Sex-dependent cognitive performance in baboon offspring following maternal caloric restriction in pregnancy and lactation

Abstract

In humans a suboptimal diet during development has negative outcomes in offspring. We investigated the behavioral outcomes in baboons born to mothers undergoing moderate maternal nutrient restriction (MNR). Maternal nutrient restriction mothers (n = 7) were fed 70% of food eaten by controls (CTR, n = 12) fed ad libitum throughout gestation and lactation. At 3.3 ± 0.2 (mean ± standard error of the mean [SEM]) years of age offspring (controls: female [FC, n = 8], male [MC, n = 4]; nutrient restricted: female [FR, n = 3] and male [MR, n = 4]) were administered progressive ratio, simple discrimination, intra-/extra-dimension set shift and delayed matching to sample tasks to assess motivation, learning, attention, and working memory, respectively. A treatment effect was observed in MNR offspring who demonstrated less motivation and impaired working memory. Nutrient-restricted female offspring showed improved learning, while MR offspring showed impaired learning and attentional set shifting and increased impulsivity. In summary, 30% restriction in maternal caloric intake has long lasting neurobehavioral outcomes in adolescent male baboon offspring.

Figure 1.

A and B, Maternal nutrient restricted offspring (n = 7—male and female combined, closed bars) respond less (A) and earn less reinforcements (B) than control offspring (n = 12—male and female combined, open bars) in the progressive ratio task to assess motivation. Mean ± SEM; #, P ≤ .06.

Figure 2.

A, Simple discrimination (SD) tasks (SD1-5).  Overall treatment effects were determined in males and females (P < .05).  Post hoc analyses show borderline differences in female nutrient restricted offspring ([FR] n = 3) make fewer errors than female control offspring ([FC], n = 8) during SD3 and in male nutrient restricted offspring ([MR], n = 4) make more errors than male control offspring ([MC], n = 4) during SD2. Mean ± standard error of the mean (SEM); #P ≤ .06-.08.B, Simple discriminations (SD6-8) followed by reversals (SR1-3).  Overall treatment effects were determined in males and females (P < .05).  Post hoc analyses show the female nutrient restricted ([FR] n = 3) offspring make fewer errors than female control ([FC] n = 3) offspring during SD6 task. No differences in male offspring, Male control ([MC] n = 4), male nutrient restricted ([MR] n = 4), offspring, mean ± SEM; *P ≤ .05.

Figure 3.

Intra-/extradimension attention set shift test. No differences in female offspring were measured, female control ([FC] n = 8), female nutrient restricted ([FR] n = 3) offspring. A treatment effect in males was determined, male nutrient restricted ([MR] n = 4) offspring make more errors than male control (MC) offspring during the ER test stage.  Mean ± standard error of the mean (SEM); *P < .05.

Figure 4.

A, Observing response latency. No differences in female offspring were found, female control ([FC] n = 8), female nutrient restricted ([FR] n = 3).  A treatment effect in males was determined, male nutrient restricted ([MR] n = 4) offspring have shorter latencies compared to male control ([MC] n = 4) offspring. Mean ± standard error of the mean (SEM); *P < .05. B, Results pooled by treatment show a borderline decrease in accuracy following 0 second delay intervals in the maternal nutrient restriction (MNR) offspring (n = 7, male and female combined, closed bars) versus CTR offspring (n = 12, male and female combined, open bars.  FC (n = 8), FR (n = 3), MC (n = 4), MR (n = 4), Mean ± SEM; #P ≤ .06-.08. C, Choice response latencies showed no differences in females, FC (n = 8) and FR (n = 3).  A treatment effect in males shows decreased choice response latencies following 1 second delay in MR (n = 4) offspring versus MC (n = 4) offspring. Mean ± SEM; *P ≤ .05.