Walter Heiligenberg

Court and spark: electric signals in the courtship and mating of gymnotoid fish

Abstract By mimicking tropical rainy season conditions in aquaria, we stimulated two species of gymnotoid electric fish, Eigenmannia virescens and Apteronotus leptorhynchus , to spawn in captivity. Their courtship activity, breeding behaviour and electric social communication were monitored in several groups over 2 years. Groups of both species established dominance hierarchies correlated with electric organ discharge frequency, aggressiveness and size. Spawning was preceded by several nights of courtship during which the male modulated its electric organ discharge to produce ‘chirps’. Continual bouts of chirping lasted for hours on evenings prior to spawning. These electrical signals play a significant role in courtship and spawning, as gravid E. virescens females could be stimulated to spawn by playing back into the tank a tape recording of male courtship chirps. In both species the chirp invovves a slight increase in frequency followed by a cessation of the dominant frequency. This suggests a common mode of signal production in these two different genera of fish. Chirps are short and abrupt during aggressive encounters, but assume a softer and more raspy quality during courtship.

Electrolocation of objects in the electric fishEigenmannia (Rhamphichthyidae, Gymnotoidei)

SummaryThe electric fish,Eigenmannia, is able to sense objects which differ in electrical conductivity from the surrounding water by detecting distortions of the current field associated with its electric organ discharges. While resting,Eigenmannia hovers near electrically-detectable objects and follows their motions. When such objects are swung in a sinusoidal manner, the fish follows with a certain gain and phase lag. This allows one to quantify performance in “electrolocation” in terms of gain and phase values as functions of frequency of object motion, object size and distance. As these parameters reach threshold values, the gain of the animals Following Response approaches zero while its phase lag tends toward-π. Electrolocation deteriorates under “jamming” conditions, i.e. in the presence of electric signals with frequencies near the animals discharge frequency.Eigenmannia prevents the deterioration of electrolocation by shifting its frequency away from noise frequencies.

Labelling of electroreceptive afferents in a gymnotoid fish by intracellular injection of HRP: The mystery of multiple maps

SummaryPhysiologically identified primary electroreceptive afferents in the gymnotiform fish,Eigenmannia, were labelled by intracellular injection of horseradish peroxidase (HRP) in order to determine their termination sites in the posterior lateral line lobe (PLLL) (Fig. 1). For each terminal field we mapped the location of the associated receptor pore on the body surface and found:1)Ampullary units project in a somatotopically ordered manner to the medial PLLL.2)Tuberous units, both P- and T-types, project in a somatotopically ordered manner to three separate regions of the PLLL, called central-medial, central-lateral and lateral (Figs. 2–4). Each tuberous unit projects to all three maps and the projections of P- and T-units are in somatotopic register. In addition to electroreceptive units, mechanoreceptive units were also encountered in the anterior lateral line nerve ganglion, but their central projections were found outside of the PLLL, in the anterior lateral line lobe (ALLL) and in the eminentia granularis. This finding is in accordance with the notion of modality-specific separation of central projections, forwarded by Maler et al. (1974).Tuberous electroreceptive afferents have larger somata and faster nerve conduction the further their receptor pores are located towards the tail end of the body (Fig. 5, 6). The faster nerve conduction of afferents from more distant regions of the body surface minimizes temporal disparity in the arrival of spikes linked to synchronous electrical events in widely separated regions of the body surface.

How sensory maps could enhance resolution through ordered arrangements of broadly tuned receivers

We investigate the properties of a model recently introduced by Heiligenberg (1987) for an array of sensors tuned to progressively higher ranges of a continuous stimulus variablex and with bell shaped single response curve with width parameterd. The main result is that asd increases, the overall response rapidly becomes almost linear in a very smooth and robust fashion. Biological relevance and implications of the model and of its extensions are discussed together with a few examples.

The Jamming Avoidance Response inEigenmannia revisited: The structure of a neuronal democracy

SummaryThe Jamming Avoidance Response (JAR) is a gradual shift in frequency of the fishs electric organ pacemaker in an attempt to increase a small difference,δf, between the fundamental frequency of electric organ discharges (EODs) of a conspecific and that of the animals own EODs. The JAR can be elicited in curarized animals by replacing the silenced EOD with a periodic electric stimulus, S1; and by simulating EODs of a conspecific with a periodic stimulus, S2, whose frequency differs byδf from the frequency of S1. Similar to the natural JAR, the frequency of the pacemaker will rise and fall in response to negative and positiveδfs respectively, provided that S1; but not S2, shares critical features with the EOD of the animal. Ambivalent or even opposite responses (Anti-JARs) may result if S1 lacks critical EOD features (Fig. 1). In search of these features the following results were obtained.1.To elicit JARs, S1 need not be phaselocked to the pacemaker. The JAR can thus be driven exclusively by electroreceptive afference, without reference to the pacemaker.2.S1 and S2 may be pure sinewaves as long as their field geometries differ sufficiently. Higher harmonics, which may be added to a sinewave to mimic the EOD wave shape, are required only if S1 and S2 have identical geometries, i.e., if they are presented through the same pair of electrodes. The animal may thus use two different strategies to determine the sign of theδf: one which is based on differences in stimulus field geometries and one which is based on the presence of higher harmonics. Only the former is considered in the following.3.The S1, but not the S2, field geometry should approximate the natural EOD field geometry. To the extent that this condition is violated, sufficiently high S2 intensities may elicit Anti-JARs (Fig. 4).4.Evidence is given that the JAR is controlled, in a cumulative manner, by local interactions of neighboring electroreceptive fields on the animals body surface which, as a consequence of different S1 and S2 field geometries, experience different degrees of contamination of S1 by S2. Simultaneous stimulations of remote areas of body surface result in almost linear summation of their associated effects on the pacemaker (Figs. 5, 6). Theoretically, no unitary central EOD representation is required.5.Based on the results in 3. und 4., we propose that correct JARs are elicited to the extent that the majority of electroreceptors is predominantly driven by Sl rather than by S2, and this condition is fulfilled to the extent that the S1 field geometry approximates that of the natural EOD.6.Effective S2 stimuli have a periodicity near that of the EOD (S1) fundamental frequency, f. This includes all stimuli with a power peak at a frequency of n·f+δf, n=l,2,3,t (Fig. 2), with the optimalδf being 3 to 8 Hz and identical for all n. Such stimuli cause consistent distortions in successive EODs (S1 pulses), which gradually travel through the EOD (S1) cycle (Fig. 3). This “motion” leads to periodic fluctuations in the amplitude of the joint signal, EOD (S1)+S2, and the phase of its positive zero-crossings with regard to those of the EOD (S1 (Fig. 7). The modulation of these two variables can be represented by a motion along a closed graph in a two-dimensional state plane (Fig. 8), which is reproducedδf times per s. The direction of motion along this graph reflects the sign of theδf. Evidence is given that this motion is detected by a mechanism comparable to a motion detector in the realm of vision.

Motor control of the jamming avoidance response of Apteronotus leptorhynchus: evolutionary changes of a behavior and its neuronal substrates

The two closely related gymnotiform fishes, Apteronotus and Eigenmannia, share many similar communication and electrolocation behaviors that require modulation of the frequency of their electric organ discharges. The premotor linkages between their electrosensory system and their medullary pacemaker nucleus, which controls the repetition rate of their electric organ discharges, appear to function differently, however. In the context of the jamming avoidance response, Eigenmannia can raise or lower its electric organ discharge frequency from its resting level. A normally quiescent input from the diencephalic prepacemaker nucleus can be recruited to raise the electric organ discharge frequency above the resting level. Another normally active input, from the sublemniscal prepacemaker nucleus, can be inhibited to lower the electric organ discharge frequency below the resting level (Metzner 1993). In contrast, during a jamming avoidance response, Apteronotus cannot lower its electric organ discharge frequency below the resting level. The sublemniscal prepacemaker is normally completely inhibited and release of this inhibition allows the electric organ discharge frequency to rise during the jamming avoidance response. Further inhibition of this nucleus cannot lower the electric organ discharge frequency below the resting level. Lesions of the diencephalic prepacemaker do not affect performance of the jamming avoidance response. Thus, in Apteronotus, the sublemniscal prepacemaker alone controls the change of the electric organ discharge frequency during the jamming avoidance response.

Comparison of the jamming avoidance responses in Gymnotoid and Gymnarchid electric fish: A case of convergent evolution of behavior and its sensory basis

Summary1.A behavioral response conforming to defining features of the jamming avoidance response (JAR) previously reported inEigenmannia andApteronotus of the Cypriniformes is found inGymnarchus of the Mormyriformes.2.Other parallel specializations of these groups are noted, of which the most relevant is the character of the electric organ discharge (EOD); it is quasisinusoidal, high in repetition rate and highly regular in each of the genera. The same features are found inSternopygus but it lacks a JAR.3.The EOD is compared inGymnarchus, Eigenmannia, Apteronotus andSternopygus, in respect to power spectrum and regularity.4.Other special features of the EOD inGymnarchus are described, including “singing” and a miniature EOD of a different frequency from the main EOD.5.The JAR inGymnarchus, compared toEigenmannia andApteronotus is longer in latency, slower in reaching plateau, smaller in maximum frequency shift and best excited by a stimulus frequency closer to its own. The voltage gradient threshold (≪2.5μV/cm) is higher and the dynamic range smaller. Some correlations with habit of life are suggested.6.Two types of electroreceptors seem particularly relevant to the JAR. They are similar to the T and P units already reported inEigenmannia but substantial differences require separate designations; we call them Type S and Type O units.7.Type S units are like T units but spontaneous at high rates and phase coding over a limited intensity range near threshold. Over a wide range of intensity, including much of the physiological range normally encountered the S unit cannot encode intensity.8.Type O units are like P units but usefully coding in a narrow intensity range; they are often unable to reach 1∶1 following. The threshold is usually about 20 db higher than in S units.9.The filter properties of both types are those of a bandpass filter. Whereas the O units are sharply tuned to the EOD frequency, the S units have a flat passband over a range of about 150 Hz, and sharp cutoffs (about 50 db/octave) on both the high and low frequency sides.

Theoretical and experimental approaches to spatial aspects of electrolocation

SummaryThe shape of an electric fishs field, within an aquarium of finite size, was calculated by numerical computer simulation (Figs. 3, 4). An object differing in conductivity from the surrounding water distorts the electric field of the fish. The associated changes in potential on the animals body surface are monitored by electroreceptors and thus represent the “electric image” of the object (Fig. 6). The “intensity” of this image decays approximately with a negative power function of the distance between object and fish (Fig. 11). Body geometry, such as an elongated tail, as well as resistances of the interior body and skin are of prime importance for electrolocation performance (Figs. 7, 8, 10). Some theoretical conclusions are supported by neurophysiological and behavioral data (Figs. 12, 13), others still have to be tested experimentally.

Evolutionary designs for electric signals and electroreceptors in gymnotoid fishes of Surinam

Summary1.Field collections of gymnotoid electric fish in coastal Surinam streams; 23 March–6 April, 1976, yielded 11 species belonging to two families (Rhamphichthyidae and Gymnotidae). Electric organ discharges (EODs) were recorded and power spectra were generated by Fourier analysis. Each species could be classified as either wave or pulse type. Although EODs varied from species to species, individuals had species-typical discharges. EODs appear to function in electrolocation and electric communication. Coexisting pulse fish diverged in either pulse spectrum or pulse repetition rate. Although each species showed ecological preferences for one habitat or another, no general correlation was found between EOD form and habitat type (Fig. 1).2.Three species of coexisting Hypopomus showed widely differing EOD durations. Peak spectral energies were nonoverlapping (Fig. 4a).3.Electrophysiologic studies of the electroreceptors in Hypopomus species revealed five types of electroreceptors. Two types of units appear to act as EOD filters, responding maximally to spectral frequencies characteristic of the peak power of the species-specific EOD (Fig. 7).4.Relationships between EOD rate and spectrum are discussed with reference to their roles in communication and in electrolocation. A theory for the evolution of EOD wave forms is presented (Fig. 9).

The coding of signals in the electric communication of the gymnotiform fish Eigenmannia : from electroreceptors to neurons in the torus semicircularis of the midbrain

SummaryIn the context of aggression and courtship, Eigenmannia repeatedly interrupts its electric organ discharges (EODs) These interruptions (Fig. 1) contain low-frequency components as well as high-frequency transients and, therefore, stimulate ampullary and tuberous electroreceptors, respectively (Figs. 2, 3). Information provided by these two classes of receptors is relayed along separate pathways, via the electrosensory lateral line lobe (ELL) of the hindbrain, to the dorsal torus semicircularis (TSd) of the midbrain. Some neurons of the torus receive inputs from both types of receptors (Figs. 14, 15), and some respond predominantly to EOD interruptions while being rather insensitive to other forms of signal modulations (Figs. 12, 13). This high selectivity appears to result from convergence and gating of inputs from individually less selective neurons.