Prenatal choline supplementation alters the timing, emotion, and memory performance (TEMP) of adult male and female rats as indexed by differential reinforcement of low-rate schedule behavior

Abstract

Choline availability in the maternal diet has a lasting effect on brain and behavior of the offspring. To further delineate the impact of early nutritional status, we examined effects of prenatal-choline supplementation on timing, emotion, and memory performance of adult male and female rats. Rats that were given sufficient choline (CON: 1.1 g/kg) or supplemental choline (SUP: 5.0 g/kg) during embryonic days (ED) 12-17 were trained with a differential reinforcement of low-rate (DRL) schedule that was gradually transitioned through 5-, 10-, 18-, 36-, and 72-sec criterion times. We observed that SUP-females emitted more reinforced responses than CON-females, which were more efficient than both groups of males. In addition, SUP-males and SUP-females exhibited a reduction in burst responding (response latencies <2 sec) compared with both groups of CON rats. Furthermore, despite a reduced level of burst responding, the SUP-males made more nonreinforced responses prior to the DRL criterion as a result of maintaining the previous DRL criterion following transition to a new criterion. In summary, long-lasting effects of prenatal-choline supplementation were exhibited by reduced frustrative DRL responding in conjunction with the persistence of temporal memory in SUP-males and enhanced temporal exploration and response efficiency in SUP-females.

Figure 1.

Mean (+SEM) modified response efficiency (A,C) and burst-responding rate (B,D) plotted as a function of sessions during the DRL 5-sec and DRL 10-sec schedule training stages. Modified response efficiency is determined by a ratio between reinforcement rate and overall responding rate (after subtraction of burst responding rate). Burst-responding rate is determined by the average occurrence of burst responding per minute in a session.

Figure 2.

Mean (+SEM) modified response efficiency plotted as a function of sessions during the DRL 18-sec (A), DRL 36-sec (B), and DRL 72-sec (C) training stages. The individual rectangles in each panel indicate the three sessions that are averaged to represent the three training phases (i.e., early, intermediate, and late phases). The means taken from the three training phases are used for statistical analysis depicted in Figure 4, left. Arrows in A and B indicate the sampled sessions that are further examined with the inter-response times (IRT)-distribution and peak time analyses presented in Figures 5 and 6, respectively.

Figure 3.

Mean (+SEM) burst-responding rate plotted as a function of sessions for DRL 18-sec (A), DRL 36-sec (B), and DRL 72-sec (C) schedule training stages. The means from the three rectangles in each panel are used for statistical analysis depicted in Figure 4, right. The arrow in A indicates the session selected for the burst-ratio analysis presented in Figure 7.

Figure 4.

Mean (+SEM) modified response efficiency (A,C,E) and burst-responding rate (B,D,F) plotted as a function of training phases for DRL 18-sec, DRL 36-sec, and DRL 72-sec schedules. The data points for the DRL 36-sec schedule from the SUP-female rats in the late training phase are duplicated from their data points in the intermediate training phase. This is because the SUP-female group was the only treatment group in which all rats achieved threshold-level performance (modified response efficiency > 0.4) and they were shifted to the DRL 72-sec schedule after an intermediate amount of training with the DRL 36-sec schedule.

Figure 5.

Mean percent maximum frequency of responding as a function of inter-response times (IRTs) plotted in 2-sec time bins during session-45 of the DRL 18-sec schedule for female rats (A) and male rats (B). Mean (+SEM) peak time (sec) for male and female rats as a function of prenatal choline treatments are plotted in C. Significance levels in comparison with SUP-male rats are indicated: *P < 0.05; **P < 0.01; ***P < 0.001.

Figure 6.

Mean percent maximum frequency of responding as a function of inter-response times (IRTs) in 4-sec time bins during session-42 of the DRL 36-sec schedule for female rats (A) and male rats (B) as a function of prenatal choline availability. Mean (+ SEM) peak times (sec) for male and female rats as a function of prenatal choline treatments are plotted in C. Significance levels in comparison with SUP-male rats are indicated: *P < 0.05; **P < 0.01.

Figure 7.

Mean frequency of responding as a function of inter-response times (IRTs) plotted in 2-sec time bins during session-45 of the DRL 18-sec schedule for male rats (A). The two rectangles represent the sample windows (8–10 sec bins and 14–18 sec bins) for burst-ratio analysis. Mean (+SEM) burst-responding ratio for male rats plotted as a function of the two sampled time windows (B). The significance level for the comparison between CON- and SUP-male rats is indicated: **P < 0.01.