Behavioral evidence for post-pause reduced responsiveness in the electrosensory system ofGymnotus carapo

2002 ◽  
Vol 205 (16) ◽  
pp. 2525-2533 ◽  
Author(s):  
Stefan Schuster

SUMMARYGymnotiform weakly electric fish find their way in the dark using a continuously operating active sensory system. An electric organ generates a continuous train of discharges (electric organ discharges, EODs), and tuberous high-frequency electroreceptors monitor the pattern of transcutaneous current flow associated with each EOD. Here, I report that a prior interruption to the continuous train of EODs dramatically affects a response shown by many pulse-type gymnotids. In this so-called novelty response, fish normally raise their electrosensory sampling rate in response to novel sensory stimuli. The gymnotid Gymnotus carapo was induced to pause its EODs briefly, and the novelty response to sensory stimuli given post-pause was analyzed. Mechanosensory stimuli given as early as 20 EODs after a pause elicited clear novelty responses, but strong high-frequency electrical stimuli were ineffective at this time. Moreover, high-frequency electrical stimuli remained less efficient in eliciting normal-sized responses until approximately 2000 EODs, or 40s, after a pause. The post-pause inefficiency of high-frequency stimuli was not due to an inappropriate choice of intensity or their temporal patterning and did not result from the stimulation that caused the pausing. Low-frequency stimuli that also recruited ampullary electroreceptors were more efficient than high-frequency stimuli in eliciting post-pause responses. These findings show that continuous activity is required either to maintain sensitivity to high-frequency electrical stimuli or to ensure that such stimuli are able to modulate efficiently the pacemaker that sets the discharge frequency.

2010 ◽  
Vol 7 (2) ◽  
pp. 197-200 ◽  
Author(s):  
Vincent Fugère ◽  
Hernán Ortega ◽  
Rüdiger Krahe

Animals often use signals to communicate their dominance status and avoid the costs of combat. We investigated whether the frequency of the electric organ discharge (EOD) of the weakly electric fish, Sternarchorhynchus sp., signals the dominance status of individuals. We correlated EOD frequency with body size and found a strong positive relationship. We then performed a competition experiment in which we found that higher frequency individuals were dominant over lower frequency ones. Finally, we conducted an electrical playback experiment and found that subjects more readily approached and attacked the stimulus electrodes when they played low-frequency signals than high-frequency ones. We propose that EOD frequency communicates dominance status in this gymnotiform species.


Author(s):  
David E. Saenz ◽  
Tingting Gu ◽  
Yue Ban ◽  
Kirk O. Winemiller ◽  
Michael R. Markham

Signal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. Signal mimicry, mate recognition, and sexual selection are potential factors maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.


2021 ◽  
Author(s):  
David E. Saenz ◽  
Tingting Gu ◽  
Yue Ban ◽  
Kirk O. Winemiller ◽  
Michael R. Markham

AbstractSignal plasticity can maximize the usefulness of costly animal signals such as the electric organ discharges (EODs) of weakly electric fishes. Some species of the order Gymnotiformes rapidly alter their EOD amplitude and duration in response to circadian cues and social stimuli. How this plasticity is maintained across related species with different degrees of signal complexity is poorly understood. In one genus of weakly electric gymnotiform fish (Brachyhypopomus) only one species, B. bennetti, produces a monophasic signal while all other species emit complex biphasic or multiphasic EOD waveforms produced by two overlapping but asynchronous action potentials in each electric organ cell (electrocyte). One consequence of this signal complexity is the suppression of low-frequency signal content that is detectable by electroreceptive predators. In complex EODs, reduction of the EOD amplitude and duration during daytime inactivity can decrease both predation risk and the metabolic cost of EOD generation. We compared EOD plasticity and its underlying physiology in Brachyhypopomus focusing on B. bennetti. We found that B. bennetti exhibits minimal EOD plasticity, but that its electrocytes retained vestigial mechanisms of biphasic signaling and vestigial mechanisms for modulating the EOD amplitude. These results suggest that this species represents a transitional phenotypic state within a clade where signal complexity and plasticity were initially gained and then lost. We discuss potential the roles of signal mimicry, species recognition, and sexual selection in maintaining the monophasic EOD phenotype in the face of detection by electroreceptive predators.


Author(s):  
Stefan Mucha ◽  
Lauren J. Chapman ◽  
Rüdiger Krahe

AbstractAnthropogenic environmental degradation has led to an increase in the frequency and prevalence of aquatic hypoxia (low dissolved oxygen concentration, DO), which may affect habitat quality for water-breathing fishes. The weakly electric black ghost knifefish, Apteronotus albifrons, is typically found in well-oxygenated freshwater habitats in South America. Using a shuttle-box design, we exposed juvenile A. albifrons to a stepwise decline in DO from normoxia (> 95% air saturation) to extreme hypoxia (10% air saturation) in one compartment and chronic normoxia in the other. On average, A. albifrons actively avoided the hypoxic compartment below 22% air saturation. Hypoxia avoidance was correlated with upregulated swimming activity. Following avoidance, fish regularly ventured back briefly into deep hypoxia. Hypoxia did not affect the frequency of their electric organ discharges. Our results show that A. albifrons is able to sense hypoxia at non-lethal levels and uses active avoidance to mitigate its adverse effects.


2013 ◽  
Vol 109 (7) ◽  
pp. 1713-1723 ◽  
Author(s):  
Michael R. Markham ◽  
Leonard K. Kaczmarek ◽  
Harold H. Zakon

We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) amplitude as a means of regulating energetic costs of AP signaling. Weakly electric fish generate an electric organ discharge (EOD) by summing the APs of their electric organ cells (electrocytes). Some electric fish increase AP amplitude during active periods or social interactions and decrease AP amplitude when inactive, regulated by melanocortin peptide hormones. This modulates signal amplitude and conserves energy. The gymnotiform Eigenmannia virescens generates EODs at frequencies that can exceed 500 Hz, which is energetically challenging. We examined how E. virescens meets that challenge. E. virescens electrocytes exhibit a voltage-gated Na+current ( INa) with extremely rapid recovery from inactivation (τrecov= 0.3 ms) allowing complete recovery of Na+current between APs even in fish with the highest EOD frequencies. Electrocytes also possess an inwardly rectifying K+current and a Na+-activated K+current ( IKNa), the latter not yet identified in any gymnotiform species. In vitro application of melanocortins increases electrocyte AP amplitude and the magnitudes of all three currents, but increased IKNais a function of enhanced Na+influx. Numerical simulations suggest that changing INamagnitude produces corresponding changes in AP amplitude and that KNachannels increase AP energy efficiency (10–30% less Na+influx/AP) over model cells with only voltage-gated K+channels. These findings suggest the possibility that E. virescens reduces the energetic demands of high-frequency APs through rapidly recovering Na+channels and the novel use of KNachannels to maximize AP amplitude at a given Na+conductance.


1997 ◽  
Vol 92 (2) ◽  
pp. 167-174 ◽  
Author(s):  
Gervais Tougas ◽  
Markad Kamath ◽  
Geena Watteel ◽  
Debbie Fitzpatrick ◽  
Ernest L. Fallen ◽  
...  

1. The heart and the oesophagus have similar sensory pathways, and sensations originating from the oesophagus are often difficult to differentiate from those of cardiac origin. We hypothesized that oesophageal sensory stimuli could alter neurocardiac function through autonomic reflexes elicited by these oesophageal stimuli. In the present study, we examined the neurocardiac response to oesophageal stimulation and the effects of electrical and mechanical oesophageal stimulation on the power spectrum of beat-to-beat heart rate variability in male volunteers. 2. In 14 healthy volunteers, beat-to-beat heart rate variability was compared at rest and during oesophageal stimulation, using either electrical (200 μs, 16 mA, 0.2 Hz) or mechanical (0.5 s, 14 ml, 0.2 Hz) stimuli. The power spectrum of beat-to-beat heart rate variability was obtained and its low- and high-frequency components were determined. 3. Distal oesophageal stimulation decreased heart rate slightly (both electrical and mechanical) (P < 0.005), and markedly altered heart rate variability (P < 0.001). Both electrical and mechanical oesophageal stimulation increased the absolute and normalized area of the high-frequency band within the power spectrum (P < 0.001), while simultaneously decreasing the low-frequency power (P < 0.005). 4. In humans, oesophageal stimulation, whether electrical or mechanical, appears to amplify respiratory-driven cardiac vagoafferent modulation while decreasing sympathetic modulation. The technique provides access to vagoafferent fibres and thus may yield useful information on the autonomic effects of visceral or oesophageal sensory stimulation.


1989 ◽  
Vol 146 (1) ◽  
pp. 229-253 ◽  
Author(s):  
C. C. Bell

Weakly electric fish use their electrosensory systems for electrocommunication, active electrolocation and low-frequency passive electrolocation. In electric fish of the family Mormyridae, these three purposes are mediated by separate classes of electroreceptors: electrocommunication by Knollenorgan electroreceptors, active electrolocation by Mormyromast electroreceptors and low-frequency passive electrolocation by ampullary electroreceptors. The primary afferent fibres from each class of electroreceptors terminate in a separate central region. Thus, the mormyrid electrosensory system has three anatomically and functionally distinct subsystems. This review describes the sensory coding and initial processing in each of the three subsystems, with an emphasis on the Knollenorgan and Mormyromast subsystems. The Knollenorgan subsystem is specialized for the measurement of temporal information but appears to ignore both intensity and spatial information. In contrast, the Mormyromast subsystem is specialized for the measurement of both intensity and spatial information. The morphological and physiological characteristics of the primary afferents and their central projection regions are quite different for the two subsystems and reflect the type of information which the subsystems preserve. This review also describes the electric organ corollary discharge (EOCD) effects which are present in the central projection regions of each of the three electrosensory subsystems. These EOCD effects are driven by the motor command that drives the electric organ to discharge. The EOCD effects are different in each of the three subsystems and these differences reflect differences in both the pattern and significance of the sensory information that is evoked by the fish's own electric organ discharge. Some of the EOCD effects are invariant, whereas others are plastic and depend on previous afferent input. The mormyrid work is placed within two general contexts: (a) the measurement of time and intensity in sensory systems, and (b) the various roles of motor command (efferent) signals and self-induced sensory (reafferent) signals in sensorimotor systems.


1999 ◽  
Vol 202 (10) ◽  
pp. 1205-1215 ◽  
Author(s):  
G. von der Emde

Weakly electric fish produce electric signals (electric organ discharges, EODs) with a specialised electric organ creating an electric field around their body. Objects within this field alter the EOD-induced current at epidermal electroreceptor organs, which are distributed over almost the entire body surface. The detection, localisation and analysis of objects performed by monitoring self-produced electric signals is called active electrolocation. Electric fish employ active electrolocation to detect objects that are less than 12 cm away and have electric properties that are different from those of the surrounding water. Within this range, the mormyrid Gnathonemus petersii can also perceive the distance of objects. Depth perception is independent of object parameters such as size, shape and material. The mechanism for distance determination through electrolocation involves calculating the ratio between two parameters of the electric image that the object projects onto the fish's skin. Electric fish can not only locate objects but can also analyse their electrical properties. Fish are informed about object impedance by measuring local amplitude changes at their receptor organs evoked by an object. In addition, all electric fish studied so far can independently determine the capacitative and resistive components of objects that possess complex impedances. This ability allows the fish to discriminate between living and non-living matter, because capacitance is a property of living organisms. African mormyrids and South American gymnotiforms use different mechanisms for capacitance detection. Mormyrids detect capacitance-evoked EOD waveform distortions, whereas gymnotiforms perform time measurements. Gymnotiforms measure the temporal phase shift of their EODs induced at body parts close to the object relative to unaffected body parts further away.


1993 ◽  
Vol 71 (11) ◽  
pp. 2301-2310 ◽  
Author(s):  
Günther K. H. Zupanc ◽  
Leonard Maler

Apteronotus leptorhynchus, a gymnotiform fish, produces highly regular electric organ discharges of 600–1000 Hz. Short-term modulations of the electric organ discharge ("chirps") were elicited by imitating the discharges of neighboring fish. Chirps displayed an increase in frequency of approximately 100 Hz, a duration of about 15 ms, and an absolute amplitude of 0.5–2 mV. Since, similar to natural conditions, chirps summated with the beat caused by interference of the fish's own electric organ discharge and the imitating discharge, the size and shape of the chirp's amplitude envelope varied greatly according to its phase relative to the beat cycle; however, the frequency of the chirp amplitude modulation was always 50–100 Hz. All 21 males examined chirped, but their rate of chirping varied considerably (range 2–59 chirps/30 s; mean 22 chirps/30 s). In contrast, only one out of nine females chirped (mean 0.25 chirps/30 s). The latency between stimulus onset and first chirp was variable and often long (range 1.0–25.0 s; median 3.3 s). We propose that chirps are not a sensory reflex but a communicatory behavior regulated by hypothalamic peptidergic input.


Sign in / Sign up

Export Citation Format

Share Document