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PubMed1998

Finding food: senses involved in foraging for insect larvae in the electric fish gnathonemus petersii

The weakly electric fish Gnathonemus petersii searches at night for insect larvae in tropical African streams. The aim of this study was to determine the contributions of different sensory modalities to foraging. The time that fish needed to find two randomly placed chironomid larvae was measured. The influence of various senses on search time was investigated by blocking the use of one or more senses. Active electrolocation was used by most fish for prey detection in the dark. In addition, passive electrolocation played a role in some individuals. If light was available, vision could become the dominant sense in some individuals, replacing active electrolocation. The presence of chemical cues decreased prey detection time in most fish. Prey movements also shortened search times when active electrolocation and vision were not possible, indicating that the mechanosensory lateral line also plays a role in the detection of moving prey. The results show that G. petersii uses several senses simultaneously during foraging. Each individual favours a specific combination of the available sensory inputs. If one sensory modality is eliminated, fish can switch to other modalities, indicating that the food detection system is flexible and plastic.

Journal Article↗
PubMed2000

The electric image in weakly electric fish: perception of objects of complex impedance.

Weakly electric fish explore the environment using electrolocation. They produce an electric field that is detected by cutaneous electroreceptors; external objects distort the field, thus generating an electric image. The electric image of objects of complex impedance was investigated using a realistic model, which was able to reproduce previous experimental data. The transcutaneous voltage in the presence of an elementary object is modulated in amplitude and waveform on the skin. Amplitude modulation (measured as the relative change in the local peak-to-peak amplitude) consists of a 'Mexican hat' profile whose maximum relative slope depends on the distance of the fish from the object. Waveform modulation depends on both the distance and the electrical characteristics of the object. Changes in waveform are indicated by the amplitude ratio of the larger positive and negative phases of the local electric organ discharge on the skin. Using the peak-to-peak amplitude and the positive-to-negative amplitude ratio of this discharge, a perceptual space can be defined and correlated with the capacitance and resistance of the object. When the object is moved away, the perceptual space is reduced but keeps the same proportions (homothetically): for a given object, the positive-to-negative amplitude ratio is a linear function of the peak-to-peak amplitude. This linear function depends on the electrical characteristics of the object. However, there are 'families' of objects with different electrical characteristics that produce changes in the parameters of the local electric organ discharge that are related by the same linear function. We propose that these functions code the perceptual properties of an object related to its impedance.

Animals↗
PubMed1988

Electrosensory maps form a substrate for the distributed and parallel control of behavioral responses in weakly electric fish.

Electroreceptors, distributed over the body surface of weakly electric fish, code the local amplitude and phase, or timing of zerocrossing, of the animal's electric signals. These signals are generated by rhythmic discharges of the electric organ and form a dipole-like field around the animal. This field is perturbed by interference with electric fields of other fish as well as by the appearance of objects electrically different from water. The spatial and temporal structure of such perturbations can be interpreted as the electric image of interfering fields and moving objects. This strategy of assessing the environment is called 'electrolocation', a form of 'seeing' with the body surface. Electric images are analyzed in somatotopically ordered strata of neurons within the central nervous system. Primary electrosensory afferents project to somatotopically ordered layers of higher-order neurons in the electrosensory lateral line lobe (ELL) of the hindbrain. Phase and amplitude information are processed in separate layers of the ELL. The phase of the signal in a given region of the body surface is coded by the timing of spikes of spherical cells marking the zerocrossings of the electric signal. This phase information is relayed to lamina 6 of the torus semicircularis of the midbrain. Rises and falls in local amplitude are coded by the activity of different pyramidal cell types, E- and I-units, which project to various laminae of the torus above and below lamina 6. The somatotopic organization of the torus allows for computations of spatial patterns in electrosensory information. Within lamina 6, differences in the phase of signals from different parts of the body surface are computed. Differential-phase information is then relayed to deeper laminae of the torus and remains in topographic register with amplitude information. This organization allows for joint evaluation of spatially related patterns of amplitude and phase modulations on the animal's body surface within local neuronal circuits of the torus. A topographic projection of the torus relays amplitude and differential-phase information to the optic tectum where a further joint evaluation of amplitude and phase serves to control behavioral responses. The control of a particular behavioral performance, the 'jamming avoidance response', is of a distributed nature in that the representations of individual sites on the body surface contribute cumulatively to shift the electric organ pacemaker frequency.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials↗
PubMed1990

Time course of structural changes in regenerating electroreceptors of a weakly electric fish.

We examined the regenerating electroreceptors of the weakly electric fish Sternopygus by light and electron microscopy to search for possible structural correlates of known physiological changes that occur during regeneration (Zakon: J. Neurosci. 6(11):3297-3308, 1986) and to compare them with developing electroreceptors in larval fish (Vischer: Brain Behav. Evol. 33:223-236). Nine days after removal of a patch of cheek skin, new skin had filled the wound and undifferentiated precursor cell clusters were located in the epidermis just above the dermis. Nerve fibers were present near most, but not all, cell clusters. A few recognizable tuberous and ampullary precursor organs were seen at this time. Tuberous organs were composed of a group of large cells surrounded by smaller cells without a lumen and showed the beginning of a cellular plug. Ampullary organs appeared as a ball of cells with a small lumen opening into a nascent canal. Degenerating cells were found within organs, and sometimes entire organs degenerated. These were not innervated. By 2 weeks the large cells of the tuberous organ were developing into sensory cells, while the smaller cells were forming the capsule wall and the underlying basal cells. The characteristic tuberous organ canal filled with loosely packed epidermal cells was evident. The sensory cells of the ampullary organs were visible within the epithelial layer at the base of the lumen, and the large synaptic discs were beginning to form. The sensory cells and postsynaptic terminals contained numerous vesicles. The presynaptic vesicles, which appear in normal receptor cells, remained throughout regeneration and presumably underlie transmitter release. The postsynaptic vesicles appeared transiently in large numbers but declined to adult values by 4 weeks. We presume that these may serve a trophic role. By 3 weeks, organs generally appeared mature and began dividing into daughter organs. The formation of individual receptor organs during regeneration is similar to that observed in development. Receptor organs continued dividing until the appropriate number of organs per afferent was reached for the size of the fish. Although the organization of the receptors appeared generally normal, there were a few anomalies. Some afferents sent sprouts into the epidermis, and, as a result of such sprouting, some of these afferents innervated multiple organs over a greater distance than normal. This was first seen early in regeneration and persisted for as long as 5 months.(ABSTRACT TRUNCATED AT 400 WORDS)

Age Factors↗
PubMed1999

Sex steroids and communication signals in electric fish: a tale of two species.

Weakly electric fish are good model animals to study the evolution of interspecific and sexual differences in communication signals. This is because the neural circuits producing these signals are simple and conserved among related species while the signals are highly species-specific, sexually-dimorphic, and under hormonal control. Here we focus on two related species of weakly electric gymnotiform fish that emit a wave-type discharge. These species differ in the direction of the sexual dimorphism of their electric organ discharge (EOD) frequencies and their propensity to produce aggressive communication signals called 'chirps'. Brown ghost (Apteronotus leptorhynchus) males produce high frequency EODs while females produce low frequency EODs. When presented with an EOD mimic, males chirp frequently, while females seldom chirp. By contrast, black ghost (A. albifrons) males discharge at lower EOD frequencies than females, and there is no sex difference in chirping in this species. Accordingly, non-aromatizable androgens raise EOD frequency in brown ghosts, but lower it in black ghosts. Androgens induce chirping in female brown ghosts, but do not increase the propensity to chirp in female black ghosts. Thus, the difference in sexually-dimorphic communication signals between these two species can be explained by differences in their responses to sex steroids. Future studies will elucidate how the neural circuits generating these signals are differentially sensitive to steroids in these species.

Aggression↗
PubMed1998

Time coding in the midbrain of mormyrid electric fish. I. Physiology and anatomy of cells in the nucleus exterolateralis pars anterior.

In mormyrid electric fish, species-specific electric organ discharge waveforms are thought to be analyzed by the Knollenorgan electroreceptor subsystem. The midbrain anterior and posterior exterolateral nuclei (ELa and ELp) are thought to be the sites of this analysis. This paper is an electrophysiological study of the properties of the neurons in ELa. We recorded intracellularly from three classes of cells within ELa: the afferent axons from the nucleus of the electrosensory lateral line lobe (NELL), the large interstitial cells of ELa and an unidentified cell type. The large cells and the NELL axons were identified by intracellular injection of biocytin and are physiologically similar. Cells in ELa responded to square pulse stimuli with one or more time-locked action potentials with 2.8-3.0 ms latency. Both large cells and NELL axons arborized extensively in ELa and contacted numerous small cells. Based on the pattern of arborizations, we constructed a counter-current flow model of temporal coding by the small cells of ELa. We postulate that individual small cells are not selectively tuned for specific stimulus durations, but rather, the firing patterns of groups of small cells must be analyzed by neurons further up in the sensory hierarchy to determine the stimulus duration.

Action Potentials↗
PubMed2001

Count and spark? The echo response of the weakly electric fish Gnathonemus petersii to series of pulses.

Weakly electric fish of the pulse type electrolocate objects in the dark by emitting discrete electric organ discharges (EODs) separated by intervals of silence. Two neighbouring pulse-type fish often reduce the risk of discharging simultaneously by means of an 'echo response': one fish will respond to a neighbour's EOD with a discharge of its own following at a fixed short latency so that its EOD will occur long before the next EOD of its neighbour. Although working elegantly for two partners, this simple strategy should fail in larger groups because two fish could discharge in response to the same EOD of a third fish. Here, I show that the mormyrid fish Gnathonemus petersii could use a simple mechanism to reduce this problem. Individuals were stimulated with two closely spaced pulses, the second following so as to coincide with an echo given in response to the first. All the fish examined were able to respond more to the second pulse so that most of their echoes did not collide with the second pulse. An analysis was made of how echoing more to the second pulse depends on (i) the delay at which the stimulus followed the last spontaneous EOD, (ii) the spontaneous firing rate, (iii) the intensity of the stimulus, (iv) the number of stimulus pulses, (v) the interval between stimulus pulses, and (vi) the level of previous stimulation with double pulses. The results suggest that echoing more in response to the second pulse is probably because the first pulse causes an after-effect whose inferred properties would be compatible with the properties of the mormyromast afferences thought to be involved in the echo response.

Animals↗
PubMed1994

The African wave-type electric fish, Gymnarchus niloticus, lacks corollary discharge mechanisms for electrosensory gating.

Gymnarchus niloticus, a wave-type African electric fish, performs its jamming avoidance response by relying solely upon afferent signals and does not use corollary discharges from the pacemaker nucleus in the medulla which generates the rhythmicity of electric organ discharges. This is in sharp contrast to the mode of sensory processing found in closely related African pulse-type electric fishes where afferent signals are gated by corollary discharges from the pacemaker for the distinction of exafferent and reafferent stimuli. Does Gymnarchus still possess a corollary discharge mechanism for other behavioral tasks but does not use it for the jamming avoidance response? In this study, I recorded from and labeled medullary neuronal structures that either generate or convey the pacemaker signal for electric organ discharges to examine whether this information is also sent directly to any sensory areas. The pacemaker nucleus was identified as the site of generation of the pacemaking signal. The pacemaker neurons project exclusively to the lateral relay nucleus which, in turn projects exclusively to the medial relay nucleus. Neurons in the medial relay nucleus send unbranched axons to the spinal electromotoneurons. These neurons are entirely devoted to drive the electric organ discharges, and no axon collaterals from these neurons were found to project to any sensory areas. This indicates that Gymnarchus does not possess the neuronal hardware for a corollary discharge mechanism.

Action Potentials↗
PubMed1989

From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish, Eigenmannia.

During their jamming avoidance response (JAR), weakly electric fish of the genus Eigenmannia shift their electric organ discharge (EOD) frequency away from a similar EOD frequency of a neighboring fish. The behavioral rules and neural substrates for stimulus recognition and motor control of the JAR have been extensively studied (see review by Heiligenberg 1986). The diencephalic nucleus electrosensorius (nE) links sensory processing within the torus semicircularis and optic tectum with the mesencephalic prepacemaker nucleus which, in turn, modulates the medullary pacemaker nucleus and hence the EOD frequency. Two separate areas within the nE responsible for JAR-related EOD frequency rises and frequency falls, respectively, were identified by iontophoresis of the excitatory amino acid L-glutamate. Bilateral lesion of the areas causing EOD frequency rises resulted in elimination of JAR-related frequency rises above a baseline frequency obtained in the absence of a jamming stimulus. Similarly, bilateral lesion of the areas causing frequency falls resulted in a loss of JAR-related frequency falls below the baseline frequency. Whether these areas are also responsible for non-JAR-related frequency shifts is not known. The strength of response and spatial extent of the areas causing frequency shifts varied among fish and also varied in individual fish, reflecting the strength of JAR-related frequency shifts and the balance of activities in frequency-rise and frequency-fall areas. Local application of bicuculline-methiodide or GABA demonstrated a tonic inhibitory input to each area and suggests a reciprocal inhibitory interaction between the two ipsilateral areas, possibly accounting for much of the individual plasticity. The nE thus is a site for neuronal transformation from distributed, topographically organized processing within the laminated structures of the torus and tectum to discrete cell clusters which control antagonistic motor responses.

Action Potentials↗
PubMed1992

Electric organ morphology of Sternopygus macrurus, a wave-type, weakly electric fish with a sexually dimorphic EOD.

In several species of electric fish with a sex difference in their pulse-type electric organ discharge (EOD), the action potential-generating cells of the electric organ (electrocytes) of males are larger and more invaginated compared to females. Androgen treatment of females and juveniles produces a longer-duration EOD pulse that mimics the mature male EOD, with a concurrent increase in electrocyte size and/or membrane infolding. In Sternopygus macrurus, which generates a wave-type EOD, androgen also increases EOD pulse duration. To investigate possible morphological correlates of hormone-dependent changes in EOD in Sternopygus, we examined electric organs from both fish collected in the field, and untreated and androgen-treated specimens in the laboratory. The electrocytes are cigar shaped, with prominent papillae on the posterior, innervated end. Electrocytes of field-caught specimens were significantly larger in all parameters than were electrocytes of specimens maintained in the laboratory. EOD pulse duration and frequency were highly correlated, and were significantly different between the sexes in sexually mature fish. Nevertheless, no sex difference in electrocyte morphology was observed, nor did any parameters of electrocyte morphology correlate with EOD pulse duration or frequency. Further, whereas androgen treatment significantly lowered EOD frequency and broadened EOD pulse duration, there was no difference in electrocyte morphology between hormone-treated and control groups. Thus, in contrast to results from studies on both mormyrid and gymnotiform pulse fish, electrocyte morphology is not correlated with EOD waveform characteristics in the gymnotiform wave-type fish Sternopygus. The data, therefore, suggest that sex differences in EOD are dependent on changes in active electrical properties of electrocyte membranes.

Analysis of Variance↗
PubMed1998

Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus).

Inhibition evoked from primary afferents in the electrosensory lateral line lobe of the weakly electric fish (Apteronotus leptorhynchus). J. Neurophysiol. 80: 3173-3196, 1998. The responses of two types of projection neurons of the electrosensory lateral line lobe, basilar (BP) and nonbasilar (NBP) pyramidal cells, to stimulation of primary electrosensory afferents were determined in the weakly electric fish, Apteronotus leptorhynchus. Using dyes to identify cell type, the response of NBP cells to stimulation of primary afferents was inhibitory, whereas the response of BP cells was excitation followed by inhibition. gamma-Aminobutyric acid (GABA) applications produced biphasic (depolarization then hyperpolarization) responses in most cells. GABAA antagonists blocked the depolarizing effect of GABA and reduced the hyperpolarizing effect. The GABAB antagonists weakly antagonized the hyperpolarizing effect. The early depolarization had a larger increase in cell conductance than the late hyperpolarization. The conductance changes were voltage dependent, increasing with depolarization. In both cell types, baclofen produced a slow small hyperpolarization and reduced the inhibitory postsynaptic potentials (IPSPs) evoked by primary afferent stimulation. Tetanic stimulation of primary afferents at physiological rates (100-200 Hz) produced strongly summating compound IPSPs (approximately 500-ms duration) in NBP cells, which were usually sensitive to GABAA but not GABAB antagonists; in some cells there remained a slow IPSP that was unaffected by GABAB antagonists. BP cells responded with excitatory or mixed excitatory + inhibitory responses. The inhibitory response had both a fast (approximately 30 ms, GABAA) and long-lasting slow phase (approximately 800 ms, mostly blocked by GABAA antagonists). In some cells there was a GABAA antagonist-insensitive slow IPSP (approximately 500 ms) that was sensitive to GABAB antagonists. Application of glutamate ionotropic receptor antagonists blocked the inhibitory response of NBP cells to primary afferent stimulation and the excitatory response of BP cells but enhanced the BP cell slow IPSP; this remaining slow IPSP was reduced by GABAB antagonists. Unit recordings in the granule cell layer and computer simulations of pyramidal cell inhibition suggested that the duration of the slow GABAA inhibition reflects the prolonged firing of GABAergic granule cell interneurons to primary afferent input. Correlation of the results with known GABAergic circuitry in the electrosensory lobe suggests that the GABAergic type 2 granule cell input to both pyramidal cell types is via GABAA receptors. The properties of the GC2 GABAA input are well suited to their putative role in gain control, regulation of phasicness, and coincidence detection. The slow GABAB IPSP evoked in BP cells is likely due to ovoid cell input to their basal dendrites.

Animals↗
PubMed2005

Electrophysiological and molecular genetic evidence for sympatrically occuring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus).

For two sympatric species of African weakly electric fish, Campylomormyrus tamandua and Campylomormyrus numenius, we monitored ontogenetic differentiation in electric organ discharge (EOD) and established a molecular phylogeny, based on 2222bp from cytochrome b, the S7 ribosomal protein gene, and four flanking regions of unlinked microsatellite loci. In C. tamandua, there is one common EOD type, regardless of age and sex, whereas in C. numenius we were able to identify three different male adult EOD waveform types, which emerged from a single common EOD observed in juveniles. Two of these EOD types formed well supported clades in our phylogenetic analysis. In an independent line of evidence, we were able to affirm the classification into three groups by microsatellite data. The correct assignment and the high pairwise F(ST) values support our hypothesis that these groups are reproductively isolated. We propose that in C. numenius there are cryptic species, hidden behind similar and, at least as juveniles, identical morphs.

Africa↗
PubMed1996

Short-range orientation in electric fish: an experimental study of passive electrolocation.

Gymnotiform electric fish are capable of locating and approaching an electrically discharging conspecific over a range of 1-2 m in a behavior called passive electrolocation. This paper investigates the movements of two species in experiments with approaches to stationary dipoles that are either silenced or jumped to a new direction during an approach. Gymnotus carapo fail to find an electrode source in trials in which the dipole electrode is switched off in mid-track. They slow their approach, become disoriented and drift away from the target within seconds of the field being switched off. This result suggests that the fish are unable to construct a cognitive map of a dipole source from brief exposure to local electrosensory stimuli. The second set of trials shows that Brachyhypopomus diazi and Gymnotus carapo bend their body to track electric vectors which are suddenly jumped to a new direction. The latency of the bend response is 0.5 s after the jump. Bending initiates a turn that reduces to zero the error between the fish's direction and the electric field vector and helps keep the fish aligned with the local electric field vector. Together, these experiments suggest that passive electrolocation is stimulus-bound and that these fish find the electrical sources simply by tracking instantaneous local electric current vectors.

Animals↗
PubMed1986

A time-comparison circuit in the electric fish midbrain. II. Functional morphology.

The weakly electric fish Eigenmannia is able to detect temporal disparities as small as 400 nsec between two signals from different parts of the body surface (Carr et al., 1986). The elements of this time-comparison circuit have been identified by EM reconstruction of its component cells. Information about the timing of the zero-crossing of signals on each area of the body surface is coded in phase-coder receptors, a subset of tuberous electroreceptors. Electroreceptors on the body surface are innervated by primary afferents with their central termination on the spherical cells of the medullary electrosensory lateral line lobe. These cells project to lamina VI of the midbrain torus, a structure similar to the inferior colliculus. Afferents entering lamina VI form a very restricted terminal arbor in which they synapse on the three cell types of this lamina. Each afferent makes gap-junction synapses on one or two giant cell somata and morphologically mixed synapses on the distal dendrites of two types of small cell. The afferent terminals thus encode the timing of the electric signal on a local patch of the body surface, forming a somatotopic map of the body surface in lamina VI. The giant cells are adendritic and their axonal arbor is such as to distribute timing information originating from one part of the body surface throughout lamina VI, so that each region of lamina VI receives information about the timing of zero-crossings from the entire body surface from giant cells, as well as information from a local portion of the body surface from the afferent terminals. The giant cells terminate exclusively on the cell bodies of the small cells of lamina VI, shown to be sensitive to small temporal disparities by Heiligenberg and Rose (1985). Thus, each small cell receives a single synapse on its soma from a giant cell that conveys phase-coding information from some portion of the body surface and receives local phase-coding input onto its dendrites from spherical cell afferents. The sensitivity of the small cells to temporal disparities appears to be conferred by their segregation of inputs from two different parts of the body surface onto dendrites and soma, respectively. We propose that the dendritic input acts as a delay line, and the small cell fires maximally when the inputs from the dendrites and the giant cell input onto the soma coincide.

Animals↗
PubMed1996

Sensory cues for the gradual frequency fall responses of the gymnotiform electric fish, Rhamphichthys rostratus.

The sensory cues for a less known form of frequency shifting behavior, gradual frequency falls, of electric organ discharges (EODs) in a pulse-type gymnotiform electric fish, Rhamphichthys rostratus, were identified. We found that the gradual frequency fall occurs independently of more commonly observed momentary phase shifting behavior, and is due to perturbation of sensory feedback of the fish's own EODs by EODs of neighboring fish. The following components were identified as essential features in the signal mixture of the fish's own and the neighbor's EOD pulses: (1) the neighbor's pulses must be placed within a few millisecond of the fish's own pulses, (2) the neighbor's pulses, presented singly at low frequencies (0.2-4 Hz), were sufficient, (3) the frequency of individual pulse presentation must be below 4 Hz, (4) amplitude modulation of the sensory feedback of the fish's own pulses induced by such insertions of the neighbor's pulses must contain a high frequency component: sinusoidal amplitude modulation of the fish's own EOD feedback at these low frequencies does not induce gradual frequency falls. Differential stimulation across body surfaces, which is required for the jamming avoidance response (JAR) of wave-type gymnotiform electric fish, was not necessary for this behavior. We propose a cascade of high-pass and low-pass frequency filters within the amplitude processing pathway in the central nervous system as the mechanism of the gradual frequency fall response.

Animals↗
PubMed1975

Comparative studies of the aggressive behaviour of two gymnotid electric fish (Gymnotus carapo and Hypopomus artedi).

Electrical and motor behaviour was studied during aggressive interactions in two species of electric fish (Gymnotus carapo and Hypopomus artedi). Paired comparison methods were used to obtain the data, and analysis of the results was undertaken at three different levels: (1) The repertoire of behaviour (motor and electrical); (2) The changes in relative frequency of components with increasing exposure to conspecifics; (3) Sequential analysis of patterns of behaviour occuring both within and between individuals. The results of the three analyses showed: (1) A great similarity in repertoire although a much higher rate of interaction for Gymnotus. The relative importance of the "off" and "burst" signals was reversed for the two species. A prolonged orientation component in Hypopomus was found to be related to the occurrence of discharge synchrony. (2) Habituation of intense components in favour of electrical signalling in both species. (3) Important differences in both the length and structure of sequences.

Aggression↗
PubMed1977

The jamming avoidance response in Rhamphichthys rostratus: an alternative principle of time domain analysis in electric fish.

A Jamming Avoidance Response was found in the weakly electric fish Rhamphichthys rostratus, a South American pulse-Gymnotid. The analysis of the response suggests that it requires a key stimulus which is fundamentally different from that in previously described harmonic Gymnotids. It relies on a sensitivity for the direction of phase shifts of stimulus pulses relative to the fish's own electric organ discharge rather than on a sensitivity for beating frequencies.

Animals↗