Environmental influences on the pace of brain development

Abstract

Childhood socio-economic status (SES), a measure of the availability of material and social resources, is one of the strongest predictors of lifelong well-being. Here we review evidence that experiences associated with childhood SES affect not only the outcome but also the pace of brain development. We argue that higher childhood SES is associated with protracted structural brain development and a prolonged trajectory of functional network segregation, ultimately leading to more efficient cortical networks in adulthood. We hypothesize that greater exposure to chronic stress accelerates brain maturation, whereas greater access to novel positive experiences decelerates maturation. We discuss the impact of variation in the pace of brain development on plasticity and learning. We provide a generative theoretical framework to catalyse future basic science and translational research on environmental influences on brain development.

Fig. 1. Associations between socio-economic status and cortical thickness.

Trajectories shown in light and dark blue are conceptual, based on findings interpolated across multiple studies. Horizontal grey lines represent the age ranges of individual studies, as shown on the horizontal axis. Brain regions shown in blue indicate negative relationships between socio-economic status (SES) and cortical thickness (ref. corresponds to grey line 1). Brain regions shown in red indicate positive relationships between SES and cortical thickness (grey line 2, ref.; grey line 3, ref.; grey line 4, ref.; grey line 5, ref.; grey line 6, ref.; grey line 7, ref.; grey line 8, ref.; grey line 9, ref.; grey line 10, ref.; grey line 11, ref.). These curves are consistent with more modest main effects of SES on cortical thickness when averaging is done across large age ranges than when small age ranges are focused upon. The inset shows a schematic of potential cellular underpinnings of cortical thickness as measured by MRI: glial number and size, neuron number and size, synaptic complexity and myelination^–. Cells are enlarged relative to cortical thickness to show detail. Brain image corresponding to grey line 1 adapted with permission from ref., OUP. Brain image corresponding to grey line 2 adapted with permission from ref., CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/). Brain image corresponding to grey line 3 adapted with permission from ref., Sage Publishing. Brain image corresponding to grey line 4 adapted with permission from ref., CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/).

Fig. 2. Associations between socio-economic status and functional brain network segregation.

Trajectories shown in solid and dashed grey lines are conceptual, based on findings interpolated across multiple studies. Horizontal grey lines represent the age ranges of individual studies, as shown on the horizontal axis (grey line 1, ref.; grey line 2, ref.; grey line 3; ref.; grey line 4, ref.). Brain regions shown in red indicate socio-economic status (SES)-associated differences in functional network segregation, with adolescents from higher-SES backgrounds showing stronger positive associations between age and segregation. Curves are drawn to be consistent with functional network segregation across the studies shown; the studies used a range of measures of segregation, as illustrated in the bottom-right inset. The top-right inset illustrates a common metric of functional connectivity used to estimate functional brain networks: the Pearson product-moment correlation coefficient. Brain images in the lower part of the figure adapted with permission from ref., OUP.

Fig. 3. Integrative theory: childhood experiences affect the pace of brain development.

According to our model, experiences that are chronic or repetitive and negative encourage faster maturation and increase allostatic load, potentially restricting plasticity. Experiences that are rare and positive, triggering surprise and awe, are associated with strong neurochemical signals to delay maturational processes and enhance plasticity. Experiences in the other quadrants (rare and negative, or repetitive and positive) are predicted to have smaller effects on the global pace of maturation.