Exposure to unpredictable maternal sensory signals influences cognitive development across species

Abstract

Maternal care is a critical determinant of child development. However, our understanding of processes and mechanisms by which maternal behavior influences the developing human brain remains limited. Animal research has illustrated that patterns of sensory information is important in shaping neural circuits during development. Here we examined the relation between degree of predictability of maternal sensory signals early in life and subsequent cognitive function in both humans (n = 128 mother/infant dyads) and rats (n = 12 dams; 28 adolescents). Behaviors of mothers interacting with their offspring were observed in both species, and an entropy rate was calculated as a quantitative measure of degree of predictability of transitions among maternal sensory signals (visual, auditory, and tactile). Human cognitive function was assessed at age 2 y with the Bayley Scales of Infant Development and at age 6.5 y with a hippocampus-dependent delayed-recall task. Rat hippocampus-dependent spatial memory was evaluated on postnatal days 49-60. Early life exposure to unpredictable sensory signals portended poor cognitive performance in both species. The present study provides evidence that predictability of maternal sensory signals early in life impacts cognitive function in both rats and humans. The parallel between experimental animal and observational human data lends support to the argument that predictability of maternal sensory signals causally influences cognitive development.

Keywords: brain development; cognition; cross-species; early experiences; maternal care.

Fig. 1.

Rats reared by dams providing less-predictable maternal sensory signals performed poorly on a spatial memory task (reduced ratio of time spent exploring objects in a novel vs. familiar location) during adolescence.

Fig. 2.

Infants exposed to less-predictable maternal sensory signals (high entropy rate) at 1 y of age have (A) lower child MDI scores at 2 y of age (r = −0.34, P < 0.001) and (B) poor child delayed-recall scores on the WRAML at 6.5 y of age (r = −0.27, P < 0.05).

Fig. 3.

Mediation model of maternal sensitivity, entropy rate, and child MDI scores. All coefficients are unstandardized. Test of indirect effects indicates that entropy rate partially mediates the relation between maternal sensitivity and child cognitive performance. The value in parentheses is the coefficient describing the relation between maternal sensitivity and child MDI scores not accounting for entropy rate. **P < 0.01, ***P < 0.001.