Prior parity positively regulates learning and memory in young and middle-aged rats

Abstract

Reproductive experience in female rats modifies acquired behaviors, induces long-lasting functional neuroadaptations and can also modify spatial learning and memory. The present study supports and expands this knowledge base by employing the Morris water maze, which measures spatial memory. Age-matched young adult (YNG) nulliparous (NULL; nonmated) and primiparous (PRIM; one pregnancy and lactation) female rats were tested 15 d after the litter's weaning. In addition, corresponding middle-aged (AGD) PRIM (mated in young adulthood so that pregnancy, parturition, and lactation occurred at the same age as in YNG PRIM) and NULL female rats were tested at 18 mo of age. Behavioral evaluation included: 1) acquisition of reference memory (platform location was fixed for 14 to 19 d of testing); 2) retrieval of this information associated with extinction of the acquired response (probe test involving removal of the platform 24 h after the last training session); and 3) performance in a working memory version of the task (platform presented in a novel location every day for 13 d, and maintained in a fixed location within each day). YNG PRIM outperformed NULL rats and showed different behavioral strategies. These results may be related to changes in locomotor, mnemonic, and cognitive processes. In addition, YNG PRIM exhibited less anxiety-like behavior. Compared with YNG rats, AGD rats showed less behavioral flexibility but stronger memory consolidation. These data, which were obtained by using a well-documented spatial task, demonstrate long lasting modifications of behavioral strategies in both YNG and AGD rats associated with a single reproductive experience.

Figure 1.

Effects of reproductive experience on the acquisition of reference memory in adult nulliparous (n = 9, dashed lines) and primiparous (n = 8, continuous lines) female rats along 14 training sessions. (A) Latency to find the platform (s). (B) Path length (cm). (C) Swim speed (cm/s). (D) Heading angle relative to platform location (degrees). (E) Number of entries within the training counter. (F) Percentage of time spent within the training quadrant. (G) Percentage of time spent in the inner ring. (H) Percentage of time spent in the intermediate ring. (I) Percentage of time spent in the outer ring. (J) Percentage of time spent in the training counter. Data are expressed as mean ± SEM of 4 trials daily. *, Significant (P < 0.05) difference between groups.

Figure 2.

Effect of reproductive experience on working memory in adult nulliparous (n = 9, dashed lines) and primiparous (n = 8, continuous lines) female rats when the ITI was 10 min (ITI 10) and 60 min (ITI 60). (A) Latency to find platform (s). (B) Path length (cm). (C) Swim speed (cm/s). (D) Number of entries within the day before critical counter. (E) Percentage of time spent within the quadrant in which the platform was located on the previous day. (F) Percentage of time spent in the inner ring. (G) Percentage of time spent within the intermediate ring. (H) Percentage of time spent in the outer ring. (I) Percentage of time spent in the previous day's critical counter. Data are expressed as mean ± SEM for trials across days 1 through 8 (ITI 10) and days 9 through 13 (ITI 60). *, Significant (P < 0.05) difference between groups.

Figure 3.

Effects of reproductive experience on the acquisition of reference memory in middle-aged nulliparous (n = 9, dashed lines) and primiparous (n = 8, continuous lines) female rats along 19 training sessions. (A) Latency to find the platform (s). (B) Path length (cm). (C) Swim speed (cm/s). (D) Heading angle relative to platform location (degrees). (E) Number of entries within the training counter. (F) Percentage of time spent within the training quadrant (G) Percentage of time spent within the inner ring. (H) Percentage of time spent within the intermediate ring. (I) Percentage of time spent within the outer ring. (J) Percentage of time spent within the training counter. Data are expressed as mean ± SEM of 4 trials per day for each group. *, Significant (P < 0.05) difference between groups.

Figure 4.

Effects of reproductive experience on retrieval of the information about the platform location and extinction of reference memory in middle-aged nulliparous (n = 9, dashed lines) and primiparous (n = 8, continuous lines) female rats along 3 consecutive time bins of 60 min each, during the probe test. (A) Path length (cm). (B) Percentage of time spent within the training quadrant. (C) Swim speed (cm/s). Data are expressed as mean ± SEM along 3 consecutive time bins of 60 s each. *, Significant (P < 0.05) difference between groups.

Figure 5.

Effects of reproductive experience on working memory in middle-aged nulliparous (n = 9, dashed lines) and primiparous (n = 8, continuous lines) female rats when the ITI was 10 min (ITI 10) or 60 min (ITI 60). (A) Latency to find platform (s). (B) Path length (cm). (C) Swim speed (cm/s). (D) Number of entries into the previous day's critical counter. (E) Percentage of time spent within the quadrant in which the platform was located on the previous day. (F) Percentage of time spent within the inner ring. (G) Percentage of time spent within the intermediate ring. (H) Percentage of time spent within the outer ring. (I) Percentage of time spent within the previous day's critical counter. Data are expressed as mean ± SEM for the trials across days 1 through 8 (ITI 10) and days 9 through 13 (ITI 60).