Introduction to the Special Issue on Understanding Neurobiological Implication of Maltreatment: From Preschool to Emerging Adulthood

Evidence on the psychological and behavioral impacts of child maltreatment is vast. More recently, empirical efforts are directed to unravel the neurobiological process that underlies the effect of adverse rearing environments on human development across the life span (Cicchetti & Toth, 2005; Gilbert et al., 2009). Such biopsychosocial models of human behavior are seeded in the concept of biological embedding, the notion that early experiences alter underlying biological systems to produce stable, long-lasting differences, ultimately influencing trajectories of health, behavior, and/or learning (Hertzman, 2000). Over the last decade, evidence for credible candidate mechanisms has emerged (Hertzman & Boyce, 2010; Rutter, 2012). Accordingly, we are now well positioned to investigate when, and by what means, child maltreatment may influence key biological systems. This special issue includes articles with empirical evidence on a range of biological mechanisms linking child maltreatment to various outcomes, spanning from preschool to emerging adulthood. Below, we provide an overview of some key concepts framing research on the biological impact of child maltreatment primarily utilizing a developmental psychopathology framework (Cicchetti & Toth, 2009). Within these concepts, we highlight the nine papers comprising this special issue, including eight empirical papers utilizing multiple methodologies and exploring diverse outcomes as well as one review paper (McCrory, Ogle, Gerin, & Viding, 2019) highlighting compromised social functioning as a key mechanism linking childhood maltreatment to subsequent psychopathology. We hope that this issue stimulates an expansion of interdisciplinary research on underlying biological systems given that mechanisms mediating enduring vulnerabilities in maltreated individuals remain relatively scarce. Furthermore, recognition of early biological markers underlying pathogenic effects of child maltreatment is important to inform both public health initiatives and clinical practice.

A key tenet of developmental psychopathology is the concept of multifinality. Multifinality suggests that individuals exposed to the same adverse event or risk factor, such as child maltreatment, may have divergent patterns of adaptation and maladaptation (Cicchetti & Rogosch, 1996). The likelihood of a specific outcome is dependent on the complex interaction of multiple factors and processes related to individual characteristics, experiences, timing, and the developmental history of the individual (Sroufe, 1990). This concept is highly relevant when attempting to understand why some individuals exposed to child maltreatment experience maladaptive outcomes, while others do not, and how biological factors may play a role in these divergent pathways. The papers in this special issue represent diverse methodological approaches to studying neurobiological pathways linking child maltreatment to adjustment and psychopathology outcome across the life span. Several papers involve longitudinal data to delineate patterns over time, leading to various outcomes including alcohol use (DeBellis et al., 2019; Oshri et al., 2019), shyness (Poole, MacMillan, & Schmidt, 2018), trait impulsivity (Hallowell et al., 2019), internalizing and externalizing problems (Demers et al., 2019; Oshri et al., 2019; Peverill, Sheridan, Busso, & McLaughlin, 2019), and adaptive functioning (Demers et al., 2019). Another important aspect in the investigation of the neurobiology of child maltreatment is the concept of multilevel analysis. While much of the research to date has focused primarily on psychosocial outcomes, in the past two decades, empirical studies have incorporated multilevel investigations of biological sequelae. Hertzman and Boyce (2010) identified four candidate systems that met the criteria for biological embedding. These systems can be influenced by and respond to early life stress experiences throughout the life course, which has the capacity to influence later behaviors and health through dysfunctional operations. These candidate systems include the hypothalamic–pituitary–adrenal (HPA) axis (e.g., cortisol), the autonomic nervous system (ANS; e.g., heart rate variability), and central nervous system structure and function, in particular executive function within prefrontal cortex and systems of social affiliation, involving the amygdala and locus coeruleus with accompanying higher order cerebral connections. These neurobiological systems are interconnected and are affected by the various stressors associated with child maltreatment, as well as being influenced by, and shaping multiple domains of biological and psychological development (Cicchetti & Handley, 2019). Furthermore, in line with the concept of multifinality, neurobiological development in maltreated individuals is not affected in the same way in all individuals. These multiple analytic levels are addressed by the collection of papers in this special issue.

The first paper involves an investigation of HPA axis activity (Hibel, Mercado, & Valentino, 2019). As the key neuroendocrine system involved in stress responses, the HPA axis has been extensively studied in the context of childhood maltreatment, with consistent evidence of dysregulated activity, mostly with hypocortisolism patterns (Koss & Gunnar, 2018). Given the sensitivity of the HPA axis to external stressors, it is not surprising that caregivers are potent regulators of HPA activity, with the quality of parent–child interactions acting as a buffer of the HPA axis for children (Atkinson et al., 2013) and is related to dyadic attunement (Atkinson, Jamieson, Khoury, Ludmer, & Gonzalez, 2016). This is particularly relevant in the context of maltreating dyads since maltreatment may undermine the capacity of early relationships to provide the stress buffering benefits (Koss & Gunnar, 2018). Using a unique cross-lagged, dyadic design to examine diurnal cortisol levels in mothers and their preschool-aged children, Hibel, Mercado, and Valentino (2019) found differential transmission (from mother to child, or vice versa) and attunement patterns between maltreating and nonmaltreating dyads. With respect to transmission, only within the maltreating group did mothers’ cortisol predict later child adrenocortical levels. Furthermore, in the maltreating group, midday cortisol levels were not attuned, suggesting a possible physiological disconnect during a time where dyads may be more likely to coregulate given interactions over the course of the day. These findings raise important issues regarding how patterns of dyadic responsivity and transmission direct the development of children’s stress response system.

The second candidate system for biological embedding, the ANS is the focus of the next two papers. As a component of the biological stress system (Stratakis & Chrousos, 1995), the ANS is an established component of emotion (Kreibig, 2010). Electrophysiological approaches are used to gauge the sympathetic and parasympathetic processes of ANS and are tuned for individual differences in self-regulation and adjustment. There is also a large body of research showing that child maltreatment is associated with emotional and self-regulation problems from childhood through adulthood. Research shows that the development of child self-regulation is bound to socialization processes that occur within the home with the primary caregiver. Lunkenheimer and colleagues (2019) add important insight to this link by examining the impact of child maltreatment on parasympathetic system reactivity, as well as its expression during a stressful dyadic interaction. More specifically, they found differences in ANS activity in maltreating and nonmaltreating dyads (Lunkenheimer, Busuito, Brown, Panlilio, & Skowron, 2019). In particular, patterns of respiratory sinus arrhythmia (RSA; a measure of heart rate variability associated with breathing rates) in response to interpersonal challenges were dependent on whether interactive repair (moving from negative or mismatched emotional or behavioral state to a mutually positive or matched state) was mother or child initiated. High levels of mother-initiated repair were present across both nonmaltreating and maltreating dyads and were protective. However, in maltreating dyads where there were lower levels of mother-initiated repair, child RSA increased over time. Furthermore, in maltreating dyads, children were initiating interactive repair highlighting the maladaptive interactive processes within these dyads. These findings are important in light of the long-term impact of ANS dysregulation over time, as illustrated in the study by Poole, MacMillan, and Schmidt (2018) who investigated ANS activity in a prospective, longitudinal study of maltreated adolescent females. Examining resting heart period (HP; a physiological measure of stress vulnerability), they found that a stable, low HP trajectory over the course of 1 year was associated with higher baseline shyness and greater stability of shyness over time, whereas a high stable HP trajectory was unrelated to shyness at either time points. Greater reports of shyness were positively associated with higher levels of anxiety. This heterogeneity in developmental patterns of resting state ANS activity may influence the continuity of traits linked with socioemotional vulnerability such as shyness.

There is strong evidence that child maltreatment is associated with structural and functional changes in the brain, particularly in the anterior cingulate cortex, hippocampus, and amygdala, as well as the prefrontal cortex (Teicher & Samson, 2016). These brain areas support higher level cognitive processes and executive functions, such as sustained attention, emotion regulation, and impulsivity, and are particularly vulnerable to the impact of child maltreatment due to the protracted development of these brain areas throughout adolescence and early adulthood (Glaser, 2014). Despite the links between child maltreatment and neurocognitive function and brain function (McCrory, Gerin, & Viding, 2017), investigations linking brain changes to outcomes have been examined less frequently and are more complex than initially believed (Teicher, Samson, Anderson, & Ohashi, 2016). The next series of papers in the special issue focus on neural structure, function, and connectivity as candidate systems for biological embedding, with several papers examining brain changes as a mechanism between child maltreatment and later outcome.

Cognitive and brain differences are evident across various disorders and are often hallmarks of psychopathology. Exposure to child maltreatment may contribute to these findings; however, analyses parsing out independent effects are often not addressed. To tease apart this issue, DeBellis and colleagues (2019) examined academic achievement, neurocognitive performance, and structural brain scans in three groups: (1) adolescents with a maltreatment history and alcohol use disorder (AUD), (2) adolescents with AUD and no history of maltreatment, and (3) healthy adolescents. Maltreated adolescents with AUD performed worse on broad tests of reading and math fluency and exhibited difficulties with sustained attention compared to healthy controls and adolescents with AUD and no childhood maltreatment history. Underlying structural differences were also seen in the maltreated/AUD group including smaller volume of the anterior corpus callosum, an area associated with sustained attention. The volume of the hippocampus, an area associated with attention and working memory, decreased significantly with age in the maltreated/AUD group. This suggests that early exposure to child maltreatment may increase the vulnerability of the hippocampus to adverse effects of alcohol later on. The documentation of preexisting problems with sustained attention in maltreated youth may contribute to treatment resistance and increased risk of relapses; thus, treatment protocols targeting attention regulation skills should be considered. It also provides evidence that maltreatment history should be addressed in neuroimaging studies of substance use.

Impulsivity, the focus of the next paper (Hallowell et al., 2019), is a multifactorial construct implicated in substance use disorders (Lee, Hoppenbrouwers, & Franken, 2019) and child maltreatment (Liu, 2019). In this study, Hallowell and colleagues (2019) investigated the impact of child maltreatment on impulsivity via functional magnetic resonance imaging (fMRI) during a verbal working memory task in a sample of emerging adult females (ages 18–25 years). Higher levels of self-reported childhood maltreatment were positively associated with impulsivity, poorer working memory performance, and overall lower neural response. Regional analyses indicated that the association was primarily driven by reduced neural activity in the left caudal middle frontal gyrus and bilateral posterior parietal regions. Notably, neural activity partially mediated the association between childhood maltreatment and impulsivity thus providing support that neural mechanisms link early exposure of maltreatment to later consequences, including impulsivity. Given that impulsivity is related to substance use, interventions involving working memory training or targeting the frontoparietal network may help improve cognitive processes as well as ameliorate engagement in risky behaviors linked to addiction.

The paper by Oshri et al. (2019) focuses specifically on the amygdala, a subcortical structure involved in fear and emotional processing, implicated in numerous psychiatric and substance use disorders, and a vulnerable site to the effects of child maltreatment. This study provides a high-resolution analysis of the impact of early adversity by parsing the morphology of the amygdala into its subnuclei and considering laterality effects with a series of elegant analyses. Using exploratory and confirmatory factor analyses on volumetric measures, reduced right amygdala volume in the basolateral amygdala and central-medial amygdala emerged as significant areas associated with severity of adverse childhood experiences. An indirect effect between early adversity and later psychopathology via reduced right baslolateral amygdalar volume was also demonstrated, using path analysis. As the first study in humans to examine the effect of early adversity on amygdalar subnuclei, these findings address some of the inconsistencies in the literature and extend research to highlight the role of amygdalar morphology in the association between early adversity and later internalizing symptomatology and substance use. Interventions which include components that target maladaptive emotion processing and promote effective emotion regulation skills may be particularly useful with individuals with histories of adverse childhood experiences.

Moving from a microlevel to macro-level examination of how early adversity influences neuroaffective development to confirm risk of stress-related emotion dysregulation, Peverill, Sheridan, Busso, and McLaughlin (2019) investigate task-related connectivity in a longitudinal study of adolescents. The focus of their study, the amygdala-ventromedial prefrontal cortex (vmPFC) circuit is implicated in threat reactivity and emotion regulation and is particularly sensitive to early stress. The authors extended previous work by demonstrating stronger negative functional connectivity between the amygdala and vmPFC in youth exposed to high threatening experiences—characterized by reports of child physical, emotional, and sexual abuse. Stronger negative connectivity was also related to internalizing and externalizing symptomatology; however, it was not a significant mediator between child abuse and later psychopathology. These findings provide additional support for theoretical models in which exposure to child abuse results in heightened appraisals of threatening circumstances, leading to enhanced reactivity to negative emotional stimuli and greater difficulty modulating emotional responses. Further research is needed to advance our understanding of the role of emotion regulation circuitry implicated in psychopathology following child maltreatment.

Quality caregiving is a species-expected stimulus that not only buffers against elevations of stress system hormones during childhood (Atkinson et al., 2016; Koss & Gunnar, 2018) but also plays a fundamental role in the development of emotion neurocircuitry, including the amygdala-medial prefrontal network (Callaghan & Tottenham, 2016). In a longitudinal study, Demers and colleagues (2019) demonstrated that the association between maternal relationship quality and frontal lobe volume was dependent on maltreatment status, with high maternal relationship quality associated with greater frontal lobe volume only in nonmaltreated individuals. Furthermore, frontal lobe volume mediated the association between maternal relationship quality and adult adaptive functioning. These findings were not seen in individuals with a history of maltreatment, suggesting that exposure to maltreatment likely disrupts the buffering effects by which maternal relationship quality impacts frontal lobe development. Given the gradual decrease in the importance of maternal modulation of children’s neurocircuitry with from childhood to adolescence (Gee et al., 2014) and the increasing importance of peers (Doom, Hostinar, VanZomeren-Dohm, & Gunnar, 2015), future research should investigate the role of positive relationships outside the caregiving environment within an early adversity framework. Interventions that bolster interpersonal skill development, problem-solving, and abilities supporting frontal lobe functioning will likely promote adaptive functioning in vulnerable youth and adults.

This special issue is rounded out with an integrative review from McCrory, Ogle, Gerin, and Viding (2019) who promote the perspective that exposure to child maltreatment compromises social functioning and attenuates social support in ways that increase vulnerability for mental health problems later on. Expanding on their latent vulnerability theoretical framework, in this review, they focus on neurocognitive adaptation, specifically highlighting the impact of stress vulnerability (ability of an individual to negotiate stress) and stress generation (probability increased future stressful events) on social function and subsequent psychopathology. Focusing on three domains underlying social function—threat processing, reward processing, and emotion regulation, they provide an overview of neuroimaging studies, which are in line with empirical findings from other papers in this special issue. The discussion highlights the importance of future research focusing on integrative and synergistic effects of various neurocognitive systems which contribute to impaired social function, as well as an expansion of indices tapping into social function, including social understanding. Finally, the authors make key suggestions to move the field forward, recommending regarding use of computational models and ecologically valid assessments that can link brain imaging to everyday behaviors and functioning. Such an approach will increase translation of mechanism to practice.

Collectively, the papers in this special issue speak to the widespread impact of child maltreatment. Capitalizing on methodological and technological innovations, these papers highlight the science of biological embedding across multiple systems and outcomes. The age ranges covered in this special issue, preschool to adolescence to emerging adulthood, represent dynamic periods of transition characterized by extraordinary psychological, social, physiological, and anatomical changes and growth (Brown & Jernigan, 2012; Steinberg, 2005; Wood et al., 2018). While these transitional periods are malleable and thereby more susceptible to stress, they also carry opportunity for neural plasticity and amenability for neurobiological change through positive experiences and interactions with the environment. Across all papers, recommendations are provided regarding developing interventions that target underlying mechanisms of action, including emotion and stress regulation, or transdiagnostic approaches to address commonly experienced issues related to maltreatment, such as interpersonal function, hyperarousal, or poor self-concept. Given the important role of early caregiving relationships, preventive interventions supporting stable, nurturing parenting practices are needed. Although many of the candidate systems of biological embedding were included in this special issue, several systems were not, including immune system and inflammation and epigenetic modification (Danese & Baldwin, 2017; Hertzman & Boyce, 2010; Rutter, 2012). We hope that future examinations of the long-term impact of child maltreatment extend their reach to include a multitude of systems, as well as developmental trajectories. Many of the papers included in this special issue were longitudinal designs. However future studies should prospectively investigate putative biological mediators, accounting for delayed phenotypic expression. In closing, we are extremely grateful to all the researchers who contributed to this special issue. Although we have learned much about the impact of child maltreatment on biological systems, there appears to be much yet to be discovered. We hope the papers in this special issue provide an impetus for additional new work which will continue to push the boundaries of our understanding about biological embedding and provides new solutions to mitigating the long-lasting impact of child maltreatment.