‘Communication’ in weakly electric fish, Gnathonemus niger (Mormyridae) I. Variation of electric organ discharge (EOD) frequency elicited by controlled electric stimuli

The weakly electric fish, Gathonemus niger, discharged with a frequency of 4 to 8 Hz during the day and 10 to 16 Hz during the night. The frequency of superimposed burst discharges (32 to 56 Hz) was independent of diurnal factors. The variation of the electric organ discharge frequency during the day was investigated in response to controlled electric stimulus patterns: (a) A free running stimulus frequency of 4 Hz, simulating the resting frequency of another fish, and different stimulus intensities, simulating different distances between two fish. (b) Free running frequencies of 4, 8, 16, …, 128 Hz and two particular stimulus intensities. (c) Discharge coupled stimuli (each discharge triggered an electric stimulus with a fixed delay) and different stimulus intensities.All three kinds of stimuli elicited defined and predictable response discharge patterns supporting the assumption that an electric fish would respond to a particular discharge pattern of another fish also in a similar and predictable manner. Low stimulus intensities (0·04 to 0·2 mV per cm) caused cessation of the discharge activity, a ‘hiding’ or ‘listening’ response. The discharge rate increased linearly with the logarithm of the stimulus intensity. The fish was particularly sensitive to stimulus frequencies which simulated its burst activity (32 to 56 Hz). Discharge coupled stimuli showed that the fish responded to about eight times lower stimulus intensities if the stimulus occurred between two discharges (15 to 30 m-s after the fish's discharge) than if the stimulus occurred within or immediately after the discharge. All suprathreshold stimuli elicited a typical discharge pattern: The irregular resting discharge activity became significantly regular. The degree of regularity was even improved during maintained stimulation. The regularisation of the discharge activity is thought to be involved in the fish's electrolocating system whereas frequency variations are considered as being involved in both the locating system and as communication signals among weakly electric fish.     

Phase and amplitude maps of the electric organ discharge of the weakly electric fish,Apteronotus leptorhynchus

Summary The electric organ discharge (EOD) potential was mapped on the skin and midplane of several Apteronotus leptorhynchus. The frequency components of the EOD on the surface of the fish have extremely stable amplitude and phase. However, the waveform varies considerably with different positions on the body surface. Peaks and zero crossings of the potential propagate along the fish's body, and there is no point where the potential is always zero. The EOD differs significantly from a sinusoid over at least one third of the body and tail. A qualitative comparison between fish showed that each individual had a unique spatiotemporal pattern of the EOD potential on its body.The potential waveforms have been assembled into high temporal and spatial resolution maps which show the dynamics of the EOD. Animation sequences and Macintosh software are available by anonymous ftp (mordor.cns.caltech.edu; cd/pub/ElectricFish).We interpret the EOD maps in terms of ramifications on electric organ control and electroreception. The electrocytes comprising the electric organ do not all fire in unison, indicating that the command pathway is not synchronized overall. The maps suggest that electroreceptors in different regions fulfill different computational roles in electroreception. Receptor mechanisms may exist to make use of the phase information or harmonic content of the EOD, so that both spatial and temporal patterns could contribute information useful for electrolocation and communication.Abbreviations EOD electric organ discharge - EO electric organ - CV coefficient of variance     

Cyclic AMP modulates electrical signaling in a weakly electric fish

Many species of electric fish show diurnal or socially elicited variation in electric organ discharge amplitude. In Sternopygus macrurus, activation of protein kinase A by 8-bromo-cAMP increases electrocyte sodium current magnitude. To determine whether the behavioral plasticity in electric organ discharge amplitude is controlled by electrocyte biophysical properties, we examined whether the effects of phosphorylation on ion currents in the electric organ translate directly into electric organ discharge changes. We injected the electric organ of restrained fish with 8-bromo-cAMP and monitored the electric organ discharge. The effect of protein kinase A activation on electrocyte action potentials was examined in isolated electric organ using two-electrode current clamp. Electric organ discharge and action potential amplitude and pulse duration increased in response to 8-bromo-cAMP. Pulse and action potential duration both increased by about 25%. However, the increase in electric organ discharge amplitude (approximately 400%) was several-fold greater than the action potential amplitude increase (approximately 40%). Resting membrane resistance decreased in electrocytes exposed to 8-bromo-cAMP. We propose that in the Thevenin equivalent circuit of the electric organ a moderate increase in action potential amplitude combined with a decrease in internal resistance produces a greater voltage drop across the external resistance (the water around the fish), accounting for the large increase in the externally recorded electric organ discharge.     

Possible involvement of the ampullary electroreceptor system in detection of frequency-modulated electrocommunication signals in Eigenmannia

Behavioral and electrophysiological experiments were conducted to examine whether frequency-modulated electrocommunication signals are detected by the ampullary electroreceptor system in Eigenmannia. First, frequency-modulated electric organ discharges were found to contain a low-frequency component that could be detected by the ampullary system. Second, fish were successfully trained to distinguish a frequency-modulated signal, which contained a low-frequency component as in natural signals, from an artificial signal in which the low-frequency component was eliminated but still modulated in frequency. Subsequently, the trained fish responded without reinforcement to a low-frequency sinusoidal signal which mimicked the low-frequency component in the frequency-modulated signal, suggesting that the fish used the ampullary system to detect frequency modulation. Finally, physiological recording from ampullary afferent fibers demonstrated that they respond to frequency-modulated signals as predicted from the signal's low-frequency component. Electrophysiological study also showed that detection of frequency modulation by the ampullary system is immune to the presence of other constant electric organ discharges. Accepted: 28 June 1998     

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.     

Responses of neurons in the electrosensory lateral line lobe of the weakly electric fish <Emphasis Type="Italic">Gnathonemus petersii</Emphasis> to simple and complex electrosensory stimuli

Mormyrid fish use active electrolocation to detect and analyze objects. The electrosensory lateral line lobe in the brain receives input from electroreceptors and an efference copy of the command to discharge the electric organ. In curarized fish, we recorded extracellularly from neurons of the electrosensory lateral line lobe while stimulating in the periphery with either a local point stimulus or with a more natural whole-body stimulus. Two classes of neurons were found: (1) three types of E-cells, which were excited by a point stimulus; and (2) two types of I-cells, which were inhibited by point stimulus and responded with excitation to the electric organ corollary discharge. While all neurons responded to a point stimulus, only one out of two types of I-units and two of the three types of E-units changed their firing behavior to a whole-body stimulus or when an object was present. In most units, the responses to whole-body stimuli and to point stimuli differed substantially. Many electrosensory lateral line lobe units showed neural plasticity after prolonged sensory stimulation. However, plastic effects during whole body stimulation were often unlike those occurring during point stimuli, suggesting that under natural conditions electrosensory lateral line lobe network effects play an important role in shaping neural plasticity.     

Behavioral responses of weakly electric fish to complex impedances

Summary Members of the family of African electric fish, Mormyridae, exhibit a novelty response, consisting of an acceleration in the rate of electric organ discharges (EODs), when faced with changes in feedback arising from their EODs. In this study, the novelty responses of three different species of mormyrids to shunts with different electrical characteristics were noted. The three species differed in the frequency contents of their EODs: two species had relatively high spectral frequencies in their EODs (>10 kHz), while the third species had only lower spectral frequencies (< 10 kHz). Primarily resistive shunts elicited novelty response accelerations in all three species, and the magnitudes of these responses, when normalized to the responses obtained for a shunt with no introduced resistance, were comparable for all three species. For primarily capacitive shunts, however, the magnitudes of the normalized responses were different for the three species: the two species with high spectral frequencies in their EODs showed larger normalized responses than the third species which had only low EOD spectral frequencies.The differences in species responses for capacitive shunts, and the similarities in species responses for resistive shunts, suggest that electric fish detect the complex impedance of objects in their near field environment: a circuit model consisting of a fish emitting discharges into the surrounding water, which can be shunted by a variable complex impedance, conforms well to the data. Thus, electrolocation is a frequency dependent sensory process, and this frequency dependency should be considered in any speculation about the adaptive value of different EOD waveforms.Abbreviation EOD electric organ discharge     

Primary afferent fibers conduct impulses in both directions under physiological stimulus conditions

Summary In electric fish of the family Mormyridae some primary afferent fibers conduct impulses not only from electroreceptors to the brain but also from the brain to the receptors. The efferent impulses may be elicited by electrical stimulation which is within the physiological range, i.e., by stimulation which is similar in amplitude and duration to the stimulation that is caused by the fish's own electric organ discharge. Afferent and efferent impulses in the same afferent fiber were identified by: simultaneously recording from a fiber at two different points, at the receptor and at the nerve trunk (Figs. 2C-H; 3B-D); by cutting the afferent fiber between the brain and the recording site as well as between the recording site and the periphery; and by intra-axonal recording from the afferent fiber near its entry into the brain (Fig. 4). The efferent impulses result from the central integration of a corollary discharge of the electric organ motor command with excitatory and inhibitory input from several different receptors near the one from which afferent impulses originate (Fig. 4). The centrally originating impulse may be capable of modifying the effect of signals originating in the periphery.Abbreviations ELLL electrosensory lateral line lobe - EOCD electric organ corollary discharge - EOD electric organ discharge - epsp excitatory postsynaptic potential - NPLL posterior lateral line nerve     

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.     

Social spacing in the mormyrid fish Gnathonemus petersii (Pisces): A multisensory approach

The sensory basis of group cohesion in the weak-electric fish Gnathonemus petersii was investigated in a circular tank with groups of four fish each, interacting through a wide-meshed plastic screen with intact or operated conspecifics, or with other stimulus objects. We confined these stimuli to one or two peripheral holding compartments. The response measures were obtained from the free swimming fish and included (1) the time the fish spent together as a group, (2) the time they spent in front of the holding compartments, (3) the circular distribution of the fish's positions, and (4) the mean nearest neighbour distances. Under empty compartment conditions, four different groups were tested, consisting of either (1) intact, electrically active fish, or (2) electrically ‘silent’ fish (with their electric organ surgically rendered inoperative), or (3) blind, or (4) ‘silent’ and blind animals. The loss of either sensory modality, vision or feedback from electric organ discharge, led to changes of comparable size, decreasing the time spent as a group and increasing the mean nearest neighbour distance. In fish lacking both modalities, group cohesion was further impaired. With stimuli present in one or both holding compartments, the strength of social attraction depended on the nature of the stimulus: the more intact stimulus conspecifics were present, the more densely did the fish group in front of the stimulus compartment. ‘Wired-in’ electric organ discharges (simulating waveform and intensity) and electrically ‘silent’ fish were equally attractive, but only half as attractive as intact fish. Blind free swimming fish aggregated with intact and also with ‘silent’ conspecifics. Under dim light conditions, group cohesion was predominantly, though not exclusively, affected by electrosensory feedback from the electric organ discharge and visual input. Mechanical and olfactory cues may also be involved.     

Electric Imaging through Evolution,a Modeling Study of Commonalities and Differences

Modeling the electric field and images in electric fish contributes to a better understanding of the pre-receptor conditioning of electric images. Although the boundary element method has been very successful for calculating images and fields, complex electric organ discharges pose a challenge for active electroreception modeling. We have previously developed a direct method for calculating electric images which takes into account the structure and physiology of the electric organ as well as the geometry and resistivity of fish tissues. The present article reports a general application of our simulator for studying electric images in electric fish with heterogeneous, extended electric organs. We studied three species of Gymnotiformes, including both wave-type (Apteronotus albifrons) and pulse-type (Gymnotus obscurus and Gymnotus coropinae) fish, with electric organs of different complexity. The results are compared with the African (Gnathonemus petersii) and American (Gymnotus omarorum) electric fish studied previously. We address the following issues: 1) how to calculate equivalent source distributions based on experimental measurements, 2) how the complexity of the electric organ discharge determines the features of the electric field and 3) how the basal field determines the characteristics of electric images. Our findings allow us to generalize the hypothesis (previously posed for G. omarorum) in which the perioral region and the rest of the body play different sensory roles. While the “electrosensory fovea” appears suitable for exploring objects in detail, the rest of the body is likened to a “peripheral retina” for detecting the presence and movement of surrounding objects. We discuss the commonalities and differences between species. Compared to African species, American electric fish show a weaker field. This feature, derived from the complexity of distributed electric organs, may endow Gymnotiformes with the ability to emit site-specific signals to be detected in the short range by a conspecific and the possibility to evolve predator avoidance strategies.     

Differential responses of two types of electroreceptive afferents to signal distortions may permit capacitance measurement in a weakly electric fish,Gnathonemus petersii

Summary Gnathonemus petersii discriminates between ohmic and capacitive objects. To investigate the sensory basis of this discrimination we recorded from primary afférents that innervate either A or B mormyromast sensory cells. Modified and natural electric organ discharges were used as stimuli. In both A and B fibres frequencies below the peak-power frequency (3.8 to 4.5 kHz) of the electric organ discharge caused minimal first-spike latencies and a maximum number of spikes. A fibres did not discriminate phase-shifted stimuli, whereas B fibres responded significantly with a decrease in first-spike latency if the phase shift was only — 1°. In both A and B fibres an amplitude increase caused a decrease in spike latency and an increase in spike number; an amplitude decrease had the reverse effect. If stimulated with quasi-natural electric organ discharges distorted by capacitive objects, the responses of A fibres decreased with increasing signal distortion. In contrast, the responses of B fibres increased until amplitude effects began to dominate. Gnathonemus may use the physiological differences between A and B fibres to detect and discriminate between capacitive and purely ohmic objects.Abbreviations ELL electrosensory lateral line lobe - EOD electric organ discharge - LFS local filtered signal - p-p peak-to-peak     

Electric organ activation in Gymnotus carapo: Spinal origin and peripheral mechanisms

A new technique of multiple-air-gap recording was developed to study the EO activation process in Gymnotus carapo. Using this technique, the spatiotemporal pattern of electromotive force generation was investigated in normal and spinal-lesioned animals.Our data indicate that the EOD may be considered as the result of the sequential activation of 3 defined portions of the EO: the abdominal portion (included in the rostral 25% of the fish body), the central portion (comprising the intermediate 50% of the fish body) and the tail portion (the caudal 25% of the fish body). The EOD generated at each portion is characterized by: 1) timing respect to the pacemaker nucleus discharge, 2) speed of progression within the region, 3) waveform, and 4) magnitude.Spinal sections demonstrated that EMNs serving relatively small portions of the EO are widely distributed (convergence) and that surgical exclusion of relatively small portions of the spinal cord diminishes the amplitude of the EOD along an extended portion of the EO (divergence).Abbreviations EMF electromotive force - EMN electromotor-neurons - EO electric organ - EOD electric organ discharge - PMNFP pacemaker nucleus field potential - PEN posterior electromotor nerve - PNA peripheral neural activity     

The jamming avoidance response ofEigenmannia: properties of a diencephalic link between sensory processing and motor output

Summary Brain regions participating in the control ofEigenmannia's electric organ discharge frequency were localized by electrical microstimulation and anatomically identified by means of horseradish peroxidase deposition. A diencephalic region was found which, when stimulated, caused electric organ discharge (EOD) frequency increases of similar magnitude and time course as the frequency increases seen during the jamming avoidance response. Single unit recordings from this region revealed one cell type which preferentially responded to stimuli that cause the acceleration phase of the jamming avoidance response (electric organ discharge frequency increase). A second cell type responded preferentially to stimuli which cause EOD frequency decrease, and both cell types were tuned to stimuli which evoked maximal jamming avoidance behaviors.The results of the horseradish peroxidase experiments showed that the recording and stimulation sites correspond to the previously described nucleus electrosensorius. Our results confirm the earlier finding that this nucleus receives output from the torus semicircularis and we also found that the N. electrosensorius projects to the mesencephalic prepacemaker nucleus. The prepacemaker projects to the medullary pacemaker nucleus which generates the commands that evoke electric organ discharges.The anatomical and physiological results described here establish this diencephalic region as a link between the major sensory processing region for the jamming avoidance response, the torus semicircularis, and a mesencephalic pre-motor region, the prepacemaker nucleus.Abbreviations AM amplitude modulation - DF Delta F - ELLL electrosensory lateral line lobe - EOD electric organ discharge - JAR jamming avoidance response - NE nucleus electrosensorius - PPN prepacemaker nucleus - PN pacemaker nucleus     

Analysis of the jamming avoidance response in the electric fish Gymnotus carapo

The electric fish Gymnotus carapo emits brief (4 ms) electric pulses separated by much longer intervals of high regularity (coefficient of variation 0.01–0.02). Two main changes in the firing patterns of electric organ discharge were observed when two fish were placed together. (1) All fish pairs showed an increase in the frequency difference between the two fish, in comparison with the value observed in isolated fish, prior to the interaction. This change increased the number of beats per second between both discharge trains, i.e., the number of times per second that the higher rate discharge sweeps the lower rate one when displayed on an oscilloscope. (2) When the sweeping velocity fell below 2–3 sweeps/s, transient frequency increases were also observed in the electric organ discharge of the higher rate fish when they were about to discharge simultaneously. The contribution to jamming avoidance of these two changes was analyzed by comparing recordings of behavioral interactions with simulations produced by a computational model. The jamming effect of the firing of a conspecific located in the same tank was evaluated by counting the number of coincidences between both trains (occurrence of discharges of the two fish within 2 ms of one another). The number of coincidences was evaluated as a function of the sweeping velocity in both simulations (with and without transient frequency increases) and real fish. As the sweeping velocity increased, single coincidences increased slightly in simulations without transient frequency increases, whereas the successive coincidences (coincidences repeated in successive discharges) decreased abruptly. The simulation including transient frequency increases eliminated the successive coincidences and decreased the single ones. Only when the sweeping velocity was less than 2–3 sweeps/s, did transient frequency increases improve the coincidence-avoiding performance of the simulation. The number of coincidences observed in natural behavioral interactions for the different sweeping velocities coincided with the distributions obtained with the simulations. As successive coincidences are known to be more detrimental for electrolocation than single ones, the increase in the sweeping velocity may be considered a jamming avoidance strategy in Gymnotus carapo, in addition to the already described transient frequency increases. Received: 2 June 1998 / Accepted in revised form: 18 November 1998     

Biomimetic Sensors： Active Electrolocation of Weakly Electric Fish as a Model for Active Sensing in Technical Systems

Instead of vision, many nocturnal animals use alternative senses for navigation and object detection in their dark environment. For this purpose, weakly electric mormyrid fish employ active electrolocation, during which they discharge a specialized electric organ in their tail which discharges electrical pulses. Each discharge builds up an electrical field around the fish, which is sensed by cutaneous electroreceptor organs that are distributed over most of the body surface of the fish. Nearby objects distort this electrical field and cause a local alteration in current flow in those electroreceptors that are closest to the object. By constantly monitoring responses of its electroreceptor organs, a fish can detect, localize, and identify environmental objects.Inspired by the remarkable capabilities of weakly electric fish in detecting and recognizing objects, we designed technical sensor systems that can solve similar problems of remote object sensing. We applied the principles of active electrolocation to technical systems by building devices that produce electrical current pulses in a conducting medium (water or ionized gases) and simultaneously sense local current density. Depending on the specific task a sensor was designed for devices could (i) detect an object, (ii) localize it in space, (iii) determine its distance, and (iv) measure properties such as material properties, thickness, or material faults. Our systems proved to be relatively insensitive to environmental disturbances such as heat, pressure, or turbidity. They have a wide range of applications including material identification, quality control, non-contact distance measurements, medical applications and many more. Despite their astonishing capacities, our sensors still lag far behind what electric fish are able to achieve during active electrolocation. The understanding of the neural principles governing electric fish sensory physiology and the corresponding optimization of our sensors to solve certain technical tasks therefore remain ongoing goals of our research.     

Biomimetic Sensors: Active Electrolocation of Weakly Electric Fish as a Model for Active Sensing in Technical Systems

Instead of vision, many nocturnal animals use alternative senses for navigation and object detection in their dark environment. For this purpose, weakly electric mormyrid fish employ active electrolocation, during which they discharge a specialized electric organ in their tail which discharges electrical pulses. Each discharge builds up an electrical field around the fish, which is sensed by cutaneous electroreceptor organs that are distributed over most of the body surface of the fish. Nearby objects distort this electrical field and cause a local alteration in current flow in those electroreceptors that are closest to the object. By constantly monitoring responses of its electroreceptor organs, a fish can detect, localize, and identify environmental objects.Inspired by the remarkable capabilities of weakly electric fish in detecting and recognizing objects, we designed technical sensor systems that can solve similar problems of remote object sensing. We applied the principles of active electrolocation to technical systems by building devices that produce electrical current pulses in a conducting medium (water or ionized gases) and simultaneously sense local current density. Depending on the specific task a sensor was designed for devices could (i) detect an object, (ii) localize it in space, (iii) determine its distance, and (iv) measure properties such as material properties, thickness, or material faults. Our systems proved to be relatively insensitive to environmental disturbances such as heat, pressure, or turbidity. They have a wide range of applications including material identification, quality control, non-contact distance measurements, medical applications and many more. Despite their astonishing capacities, our sensors still lag far behind what electric fish are able to achieve during active electrolocation. The understanding of the neural principles governing electric fish sensory physiology and the corresponding optimization of our sensors to solve certain technical tasks therefore remain ongoing goals of our research.     

An internal current source yields immunity of electrosensory information processing to unusually strong jamming in electric fish

Summary The electric organ of a fish represents an internal current source, and the largely isopotential nature of the body interior warrants that the current associated with the fish's electric organ discharges (EODs) recruits all electroreceptors on the fish's body surface evenly. Currents associated with the EODs of a neighbor, however, will not penetrate all portions of the fish's body surface equally and will barely affect regions where the neighbor's current flows tangentially to the skin surface. The computational mechanisms of the jamming avoidance response (JAR) in Eigenmannia exploit the uneven effects of a neighbor's EOD current to calculate the correct frequency difference between the two interfering EOD signals even if the amplitude of a neighbor's signal surpasses that of the fish's own signal by orders of magnitude. The particular geometry of the fish's own EOD current thus yields some immunity against the potentially confusing effects of unusually strong interfering EOD currents of neighbors.Abbreviations DF frequency difference - ELL electrosensory lateral line lobe - EOD electric organ discharge - JAR jamming avoidance response