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

Stefan Schuster

Institut für Biologie I, Hauptstrasse 1, Albert-Ludwigs-Universität Freiburg, D-79104 Freiburg, Germany

View larger version (11K): [in a new window]   Fig. 1. Measurement of the efficiency with which a given stimulus elicited a novelty response after a pause in the ongoing electric organ discharges (EODs). The stimulus was given twice (vertical arrows): (1) n EODs after the pause and (2) 10 000 EODs, or approximately 200 s, later when the fish had returned to steady firing. The response is a transient shortening in the interpulse interval between successive EODs (ordinate). In the schematic trace shown, a Gymnotus carapo fired with a stable interpulse interval of approximately 20 ms. The fish was then induced to pause its EODs for the period indicated in grey. For each of the two subsequently elicited responses, the maximum reduction T in interpulse interval from the pre-stimulus interval T was determined, and T was normalized to T. The efficiency of the stimulus when given n EODs after the pause, (n), was taken as the ratio of the two normalized interval modulations, as indicated.

View larger version (10K): [in a new window]   Fig. 2. Even strong electrosensory stimuli failed to elicit novelty responses when given directly after a pause in the electric organ discharge (EOD). The stimulus was a single cycle of a 1 kHz sine wave delivered far above threshold at a peak-to-peak field strength of 235 mV cm-1. Each row illustrates the two responses obtained, first when the stimulus was given at the nth post-pause EOD (left traces; n=50, 100, 1000, top to bottom row) and, second, 10 000 EODs later during steady firing (right traces). Stimulus timing is indicated by arrows. Pause durations were 3.9, 16 and 17 s (top to bottom).

View larger version (10K): [in a new window]   Fig. 3. Mechanosensory stimuli were able to elicit novelty responses immediately after a prior discharge interruption. The three rows illustrate pairs of responses obtained when the stimulus (top trace) was given n electric organ discharges (EODs) after a pause (left traces; n=50, 100, 1000, top to bottom row) and 10 000 EODs later during steady firing (right traces). Stimulus timing is indicated by arrows. Pause durations were 7, 75 and 20 s (top to bottom).

View larger version (10K): [in a new window]   Fig. 4. The dramatic post-pause reduction in the size of electrically elicited novelty responses is not an aftereffect of a pause-eliciting electrical `shock'. Post-pause efficiency, (100), was determined 100 electric organ discharges (EODs) after a pause. The stimulus used was an electrical pulse (one cycle of a 1 kHz sinewave, peak-to-peak field strength 235 mV cm-1). Pausing was elicited either by electrical shocks (`Electrical'; fish gc1, dark grey columns, 18 pauses; fish gc2, light grey columns, 10 pauses; fish gc3, black columns, 15 pauses) or, after appropriate training of the fish, by gently tapping on the wall of the tank (`Mechanical'; 12, 10 and 15 pauses, respectively). Values are means + S.E.M.

View larger version (12K): [in a new window]   Fig. 5. The reduced efficiency of electrical pulses in eliciting a normal-sized post-pause novelty response was not due to insufficient intensity (A) or temporal patterning (B). (A) One cycle of a 1 kHz sinewave was delivered at one of the set field strengths indicated on the abscissa (0.9-235 mV cm-1 peak-to-peak). Different symbols relate to three fish, gc1 (circles), gc2 (squares) and gc3 (triangles), and show (100), average efficiencies 100 electric organ discharges (EODs) after a pause. Measurements were obtained after 220 pauses. The number of pauses for each fish, given in order from low to high intensity, was: gc1, 20, 20, 7, 53; gc2, 10, 30, 10, 30; gc3, 10 each). The steady-state response strengths increased with increasing intensity but so did the post-pause strengths, leaving their ratio constant. (B) The post-pause efficiency (100) did not differ when either a single pulse or an extended series of pulses was given as stimulus. Means + S.E.M. are shown, obtained in experiments with two fish, gc1 (dark grey columns) and gc2 (light grey columns). The different time courses of the stimuli are illustrated schematically below the columns. Stimuli were a single cycle of a 1-kHz sine wave, a group of six such pulses with 20 ms silent intervals separating successive pulses or a continuous wave of 100 cycles. All stimuli had the same intensity (235 mV cm-1 peak-to-peak).

View larger version (8K): [in a new window]   Fig. 6. Low-frequency (LF) electrical stimuli that recruit the ampullary electroreceptors more and the tuberous electroreceptors less than high-frequency stimuli (HF) are more efficient in eliciting post-pause responses. Means + S.E.M. of efficiency, (100), 100 electric organ discharges (EODs) after a pause were determined for three different types of stimulus: the mechanical stimulus (`Mech'; shown in Fig. 3), a low-frequency stimulus (a single cycle of a 2 Hz or a 10 Hz sine wave, selected with equal likelihood) and a high-frequency electrical stimulus (one cycle of a 1 kHz sine wave). LF and HF electrical stimuli had the same intensity (2.35 mV cm-1 peak-to-peak). Data were obtained from 171 pauses in two fish (fish gc1, dark grey columns, 26, 35 and 20 measurements for mechanosensory, LF and HF stimuli, respectively; fish gc2, light grey columns, 30 measurements for each stimulus type).

View larger version (13K): [in a new window]   Fig. 7. The post-pause recovery of efficiency in eliciting a novelty response. Means ± S.E.M. of are shown for the electrical stimulus (filled symbols) and for the mechanical stimulus (open symbols). The diagram comprises 972 responses of two fish (fish gc1, circles; fish gc2, squares) after a total of 486 pauses. The electrical stimulus (see Fig. 2) was given at various preselected values of n after 153 (gc1) and 120 (gc2) pauses; the mechanical stimulus (see Fig. 3) was given after 93 (gc1) and 120 (gc2) pauses. When given 20 electric organ discharges (EODs) after a pause, the electrical stimulus failed to elicit a response in either fish. Tentative courses of post-pause efficiency towards the `normal' efficiency (=1; indicated by the dotted horizontal line) are fitted by eye for the electrical stimulus (continuous line) and the mechanical stimulus (broken line).

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