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Probability and amplitude of novelty responses as a function of the change in contrast of the reafferent image in G. carapo

A. A. Caputi^*, P. A. Aguilera and M. E. Castelló

Department of Neurofisiología Comparada, Instituto de Investigaciones Biológicas Clemente Estable, Associated Unit of Facultad de Ciencias, Av. Italia 3318, Montevideo, Uruguay, CP 11600

View larger version (23K): [in a new window]   Fig. 1. Characterization of reafferent electrosensory image and its changes. (A) The diagram illustrates the methodology employed. Local electric organ discharge (LEOD) of Gymnotus carapo was recorded between an electrode adjacent to the skin, and the closest base of a cylindrical object placed 2 mm away from the skin. The electrode was a 100 µm bare-tip insulated wire; the object consisted of a 2 mm diameter, 10 mm long plastic tube with a carbon plug electrode in each opening. An external variable resistor r0 was connected to the carbon plugs to set the baseline amplitude (bPP) of the local EOD. A second variable resistor r1 was periodically connected in parallel, using a timed switch setting the comparison LEOD amplitude (cPP). Changes in object longitudinal resistance resulted in marked changes in image contrast. (B) LEOD recorded at the center of the image of a cylindrical object facing the electrosensory fovea. Left: baseline LEOD obtained without load (r=) and right: comparison LEOD obtained when the same object was loaded with a short circuit (r=0). Wave components are labeled as V1, V3 and V4 (according to the nomenclature introduced by Trujillo-Cenóz et al., 1984; V2 is not present at the foveal region). (C) The object resistance change mainly effects the contrast of the image. The amplitudes of each of these LEOD peaks are `one-to-one' functions of the peak-to-peak LEOD (PP), indicating that changes in waveform are small and predictable from the change in PP. (D) The electric image of a metal cylinder consists of a Mexican-hat spatial profile. This is illustrated by the plot of the change in the peak of V3 caused by the presence of the object as a function of distance from the projection of the center of the object. The dotted line indicates the amplitude of V3 in the absence of the object (modified from Caputi et al., 2003).

View larger version (24K): [in a new window]   Fig. 2. Experimental paradigm. (A) The schematic diagrams illustrate the experimental procedures and the corresponding electric images when the change in contrast is maximum (r0= and r1=0). Note the opposite orientation of the `Mexican-hat' profile, referred in the text as `top-inward' and `top-outward', respectively. The raw record at the center of the `Mexican hat' allowed us to measure the difference (PP) between the baseline amplitude and comparison amplitude of the stimulus. The temporal course of the corresponding novelty response elicited by the change in object resistance is shown in the bottom plot. (B) Studies were performed using series of trials consisting of a baseline period followed by a comparison period. Four variables were controlled: the baseline amplitude (depending on r0), the comparison amplitude (depending on r1), the number of baseline images (depending on the duration of the baseline period), the number of comparison images (depending on the duration of the comparison period). (C—F) The experimental paradigms used to elucidate the following issues. The number of images different from the baseline that suffice for detection (C); the effect of the difference between baseline and comparison amplitudes (PP) on the amplitude and the probability of the novelty response (D); the effects of the baseline on amplitude and probability of the novelty response (E); and the effect of stimulus history on the amplitude and probability of the novelty response (F).

View larger version (25K): [in a new window]   Fig. 4. Study of the effect of the number of comparison images on the amplitude of the novelty response. (A) The amplitude of the novelty responses elicited by a single odd event (left) and an increase-and-hold pattern (middle) are not significantly different (t-test, P<0.05, N=20). In the right plot, normalized intervals (1-I/I0) obtained using both experimental paradigms are plotted one-to-one, according to their ordinal number. The linear relationship indicates a similar time course for both novelty responses. (B) Amplitude of the novelty response as a function of difference between baseline and comparison amplitudes (PP) obtained applying a single-odd-event pattern (open symbols) and an increase-and-hold pattern (filled symbols). The experimental protocols are illustrated in the inset. Starting from a single baseline level (43 mV cm-1 in the example), each trial consisted of a pair of stimuli: a single odd event followed 30 s later by a 4 s held stimulus of identical PP, or vice versa. In successive trials PP was varied in a random fashion.

View larger version (17K): [in a new window]   Fig. 5. Probability and amplitude of the novelty response as functions of the increase in image contrast (PP). (A) Amplitude of the novelty response plotted as a function of PP. Data obtained, starting at different baseline contrast, are represented by: 109.27 mV cm-1 (closed circles), 101.35 mV cm-1 (open triangles), 85.43 mV cm-1 (open circles), 58.15 mV cm-1 (open squares) and 51.05 mV cm-1 (closed squares). Parameters calculated fitting the data obtained, starting from every baseline contrast, were similar to those from pooled data. Curve-fitting of the pooled data: novelty response amplitude=0.105xlog10(PP/5.77), r=0.778, N=216, P<0.0001. (B) Probabilities of evoking novelty responses are plotted as a function of PP. Each point represents the probability of evoking a novelty response estimated by its relative frequency in 10 trials using a given pair of baseline contrast and PP in the same fish. Baseline contrast: 58 mV cm-1 (closed squares), 77 mV cm-1 (open circles), 88 mV cm-1 (closed circles) and 108 mV cm-1 (open squares). The threshold50 (PP yielding novelty responses in 50% of the cases) is indicated by the arrow.

View larger version (15K): [in a new window]   Fig. 6. Dynamics of the storage and update of the neural representation of the electric image. Amplitude of the novelty response is plotted as a function of the number of local electric organ discharges (LEODs) in the baseline period. Values are means ± S.D. of the novelty response amplitude (I/I0) obtained in series of trials having baseline periods of the same duration. The inset illustrates the experimental paradigm. The duration of the baseline period of the increase-and-hold pattern was varied to change the number of baseline LEODs before the amplitude step. The number of baseline LEODs were counted (short baseline periods) or estimated by multiplying the period duration by the fish EOD rate. Trial duration was 100 s (two fish, filled symbols) or 30 s (three fish, open symbols). Each symbol shape represents a different fish.

View larger version (27K): [in a new window]   Fig. 7. Parameters of the function relating novelty response and the change in image contrast (PP). (A) Results obtained in a single fish using different increase-and-hold patterns of stimulation, where the amplitude of the novelty response (I/I0) is plotted as a function of PP for three different baseline periods. Symbols indicate the duration of the baseline period: 2 s (open squares; 44 EODs), 10 s (closed circles; 210 EODs), 29 s (open circles; 600 EODs). Trial duration was the same in all experiments (30 s). Note that the scaling constant (the slope of the line fitting the data) increases as a function of the duration of the baseline period. (B) The scaling constants, obtained in the same way in three fish, are plotted as a function of the number of baseline local electric organ discharges (LEODs) (r2=0.88, P<0.01, N=8). Each symbol corresponds to a different fish. (C,D) Threshold50 was studied in three fish for different baseline periods. Probability of evoking novelty responses is plotted as a function of PP. In (C) data obtained from a single fish using baselines of 2 s (closed triangles), 10 s (closed circles) and 29 s (open circles) are compared. In (D) the results were obtained using extreme baseline periods; 0.5 s (open symbols) and 29 s (filled symbols) are compared. Each symbol shape corresponds to a different fish (N=3).

View larger version (20K): [in a new window]   Fig. 3. Electromotor responses to changes in contrast of the electrosensory image of a cylindrical object. (A,B) Mean ± S.D. of the normalized intervals (1-I/I0) plotted as a function of the interval order (N=10 trials). (A) The increase of electric image contrast elicits a typical novelty response characterized by a shortening of the first two intervals after the change in image contrast followed by a slow relaxation curve. Note the significant increase in the S.D. (ANOVA, P<0.01). (B) The same change in contrast but in opposite direction does not elicit a novelty response although there is a significant increase of variability (ANOVA, P<0.01). (C) Single trial recordings of the local electric organ discharge (LEOD) illustrating the experimental paradigm.

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