fish, we demonstrate that the electrosensory space for prey detection has an unusual, omnidirectional shape. We compare this sensory volume with the animal's motor volume—the volume swept out by the body over selected time intervals and over the time it takes to come to a stop from typical hunting velocities. We find that the motor volume has a similar omnidirectional shape, which can be attributed to the fish's backward-swimming capabilities and body dynamics. We assessed the electrosensory space for prey detection by analyzing simulated changes in spiking activity of primary electrosensory afferents during empirically measured and synthetic prey capture trials. The animal's motor volume was reconstructed from video recordings of body motion during prey capture behavior. Our results suggest that in weakly electric fish, there is a close connection between the shape of the sensory and motor volumes. We consider three general spatial relationships between 3-D sensory and motor volumes in active and passive-sensing animals, and we examine hypotheses about these relationships in the context of the volumes we quantify for weakly electric fish. We propose that the ratio of the sensory volume to the motor volume provides insight into behavioral control strategies across all animals.