REM restriction persistently alters strategy used to solve a spatial task

Abstract

We tested the hypothesis that rapid eye movement (REM) sleep is important for complex associative learning by restricting rats from entering REM sleep for 4 h either immediately after training on an eight-box spatial task (0-4 REMr) or 4 h following training (4-8 REMr). Both groups of REM-restricted rats eventually reached the same overall performance level as did nonrestricted controls, but 0-4 REMr animals were delayed in their improvement in the first few days and lagged behind controls in the middle portion of the training period. More importantly, performance gains of 0-4 REMr rats depended more on simple local cues throughout the 15-d study since, unlike control and 4-8 REMr animals, their error rate increased after daily disruption of the relationship between local (intramaze) cues and the food reward. Thus, although overall performance was only subtly and transiently impaired, due to the ability to use alternate, nonspatial behavioral strategies, complex associative (spatial) learning was persistently impaired by restricting REM for a short critical period each day.

Figure 1.

Learning (A) and improvement (B) curves for the 15-d experiment. (A) For the learning curve the mean number of errors committed per lap are plotted against day of training for controls (solid squares) and 0-4 REMr (open circles). Error bars indicate SEM. Controls committed fewer errors during the middle segment of the study (second 5-d segment; 2) than did the 0-4 REMr group. No significant difference in performance was seen between groups in either the first 5-d segment (1) or the third 5-d segment (3) of the study. (B) Improvement is calculated by subtracting each day's mean number of errors per lap from the group average number of errors per lap on day 1. The 0-4 REMr group (open circles) showed less improvement than did controls (solid squares) during segments 2 and 3 of the study.

Figure 2.

(A) Errors of commission across days. Errors of commission accounted for the differences in learning and improvement curves (Fig. 1 A,B) between 0-4 REMr (open circles) and controls (solid squares). There was a significant difference in errors of commission between groups on day 10 and day 11, as indicated by an asterisk (P < 0.01). Errors of hesitation (B) and errors of omission (C) showed no difference between groups across days.

Figure 3.

(A) Errors per lap on first five laps each day. Rats in the 0-4 REMr group (open circles) committed a higher average number of errors per lap on the initial five laps on 13 of 15 d compared with controls (solid squares). (B) Errors across laps. Both groups showed a decrease in average errors committed from the beginning of the session (lap 1) to the end of the session (lap 30) across days. Errors each lap were averaged across days, with the cutoff set at lap 30 as fewer than two rats per group were completing >30 laps. The 0-4 REMr group increased errors on laps 11 and 12, indicating an effect of disruption due to maze rotation (see Materials and Methods).

Figure 4.

Rat weight and number of laps completed across days. Weight (left axis) decreased for both 0-4 REMr (open circles, thick line) and controls (solid squares, thick line) across the experiment. Controls were significantly heavier during the third 5-d segment. Number of laps completed (right axis) increased for both 0-4 REMr (open triangles, thin line) and controls (solid diamonds, thin line) across the experiment, with no group difference.

Figure 5.

(A) Difference in average errors per lap on the first five laps between 0-4 and 4-8 REMr groups. The average errors per first five laps of 4-8 REMr animals were subtracted from the average errors per first five laps of 0-4 REMr animals each day. The zero line indicates equivalent performance. On 13 of 15 d, 0-4 REMr rats had a higher average number of errors on the first five laps. (B-D) Performance prior to and following maze rotation. The number of errors on lap 10 was subtracted from the number of errors on lap 11 to show an increase (positive numbers) or decline (negative numbers) in errors after the maze was rotated 180°. Small symbols depict one animal, medium sized symbols depict two animals, and large symbols depict three animals. For clarity, points falling on the zero line were omitted. The 0-4 REMr group (B) had a majority of points greater than equivalency, indicating an increase in errors after maze rotation. The 4-8 REMr group (C) and control group (D) have a more equal distribution of points, indicating no overall effect of maze rotation.

Figure 6.

Overhead schematic of the eight-box task. The spatial task required rats to learn locations of food placement from three of eight available box choices on a raised rectangular track. The food-baited boxes are depicted with a star. The same three box positions were baited every lap across the 15 d. Posters, curtains, and colored objects of different shapes (depicted by the gray symbols) surrounded the maze. All environmental cues remained constant throughout the study.