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Early life exposure to unpredictable parental sensory signals shapes cognitive development across three species.

ABSTRACT: Exposure to early life adversity has long term consequences on cognitive function. Most research has focused on understanding components of early life adversities that contribute to later risk, including poverty, trauma, maltreatment, and neglect. Whereas these factors, in the aggregate, explain a significant proportion of emotional and cognitive problems, there are serious gaps in our ability to identify potential mechanisms by which early life adversities might promote vulnerability or resilience. Here we discuss early life exposure to unpredictable signals from the caretaker as an understudied type of adversity that is amenable to prevention and intervention. We employ a translational approach to discover underlying neurobiological mechanisms by which early life exposure to unpredictable signals sculpts the developing brain. First, we review evidence that exposure to unpredictable signals from the parent during sensitive periods impacts development of neural circuits. Second, we describe a method for characterizing early life patterns of sensory signals across species. Third, we present published and original data illustrating that patterns of maternal care predict memory function in humans, non-human primates, and rodents. Finally, implications are discussed for identifying individuals at risk so that early preventive-intervention can be provided.

SUBMITTER: Davis EP

PROVIDER: S-EPMC9630745 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Early life exposure to unpredictable parental sensory signals shapes cognitive development across three species.

Davis Elysia Poggi EP McCormack Kai K Arora Hina H Sharpe Desiree D Short Annabel K AK Bachevalier Jocelyne J Glynn Laura M LM Sandman Curt A CA Stern Hal S HS Sanchez Mar M Baram Tallie Z TZ

Frontiers in behavioral neuroscience 20221020

Exposure to early life adversity has long term consequences on cognitive function. Most research has focused on understanding components of early life adversities that contribute to later risk, including poverty, trauma, maltreatment, and neglect. Whereas these factors, in the aggregate, explain a significant proportion of emotional and cognitive problems, there are serious gaps in our ability to identify potential mechanisms by which early life adversities might promote vulnerability or resilie ...[more]

PMID: 36338881

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Project description:BackgroundEarly 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.MethodsIn 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.OutcomesIn 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.InterpretationsThe 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).

Project description:BackgroundExcess bodyweight (BMI >25 kg/m2) in midlife (age 40-65 years) has been linked to future cognitive decline and an increased risk of dementia. Whether chronic exposure to excess bodyweight in the early decades of life (<40 years) is associated with compromised cognitive function by midlife, however, remains unclear. This study therefore aimed to test potential bidirectional direct and indirect pathways linking cumulative exposure to excess bodyweight and cognitive function in the early decades of life.MethodsIn this longitudinal analysis, harmonised measures of BMI and cognitive function were available in 19 742 participants aged 47-53 years recruited to the 1946 National Survey of Health and Development (n=2131), the 1958 National Child Development Study (n=9385), and the 1970 British Cohort Study (n=8226). Individual BMI trajectories spanning three decades from age 10-40 years were created for each participant and excess bodyweight duration, BMI change between ages, and cumulative excess bodyweight exposure were calculated. Harmonised measures of verbal and non-verbal ability, mathematical ability, and reading ability were used to create a latent factor for childhood cognitive function, and immediate and delayed recall, animal naming, and letter-search speed tests were used for midlife cognitive function. Multivariable linear regression and structural equation models (SEM) were used to test for potential bidirectional relationships between cognition and excess bodyweight in both individual cohorts and pooled datasets while accounting for other potential early-life confounders.FindingsIncreases in BMI during adolescence and greater cumulative exposure to excess bodyweight across early life were associated with lower midlife cognitive function in all cohorts (eg, pooled difference in cognitive function per 10 years excess bodyweight duration -0·10; 95% CI -0·12 to -0·08; p<0·001). Further adjustment for childhood cognitive function attenuated many of these associations towards the null (eg, pooled difference in cognitive function per 10 years excess bodyweight duration -0·04; 95% CI -0·06 to -0·02; p=0·001), however, with any remaining associations then fully attenuating once further adjusted for other early-life factors (eg, pooled difference in cognitive function per 10 years excess bodyweight duration 0, -0·03 to 0·01; p=0·38). In the reverse direction, low childhood cognition was associated with greater cumulative exposure to excess bodyweight over the next four decades, although much of this relationship was found to probably be explained via other potentially modifiable upstream early-life factors such as childhood disadvantage. SEM in all cohorts suggested the presence of modest direct and indirect pathways connecting earlier cognitive function to later excess bodyweight, but scarce evidence for an effect of early-life excess bodyweight on cognitive function by midlife.InterpretationThe association between cumulative exposure to excess bodyweight in early life and lower cognitive function in midlife is probably confounded by a persistently lower cognitive function from childhood. Initiatives to improve early-life factors such as childhood disadvantage and education, however, might exert dual but independent benefits on both of these factors before old age.FundingAlzheimer's Research UK, Diabetes Research and Wellness Foundation, Diabetes UK, British Heart Foundation, and Medical Research Council.

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Early life exposure to unpredictable parental sensory signals shapes cognitive development across three species.

Publications

Early life exposure to unpredictable parental sensory signals shapes cognitive development across three species.

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