Neural meaning making, prediction, and prefrontal–subcortical development following early adverse caregiving

Abstract

Early adversities that are caregiving-related (crEAs) are associated with a significantly increased risk for mental health problems. Recent neuroscientific advances have revealed alterations in medial prefrontal cortex (mPFC)-subcortical circuitry following crEAs. While this work has identified alterations in affective operations (e.g., perceiving, reacting, controlling, learning) associated with mPFC–subcortical circuitry, this circuitry has a much broader function extending beyond operations. It plays a primary role in affective meaning making, involving conceptual-level, schematized knowledge to generate predictions about the current environment. This function of mPFC–subcortical circuitry motivates asking whether mPFC–subcortical phenotypes following crEAs support semanticized knowledge content (or the concept-level knowledge) and generate predictive models. I present a hypothesis motivated by research findings across four different lines of work that converge on mPFC–subcortical neuroanatomy, including (a) the neurobiology supporting emotion regulation processes in adulthood, (b) the neurobiology that is activated by caregiving cues during development, (c) the neurobiology that is altered by crEAs, and (d) the neurobiology of semantic-based meaning making. I hypothesize that the affective behaviors following crEAs result in part from affective semantic memory processes supported by mPFC–subcortical circuitry that over the course of development, construct affective schemas that generate meaning making and guide predictions. I use this opportunity to review some of the literature on mPFC–subcortical circuit development following crEAs to illustrate the motivation behind this hypothesis. Long recognized by clinical science and cognitive neuroscience, studying schema-based processes may be particularly helpful for understanding how affective meaning making arises from developmental trajectories of mPFC–subcortical circuitry.

Heterogeneity in caregiving-related early adversity: Creating stable dimensions and subtypes

“…Here, we focus on caregiving-related early adversities (crEAs), which include adverse experiences that directly undermine the parent-child relationship, including caregiver-involved maltreatment and separations from caregivers. In contrast to other childhood adversities, crEAs represent interruptions, separations, and/ or dysfunctions in the parent-child transactional system (Cicchetti & Rizley, 1981;Sameroff & Chandler, 1975) and can disrupt the developmental processes that play a foundational role in emotional and cognitive health (discussed in Cicchetti & Toth, 2005;Tottenham, 2020). Yet, there is heterogeneity within crEAs that may predict unique outcomes.…”

Assessing Unpredictability in Caregiver-Child Relationships: Insights from Theoretical and Empirical Perspectives

“…Animal models suggest that predictability supports the development of hippocampal/limbic and pleasure/reward-related brain circuitry (Bolton et al, 2018;F. K. Johnson et al, 2018;Molet et al, 2016), with important implications for prefrontalsubcortical development and the stress response system (Bolton et al, 2019;Tottenham, 2020).…”

“…In this paper we aim to integrate different theoretical and corresponding empirical orientations to provide a set of conceptual and methodological tools for researchers seeking connections between caregiver-child unpredictability and other constructs of interest. We focus on children's immediate caregiving system across infancy and early childhood because it is the primary source of information about the type of environment children can expect concurrently and probabilistically across their lifespan, shaping development accordingly (Bateson et al, 2004;Tottenham, 2020). We broadly define caregivers as biological, adoptive, and foster parents or other custodial relatives who support a child's development and use the term dyad or dyadic when we refer to both caregiver and child.…”

“…Contingent exchanges between caregivers and children might be sources of information about the environment, as infants depend on their caregiver to regulate all their primary needs (Beebe et al, 2010). For instance, a responsive caregiving environment may produce an association between "needs + needs-are-met," fostering infants' mental representation of security that contributes to a rule of regulation regarding the caregiver (Cassidy et al, 2013;Tottenham, 2020). Conversely, a non-contingent environment may create the association between "needs + needs-are-not-met," promoting a rule of non-regulation.…”

“…Conversely, a non-contingent environment may create the association between "needs + needs-are-not-met," promoting a rule of non-regulation. With repetition, these associations may contribute to an affective schema or mental model that contributes to children's ability to forecast caregivers' behavior (Thompson et al, 2003;Tottenham, 2020).…”