Poor nutrition during pregnancy and lactation negatively affects neurodevelopment of the offspring: evidence from a translational primate model

Abstract

Background: Studies of the effects of prenatal nutrition on neurodevelopment in humans are complicated because poor nutrition occurs in the context of psychosocial stressors and other risk factors associated with poor developmental outcomes.

Objective: Under controlled experimental conditions, we tested an effect of prenatal nutrition on neurodevelopmental outcomes in the nonhuman primate.

Design: Juvenile offspring of 19 female baboons, whose diets were either restricted [maternal nutrition restriction (MNR)] or who were fed ad libitum (control), were administered the progressive ratio task from the Cambridge Neuropsychological Test Automated Battery. Activity, persistence, attention, and emotional arousal were coded from videotapes. These established, reliable methods were consistent with those used to assess individual differences in the behaviors of school-age children.

Results: MNR offspring (3 female and 4 male offspring) had significantly fewer responses and received fewer reinforcements on the progressive ratio task than did control offspring (8 female and 4 male offspring). MNR offspring showed a more variable activity level and less emotional arousal than did control offspring. Female MNR offspring showed more variable and lower levels of persistence and attention than did female control offspring. Thus, under controlled experimental conditions, data support a main effect of prenatal nutrition on highly translatable neurodevelopmental outcomes.

Conclusions: Nutritional interventions during pregnancy have been successfully used to target neurodevelopmental problems, such as increasing folic acid intake during pregnancy to decrease the incidence of neural tube defects. Results from the current study can be used to support the testing of nutritional preventive interventions for the most-common childhood behavior problems.

FIGURE 1.

Number of responses by nutrition group averaged across sessions (A) and for each session (B). Significant between–nutrition-group effect on the number of responses with age and sex controlled for (ANOVA): F_[1,14] = 5.20, P = 0.039, partial η² = 0.27. There were no significant effects of sex and no nutrition group or sex effects on the pattern of response over time. CTL, control; MNR, maternal nutrition restriction.

FIGURE 2.

Number of responses by nutrition group averaged across sessions (A) and for each session (B). Significant between–nutrition-group effect on the number of responses with age and sex controlled for (ANOVA): F_[1,14] = 5.20, P = 0.039, partial η²= 0.27. There were no significant effects of sex and no nutrition group or sex effects on the pattern of response over time. CTL, control; MNR, maternal nutrition restriction.

FIGURE 3.

Activity level by nutrition group averaged across sessions (A) and for each session (B). Effect of nutrition on the activity level over time (repeated-measures ANOVA): F_[9,126] = 2.41, P = 0.015, partial η² = 0.17. CTL, control; MNR, maternal nutrition restriction.

FIGURE 4.

Persistence level for females by nutrition group averaged across sessions (A) and for each session (B). A: With the use of ANOVA, there were no significant effects of group or group by sex on the level of persistence averaged across sessions; data shown for females. B: With the use of repeated-measures ANOVA, there was an interaction effect of nutrition group and sex on persistence over time (F_[9,126] = 2.19, P = 0.027, partial η² = 0.16); data shown for females. CTL, control; MNR, maternal nutrition restriction.

FIGURE 5.

Attention level for females by nutrition group averaged across sessions (A) and for each session (B). A: With the use of ANOVA, there were no significant effects of group or group by sex on level of persistence averaged across sessions; data shown for females. B: With the use of repeated-measures ANOVA, there was an interaction effect of nutrition group and sex on attention over time (F_[9,126] = 3.55, P = 0.001, partial η² = 0.25); data shown for females. CTL, control; MNR, maternal nutrition restriction.

FIGURE 6.

Observed arousal behaviors across all testing sessions by nutrition group. With the use of ordinal logistic regression, there was an effect of nutrition group on total number of observed arousal behaviors summed across session (Wald's chi-square = 4.79, P = 0.029). MNR, maternal nutrition restriction.