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First published online November 14, 2008
Journal of Experimental Biology 211, 3720-3728 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.020099
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Plasticity in a cerebellar-like structure: suppressing reafference during episodic behaviors

Zhi Zhang* and David Bodznick

Biology Department, Wesleyan University, Middletown, CT 06459 and Marine Biological Laboratory, Woods Hole, MA 02543, USA


Figure 1
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  		Fig. 1. Coupling test protocol. (A) During the pre-coupling period, only parallel fiber stimulus trains (see B) are given to test the AEN responsiveness before coupling. During the coupling period, an excitatory electrosensory stimulus is delivered simultaneously with each parallel fiber train either continuously for 5 min (continuous coupling) or, as illustrated here, in five short bouts of coupling separated by rest periods during which neither parallel fiber stimuli nor electrosensory stimuli are presented (episodic coupling). One coupling cycle is composed of one coupling period (30–60 s) and one resting period (1–9 min). At the bottom, the AEN activity throughout the experiment is illustrated as a raster plot. During the postcoupling period, parallel fiber stimulus trains are again given alone. (B) The duration of a single parallel fiber stimulus train is 250 ms and the inter-train interval is 2 s. Each train has six pulses, each 0.2 ms in duration (25 Hz intra-train frequency). The dipole electric field (2–10 µV, 250 ms) is presented simultaneously with each parallel fiber train. The AEN response to each parallel fiber train is defined as one trial. In tests with fin movement, a single cycle sinusoidal (1 Hz) passive fin movement replaces the parallel fiber stimulus train. St, number of spikes counted during the stimulation period; Tt, duration of the stimulation period in seconds; So, number of spikes counted during the arbitrary control interval outside the stimulation period; To, duration of the arbitrary control interval outside the stimulation period in seconds; see Eqn 1.

 

Figure 2
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  		Fig. 2. Cancellation signals are developed after 5 min of continuous coupling of an electrosensory stimulus to ventilatory movements (A), passive fin movements (B) or direct parallel fiber stimulation (C). A raster plot in each case shows the activity of an AEN before, during and after the 5 or 10 min coupling. Note that the red dots on the left indicate trials when the electrosensory stimulus is presented coupled to ventilation, fin movement or parallel fiber stimulation (blue dots). On the right are spike histograms of 30 trials from the times indicated. Boxes on the bottom traces indicate cancellation signals. In each case there is a significant decrease in the AEN subtracted spike rate after the coupling (P<0.01) compared with that before. V, ventilation; V+E, 2 µV local dipole stimulus coupled to ventilatory movements. F, passive fin movement; F+E, 2 µV dipole stimulus coupled to fin movement. PF, parallel fiber electrical stimulation alone; PF+E, 2 µV dipole coupled with parallel fiber stimulus trains. The arrowheads beneath the raster plots indicate the periods of ventilatory movement, fin movement or parallel fiber stimulation. During coupling the E field stimulus is also presented throughout this same stimulus period.

 

Figure 3
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  		Fig. 3. A cancellation signal appeared in an AEN after five 1 min periods of coupling parallel fiber stimulation to an electrosensory stimulus. (A) Raster plot shows activity of an AEN before, during and after the five 1 min couplings of a 2 µV dipole stimulus to direct parallel fiber stimulation. No measurable change is found after a single 1 min coupling test (P>0.05) during the precoupling period. However, the cancellation signal (or negative image) following five 1 min coupling cycles appears as soon as parallel fiber stimulation is resumed in the post-coupling period (P<0.01), and then fades within minutes as parallel fiber stimulation is given alone. Note that since the parallel fiber inputs are the source of the cancellation signal in the AEN there is no cancellation signal present during the rest periods when the parallel fiber stimulation is stopped along with the electrosensory stimulus. (B) Histograms (30 trials each) from the same data as in the raster plots in A, representing the AEN activity before, during and after a single 1 min coupling test. (C) Histograms before, during and after the five 1 min episodes of coupling. Note the presence of the cancellation signal (seen as a negative image of the initial response of the AEN) when parallel fiber stimulation is resumed after the five 1 min couplings (P<0.01). Also note that during the five 1 min couplings, the response of the AEN to the dipole stimulus gradually declines with each additional coupling cycle. Rasters, histograms and labels as in Fig. 2.

 

Figure 4
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  		Fig. 4. Cancellation signals are absent after one 30 s coupling period but develop during five 30 s coupling periods separated by 5 min rest periods. An excitatory electrosensory stimulus (2 µV) was coupled with parallel fiber stimulus trains (A) or passive fin movements (B). Note the presence of the cancellation signal in the AEN activity when the parallel fiber trains or fin movements are resumed during the post-coupling period. Rasters, histograms and labels as in previous figures.

 

Figure 5
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  		Fig. 5. A cancellation signal is developed after five 30 s couplings separated by irregular rest intervals. (A) A raster plot showing activity of an AEN before, during and after the five 30 s couplings separated by variable rest intervals. The cancellation signal is apparent when parallel fiber stimulation resumes after the last rest period. (B) Histograms of AEN activity from the periods indicated. Note the AEN response to the dipole stimulus gradually declines with each additional coupling cycle. Labels as in previous figures.

 

Figure 6
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  		Fig. 6. Once the negative image is fully developed, it can be long lasting. (A) The negative image appears after five 30 s coupling tests, and then another five 30 s couplings are given to reinforce the negative image. The negative image is still apparent after a 2 h rest period without parallel fiber or electrosensory stimulation, but then fades over 20 min after parallel fiber stimulus trains alone are resumed. (B) Histograms as in previous figures.

 

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© The Company of Biologists Ltd 2008