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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.

SUBMITTER: Davis EP

PROVIDER: S-EPMC5625898 | biostudies-other | 2017 Sep

REPOSITORIES: biostudies-other

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Exposure to unpredictable maternal sensory signals influences cognitive development across species.

Davis Elysia Poggi EP Stout Stephanie A SA Molet Jenny J Vegetabile Brian B Glynn Laura M LM Sandman Curt A CA Heins Kevin K Stern Hal H Baram Tallie Z TZ

Proceedings of the National Academy of Sciences of the United States of America 20170911 39

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 (<i>n</i> = 128 mo ...[more]

PMID: 28893979

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Project description:BACKGROUND:Early life experiences have persisting influence on brain function throughout life. Maternal signals constitute a primary source of early life experiences, and their quantity and quality during sensitive developmental periods exert enduring effects on cognitive function and emotional and social behaviors. Here we examined if, in addition to established qualitative dimensions of maternal behavior during her interactions with her infant and child, patterns of maternal signals may contribute to the maturation of children's executive functions. We focused primarily on effortful control, a potent predictor of mental health outcomes later in life. METHODS:In two independent prospective cohorts in Turku, Finland (N = 135), and Irvine, CA, USA (N = 192) that differed significantly in race/ethnicity and sociodemographic parameters, we assessed whether infant exposure to unpredictable patterns of maternal-derived sensory signals portended poor effortful control. OUTCOMES:In both the Irvine and Turku cohorts, unpredictable sequences of maternal behavior during infancy were associated with worse effortful control at one year of age. Longitudinal analyses demonstrated that this association persisted for as long as each cohort was assessed-until two years of age in the Turku cohort and to 9.5 years in the Irvine cohort. The relation of unpredictable maternal signals during infancy and the measures of executive function persisted after adjusting for covariates. INTERPRETATIONS:The consistency of our findings across two cohorts from different demographic backgrounds substantiated the finding that patterns, and specifically unpredictable sequences, of maternal behaviors may influence the development of executive functions which may be associated with vulnerability to subsequent psychopathology. FUND: This research was supported by the National Institutes of Health (NIH) awards P50MH096889, HD051852, NS041298, HD02413, HD050662, HD065823, and by the FinnBrain funders: Academy of Finland (129839, 134950, 253270, 286829, 287908, 308176, 308252), Jane and Aatos Erkko Foundation, Signe and Ane Gyllenberg Foundation, Yrjö Jahnsson Foundation, and State Research Grants (P3498, P3654).

Dataset Information

Exposure to unpredictable maternal sensory signals influences cognitive development across species.

Publications

Exposure to unpredictable maternal sensory signals influences cognitive development across species.

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