Across continents and demographics, unpredictable maternal signals are associated with children's cognitive function

Abstract

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).

Unpredictable maternal behavior is associated with a blunted infant cortisol response

“…Entropy rate can vary between a minimum value of zero, when a process is perfectly predictable, to a maximum value of 2.807 (the logarithm [base two] of the number of possible transitions [7] of sensory signals at each step), when all possible transitions in this coding scheme are equally likely and maternal signals are most unpredictable. The entropy rates of maternal sensory signals during the 6‐ and 12‐month mother–infant play interactions were correlated ( r = 0.46, p < .01) and consistent with prior research averaged to create a composite measure of unpredictable maternal sensory signals in infancy (Davis et al, 2019).…”

“…Patterns of sensory signals, and particularly their unpredictability, additionally affect the development of systems involved in memory (Molet et al, 2016) and reward (Bolton, Molet, et al, 2018). Recent cross‐species (rodents and humans) evidence suggests unpredictable maternal sensory signals affect cognitive function, with replication across continents (North America and Europe) (Davis et al, 2017, 2019).…”

Chronic psychosocial stress during pregnancy affects maternal behavior and neuroendocrine function and modulates hypothalamic CRH and nuclear steroid receptor expression

“…Our results are consistent with previously published findings and further demonstrate that chronic psychosocial stress during pregnancy can affect qualitative aspects of maternal care, resulting in fragmented and unpredictable care patterns. Erratic maternal care patterns have been previously reported in dams subjected to impoverished/limited bedding environment [42][43][44] and have been linked to emotional and cognitive disturbances in rodent and human offspring 42,43,[53][54][55] . We also find psychosocial stressors contribute to the emergence of PPD by interfering with basal and stress-induced peripartum HPA axis adaptations.…”

“…In addition to these typical measures of maternal care, we analyzed more qualitative aspects of maternal behavior after CGS exposure, including the degree of fragmentation and unpredictability of maternal signals. Fragmented and unpredictable care patterns seem to reflect poorer maternal care quality and have been associated with maternal pathology [42][43][44][53][54][55] . For CGS dams, the mean duration of licking/grooming bouts was significantly shorter than control dams (t-test, t 32 = 2.709, P = 0.011) ( Fig.…”

Early-life adversity and neurological disease: age-old questions and novel answers

“…These correlations persisted when typical measures of adversity, including SES and maternal depression, were included in the models. A second study in an ethnically and demographically distinct prospective cohort identified a relationship between unpredictability of environmental signals in infancy and cognitive outcomes 78 .…”