‘Recognition units’ at the top of a neuronal hierarchy?

The electric fish, Eigenmannia, is able to discriminate the sign of the frequency difference, Df, between a neighbor's electric organ discharges (EODs) and its own. The fish lowers its EOD frequency for positive Dfs and raises its frequency for negative Dfs to minimize jamming of its electrolocation ability by a neighbor's EODs of similar frequency. This jamming avoidance response (JAR) is controlled by a group of 'sign-selective' neurons in the prepacemaker nucleus (PPN) that is located at the boundary of the midbrain and the diencephalon (Fig. 1). Extracellular recordings from a total of 35 neurons revealed a great similarity between behavioral and neuronal response properties: 1. All neurons fired vigorously for negative Dfs and were almost silent for positive Dfs, regardless of the orientation of the jamming stimulus, and thus discriminated the sign of Df unambiguously (Fig. 2). 2. In accordance with behavioral observations, individual neurons failed to discriminate the sign of Df when the jamming stimulus had the same field geometry as the signal mimicking the animal's own EOD (Fig. 3). 3. Df magnitudes which evoke strongest JARs, usually 4 to 8 Hz, also induced most vigorous responses in sign-selective neurons (Fig. 5). 4. Behavioral and neuronal thresholds for the detection of small jamming signals were similar. Threshold for sign selectivity was reached when the amplitude ratio of the jamming signal to the EOD mimic, measured near the head surface, was 0.001. This value corresponds to a maximal temporal disparity (a necessary cue for performing a correct JAR) of 1 to 2 microseconds for signals received by the two sides of the body in a transverse jamming field (Fig. 7). 5. The effects of two jamming fields, offered orthogonally to each other, may interact nonlinearly at the behavioral as well as at the neuronal level. A positive Df presented in one field may suppress behavioral and neuronal responses to modulations of the sign of Df in the other field (Fig. 8c).     

Testosterone modulates female chirping behavior in the weakly electric fish,Apteronotus leptorhynchus

The weakly electric fish, Apteronotus leptorhynchus, produces a wave-like electric organ discharge (EOD) utilized for electrolocation and communication. Both sexes communicate by emitting chirps: transient increases in EOD frequency. In males, chirping behavior and the jamming avoidance response (JAR) can be evoked by an artificial EOD stimulus delivered to the water at frequencies 1–10 Hz below the animal's own EOD. In contrast, females rarely chirp in response to this stimulus even though they show consistent JARs. To investigate whether this behavioral difference is hormone dependent, we implanted females with testosterone (T) and monitored their chirping activity over a 5 week period. Our findings indicate that elevations in blood levels of T cause an enhancement of chirping behavior and a lowering of basal EOD frequency in females. Elevated blood levels of T also appear to modulate the quality of chirps produced by hormone treated females. The effects of T on female chirping behavior and basal EOD frequency appear specific, since the magnitude of the JAR was not affected by the hormonal treatment. These findings suggest that seasonal changes in circulating concentrations of T may regulate behavioral changes in female chirping behavior and basal EOD frequency.Abbreviations DHT dihydrotestosterone - E estradiol - EOD elecdric organ discharge - GSI gonadal size index - JAR jamming avoidance response - PPn prepacemaker nucleus - T testosterone     

Discrimination of the sign of frequency differences bySternopygus,an electric fish without a jamming avoidance response

Several species of weakly electric fish reflexively change their frequency of electric organ discharge (EOD) in response to sensing signals of similar frequency from conspecifics; that is, they exhibit jamming avoidance responses (JAR).Eigenmannia increases its EOD frequency if jammed by a signal of lower frequency and decreases its EOD frequency if jammed by a signal of higher frequency. This discrimination is based on an analysis of the patterns of amplitude modulations and phase differences resulting from signal interference. Fish of the closely related genus,Sternopygus, however, do not exhibit a JAR. Here we show that despite lacking this behavior,Sternopygus shares many sensory processing capacities withEigenmannia:

Stimulus discrimination in the diencephalon ofEigenmannia: the emergence and sharpening of a sensory filter

Summary Neuronal reliability and sensitivity to behaviorally relevant stimulus patterns were investigated in a higher-order nucleus of the diencephalon believed to participate in the jamming avoidance response (JAR) of the weakly electric fish,Eigenmannia. The fish raises or lowers its frequency of electric organ discharge (EOD) to minimize interference from a neighboring fish's EOD. Proper JARs require determination of the sign of the difference frequency (Df) between the neighboring fish's EOD and the fish's own EOD. Bastian and Yuthas (1984) recently described diencephalic neurons within the nucleus electrosensorius that are able to make this determination. In the present study, response properties of such neurons were compared with those of lower-level sign-selective cells found in the torus semicircularis and the optic tectum (Heiligenberg and Rose 1985) as well as with properties of the intact behavior.Most sign-selective cells within the nucleus electrosensorius show a high degree of selectivity for one sign of the difference frequency; cells with either sign preference were found in approximately equal numbers. The sign preference and the degree of sign selectivity is most often independent of the spatial orientation of the jamming stimulus. In contrast, the responses of toral and tectal cells are less robust and consistent and are often highly dependent on the geometry of the jamming stimulus.Determination of the sign of the difference frequency requires the analysis of amplitude modulations coupled with modulations in phase (timing) differences between pairs of areas of the body surface. The most sensitive cells recorded in the nucleus electrosensorius can determine the sign of the difference frequency with timing differences of 1 s or less, roughly comparable to the behavioral threshold of 400 ns (Carr et al. 1986). The best toral/tectal response required at least a 16 s modulation.Cells within the nucleus electrosensorius thus code the sign of Df with a high degree of reliability and sensitivity. Ambiguities persist, however, which suggest that single cells at this level cannot completely account for the behavioral discrimination. Additional processing may be necessary to transform a still primarily sensory code into a motor program for control of the JAR (Rose et al. 1988).Abbreviations EOD electric organ discharge - JAR jammning avoidance response - Df difference frequency between jamming signal and fish's own EOD - S ₁ sinusoidal EOD mimic of subject fish - S ₂ sinusoidal EOD mimic of neighbor     

Gating of sensory information: Joint computations of phase and amplitude data in the midbrain of the electric fish,Eigenmannia

Summary Eigenmannia is able to determine whether the electric organ discharge (EOD) of a neighbor is of higher or lower frequency than its own EOD. For small frequency differences, Df, the fish avoids jamming by shifting its frequency away from that of its neighbor. This jamming avoidance response (JAR), therefore, requires that the fish discriminate the sign of Df. The interference pattern of two EODs of similar frequency is characterized by local modulations of the instantaneous amplitude and the spatial difference of the instantaneous phase, or differential phase, of the mixed signal. When amplitude and differential phase are plotted in a two-dimensional state plane, circular graphs are obtained with a sense of rotation that reflects the sign of Df.Behavioral studies have shown that both amplitude and differential phase modulations are required for the control of the JAR. Considering two regions of the body surface, A and B, that receive strong and weak contamination by the jamming signal, respectively, rises and falls of the signal amplitude in A will be accompanied by respective advances and delays of the signal in A relative to that in B if the jamming signal is of lower frequency, i.e. if Df is negative. A plot of amplitude versus differential phase yields a clockwise sense of rotation in this case (Fig. 1). The opposite relation between amplitude and phase modulations, resulting in a counterclockwise rotation, holds for a positive Df. For the less strongly contaminated area B, however, the relation between the sign of Df and the sense of rotation is reversed, so that for a negative Df, a rise of amplitude in B will coincide with a delay of the signal in B relative to that in A.By independent experimental control of amplitude and differential-phase modulations, we explored midbrain neurons that discriminate the sense of rotations in the amplitude-phase plane. We found that these neurons achieve this discrimination by gating amplitude inputs by differentialphase information, thus exploiting the particular combinations of amplitude and differential phase that characterize a given sense of rotation (Figs. 2–4). Since the response properties of such neurons only reflect the sense of rotation, and since the same sense of rotation can be obtained for either sign of Df (depending upon the relative contamination of the receptive fields involved), individual neurons do not yet provide unambiguous information about the sign of Df. It can be shown, however, that large populations of such neurons will, nevertheless, reliably detect the correct sign of Df (Fig. 7). Response properties of these neurons offer plausible explanations for a number of earlier behavioral observations, particularly for the notion of a precise behavior controlled by a distributed system of unreliable components.     

Intracellular recording in the medullary pacemaker nucleus of the weakly electric fish,Apteronotus, during modulatory behaviors

1. The weakly electric gymnotiform fish, Apteronotus leptorhynchus, can be induced to perform a variety of modulations of its quasi-sinusoidal, electric organ discharge (EOD) in acute physiological preparations. These modulations, many of which are communicatory in function, include the jamming avoidance response (JAR). We have recorded intracellularly from neurons of the medullary pacemaker nucleus which is responsible for maintaining the ongoing EOD frequency during these modulatory behaviors. 2. We have used dye-filled microelectrodes to characterize single cell morphology of the two types of cells in the pacemaker nucleus (relay and pacemaker cells) and to localize anatomically the site of the differing responses we see during frequency modulations. We have also recorded with KCl-filled electrodes and attributed these data to cell type and location on the basis of characteristic behavior during these modulations. 3. Much of our data deals with chirps, brief accelerations of the EOD frequency lasting 10 to 14 ms. We see distinct patterns of activity in the pacemaker nucleus corresponding to different anatomical locations: the relay cell soma and axon, and the pacemaker cell soma and axon. Most of these loci show a marked rise in baseline voltage during the acceleration in spike frequency. The most unusual of these is the pacemaker cell axon which displays an often extreme decline in spike amplitude concurrent with the chirp (Fig. 7A). 4. 'Yodeling' (Dye 1987) appears to involve similar, characteristic changes in the pattern of firing as those seen during chirping. Similar quantitative analyses suggest that the JAR involves a different mechanism, however.     

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.Abbreviations EOD electric organ discharge - f frequency of EOD or pacemaker command signal - JAR jamming avoidance response - S ₁ stimulus mimicking fish's own EOD - f ₁ frequency of S₁ - S ₂ stimulus mimicking neighbor's EOD - f ₂ frequency of S₂     

Behavioral responses to jamming and ‘phantom’ jamming stimuli in the weakly electric fish <Emphasis Type="Italic">Eigenmannia</Emphasis>

The jamming avoidance response (JAR) of the weakly electric fish Eigenmannia is characterized by upward or downward shifts in electric organ discharge (EOD) frequency that are elicited by particular combinations of sinusoidal amplitude modulation (AM) and differential phase modulation (DPM). However, non-jamming stimuli that consist of AM and/or DPM can elicit similar shifts in EOD frequency. We tested the hypothesis that these behavioral responses result from non-jamming stimuli being misperceived as jamming stimuli. Responses to non-jamming stimuli were similar to JARs as measured by modulation rate tuning, sensitivity, and temporal dynamics. There was a smooth transition between the magnitude of JARs and responses to stimuli with variable depths of AM or DPM, suggesting that frequency shifts in response to jamming and non-jamming stimuli represent different points along a continuum rather than categorically distinct behaviors. We also tested the hypothesis that non-jamming stimuli can elicit frequency shifts in natural contexts. Frequency decreases could be elicited by semi-natural AM stimuli, such as random AM, AM presented to a localized portion of the body surface, transient changes in amplitude, and movement of resistive objects through the electric field. We conclude that ‘phantom’ jamming stimuli can induce EOD frequency shifts in natural situations.     

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

Summary During their jamming avoidance response (JAR), weakly electric fish of the genusEigenmannia 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.Abbreviations EOD electric organ discharge - JAR jamming avoidance response - Df difference frequency between jamming signal and the fish's own EOD - nE nucleus electrosensorius - PPn prepacemaker nucleus     

Species-specific differences in sensorimotor adaptation are correlated with differences in social structure

Here, we report a species difference in the strength and duration of long-term sensorimotor adaptation in the electromotor output of weakly electric fish. The adaptation is produced by changes in intrinsic excitability in the electromotor pacemaker nucleus; this change is a form of memory that correlates with social structure. A weakly electric fish may be jammed by a similar electric organ discharge (EOD) frequency of another fish and prevents jamming by transiently raising its own emission frequency, a behavior called the jamming avoidance response (JAR). The JAR requires activation of NMDA receptors, and prolonged JAR performance results in long-term frequency elevation (LTFE) of a fish’s EOD frequency for many hours after the jamming stimulus. We find that LTFE is stronger in a shoaling species (Eigenmannia virescens) with a higher probability of encountering jamming conspecifics, when compared to a solitary species (Apteronotus leptorhynchus). Additionally, LTFE persists in Eigenmannia, whereas, it decays over 5–9 h in Apteronotus.     

The development of the Jamming Avoidance Response (JAR) in Eigenmannia: An innate behavior indeed

Summary In its Jamming Avoidance Response (JAR), the gymnotiform electric fish Eigenmannia shifts its electric organ discharge (EOD) frequency away from similar interfering frequencies. Continual behavioral measurements were carried out in 164 juvenile fish until a correct JAR emerged. Sixty-four of these fish were raised in complete isolation, the remainder in a community of their siblings. A correct JAR emerged in fish of 1.2–1.6 cm in body length, corresponding to a developmental age of 24–32 days. In 6 of 164 fish, the emergence of a correct JAR followed an interim appearance of an incorrect JAR, which involved frequency shifts in the direction opposite to those of a correct JAR. The fish raised in isolation developed the same forms of behavior and showed the same sequence in their appearance as did socially raised fish. This indicates that the JAR and its developmental schedule are innate. The appearance of an incorrect JAR suggests initial errors or incompleteness in the wiring of central nervous connections. A correct JAR ultimately emerged even if a stimulus regimen was offered that rewarded frequency shifts in the direction opposite to those of a correct JAR. This indicates that the development of the JAR is immune to experimental alterations of sensory experience.Abbreviations Df frequency difference between a jamming stimulus and fish's EOD - ELL electrosensory lateral line lobe - EO electric organ - EOD electric organ discharge - JAR Jamming Avoidance Response - nE nucleus electrosensorius - nE subnucleus of nE, causing drop of EOD frequency - nE subnucleus of nE, causing rise of EOD frequency - Pn pacemaker nucleus - PPn prepacemaker nucleus     

‘Ancestral’ neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response

Summary The genusSternopygus, believed to reflect ancestral traits of gymnotiform electric fish, is closely related to the more modern genusEigenmannia (Mago-Leccia 1978; Fink and Fink 1981).Sternopygus is the only known genus of electric fish that does not perform a jamming avoidance response (JAR) to minimize the potentially detrimental effects of signal interference between discharging neighbors (Bullock et al. 1972, 1975), and its ability to electrolocate objects is rather immune to jamming (Matsubara and Heiligenberg 1978).By studying the responses of midbrain neurons to stimulus regimes effective in eliciting the JAR inEigenmannia, we found thatSternopygus has neurons capable of discriminating the sign of the difference frequency between interfering electric organ discharges (EODs). These sign-selective neurons, which are believed to be important elements in the control of the JAR inEigenmannia, may, therefore, fulfill a more general function in the detection of moving objects and conspecifics but could potentially be assembled for the evolution of a JAR inSternopygus. The relative immunity to jamming in this genus may result, in part, from a stronger reliance upon the ampullary electrosensory system which operates in the DC and low-frequency range, outside the EOD spectrum of these fish.Abbreviations AM amplitude modulation - Df frequency difference - EOD electric organ discharge - JAR jamming avoidance response     

Social interactions and cortisol treatment increase the production of aggressive electrocommunication signals in male electric fish,Apteronotus leptorhynchus

Brown ghost knife fish, Apteronotus leptorhynchus, continually emit a weakly electric discharge that serves as a communication signal and is sensitive to sex steroids. Males modulate this signal during bouts of aggression by briefly (approximately 15 ms) increasing the discharge frequency in signals termed "chirps." The present study examined the effects of short-term (1-7 days) and long-term (6-35 days) male-male interaction on the continuous electric organ discharge (EOD), chirping behavior, and plasma levels of cortisol and two androgens, 11-ketotestosterone (11KT) and testosterone. Males housed in isolation or in pairs were tested for short-term and long-term changes in their EOD frequency and chirping rate to standardized sinusoidal electrical stimuli. Within 1 week, chirp rate was significantly higher in paired fish than in isolated fish, but EOD frequency was equivalent in these two groups of fish. Plasma cortisol levels were significantly higher in paired fish than in isolated fish, but there was no difference between groups in plasma 11KT levels. Among paired fish, cortisol levels correlated positively with chirp rate. To determine whether elevated cortisol can cause changes in chirping behavior, isolated fish were implanted with cortisol-filled or empty Silastic tubes and tested for short-term and long-term changes in electrocommunication signals and steroid levels. After 2 weeks, fish that received cortisol implants showed higher chirp rates than blank-implanted fish; there were no difference between groups in EOD frequency. Cortisol implants significantly elevated plasma cortisol levels compared to blank implants but had no effect on plasma 11KT levels. These results suggest that male-male interaction increases chirp rate by elevating levels of plasma cortisol, which, in turn, acts to modify neural activity though an 11KT-independent mechanism.     

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.     

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.     

EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips.

Weakly electric "wave" fish make highly regular electric organ discharges (EODs) for precise electrolocation. Yet, they modulate the ongoing rhythmicity of their EOD during social interactions. These modulations may last from a few milliseconds to tens of minutes. In this paper we describe the different types of EOD modulations, what they may signal to recipient fish, and how they are generated on a neural level. Our main conclusions, based on a species called the brown ghost (Apteronotus leptorhynchus) are that fish: (1) show sexual dimorphism in the signals that they generate; (2) make different signals depending on Whether they are interacting with a fish of the opposite sex or, within their own sex, to a fish of that which is dominant or subordinate to it; (3) are able to assess relative dominance from electrical cues; (4) have a type of plasticity in the pacemaker nucleus, the control center for the EOD, that occurs after stimulation of NMDA receptors that causes a long-lasting (tens of minutes to hours) change in EOD frequency; (5) that this NMDA receptor-dependent change may occur in reflexive responses, like the jamming avoidance response (JAR), as well as after certain long-lasting social signals. We propose that NMDA-receptor dependent increases in EOD frequency during the JAR adaptively shift the EOD frequency to a new value to avoid jamming by another fish and that such increases in EOD frequency during social encounters may be advantageous since social dominance seems to be positively correlated with EOD frequency in both sexes.     

Electrosensory phase sensitivity in the weakly electric fish Eigenmannia in the detection of signals similar to its own

The electric organ discharge (EOD) of the South American knifefish Eigenmannia sp. is a permanently present wave signal of usually constant amplitude and frequency (similar to a sine wave). A fish perceives discharges of other fish as a modulation of its own. At frequency identity (F = 0 Hz) the phase difference between a fish's own electric discharge and that of another fish affects the superimposed waveform. It was unclear whether or not the electrosensory stimulus-intensity threshold as behaviourally determined depends on the phase difference between a fish's own EOD and a sine-wave stimulus (at F = 0 Hz). Also the strength of the jamming avoidance response (JAR), a discharge frequency shift away from a stimulus that is sufficiently close to the EOD frequency, as a function of phase difference was studied. Sine-wave stimuli were both frequency-clamped and phase-locked to a fish's discharge frequency (F = 0 Hz). In food-rewarded fish, the electrosensory stimulus-intensity threshold depended significantly on the phase difference between a fish's discharge and the stimulus. Stimulus-intensity thresholds were low (down to 3 V/cm, peak-to-peak) when the superimposed complex wave changed such that the shift in zero-crossings times relative to the original EOD was large but amplitude change minimal; stimulus-intensity thresholds were high (up to 16.9 V/cm, peak-to-peak) when the shift in zero-crossings times was small but amplitude change maximal. Similar results were obtained for the non-conditioned JAR: at constant supra-threshold stimulus intensities and F = 0 Hz, the phase difference significantly affected the strength of the JAR, although variability between individuals was higher than that observed in the conditioned experiments.Abbreviations ACP active phase coupling - EOD electric organ discharge - JAR jamming avoidance response - F frequency (fish) — frequency (stimulus) [Hz] - p-p peak-to-peak     

Emergence of temporal-pattern sensitive neurons in the midbrain of weakly electric fish Gymnarchus niloticus.

Sensitivity of neurons in the torus semicircularis of a weakly electric fish, Gymnarchus niloticus, to two stimulus parameters that are critical for its behavior the jamming avoidance response was examined. The first parameter is the sign of frequency difference between discharge frequencies of fish's own electric organ and that of a neighbor's. The second parameter is the spatial orientation of neighbor's electric field. Whereas neuronal ambiguity of frequency coding for different orientations of neighbor's electric field is predicted, unambiguous JAR occurs at the behavioral level. Most neurons in the torus semicircularis showed sensitivity to the sign of frequency difference. Although a small number of neurons showed preference to a consistent sign of the frequency difference, the coding of the sign of frequency differences was found to be ambiguous with a highly variable pattern of responses for different orientations in most of neurons.     

The jamming avoidance response in gymnotoid pulse-species: A mechanism to minimize the probability of pulse-train coincidence

Summary Gymnotoid electric fish with pulse-type electric organ discharges (EODs) shorten (lengthen) their EOD intervals as pulses of a slightly slower (faster) train scan their EODs (Figs. 1, 2). They thus minimize the chance of pulse coincidence by transient accelerations (decelerations) of their EOD rate.Studies in curarized preparations demonstrate that this Jamming Avoidance Response (JAR) is controlled by electroreceptive input alone and without reference to an internal electric organ pacemaker-related signal (Fig. 8). A sufficient stimulus input consists of a train of strong, EOD-like stimulus pulses (S₁), which mimic the animal's experience of its own EOD, and a train of small pulses (S₂) of slightly different repetition rate, which mimic EODs of a neighbor. Correct behavioral responses require S₁ pulses of sufficient intensity to recruit pulse-markertype receptors; also spatial and temporal patterns must closely resemble those of the animal's EOD. These features are of little significance for S₂ pulses which, while scanning S₁ pulses, only provide a small perturbation of electroreceptive feedback from S₁ pulses. Inappropriate S₁ stimulation impairs and sometimes reverses (Fig. 7) the behavioral discrimination of scan directions. The JAR is explained in terms of excitatory and inhibitory processes (Fig. 3) which are triggered by S₂ stimulation, at specific phases within the S₁ cycle (Figs. 4–6).The JAR in pulse species strongly resembles the JAR in wave-species (Bullock et al., 1972) and could be considered an evolutionary ancestor of the latter. It is a response to a particular novelty in electroreceptive feedback.We thank Drs. T.H. Bullock, C. Hopkins and an anonymous referee for most helpful criticism. This research was supported by NSF grand BMS74-18640 and NIMH grant PHSMH-2614901 to W.H. and NIH grant/ROI NS 12337-01 to J.B.