Introduction
Across development, caregivers play an outsize role in the emotional lives of children (Ainsworth, Reference Ainsworth1969; Bowlby, Reference Bowlby1969; Lieberman, Reference Lieberman2017), particularly in children’s development of the capacity to regulate emotions (Calkins & Hill, Reference Calkins and Hill2007; Cassidy, Reference Cassidy1994). Beginning at birth, stable caregiving is fundamental to children’s emotional development (Hofer, Reference Hofer1978, Reference Hofer1994; Tottenham, Reference Tottenham2012), and caregivers provide extrinsic scaffolding of children’s increasingly emergent capacity to regulate their own emotions (Dozier et al., Reference Dozier, Roben, Caron, Hoye and Bernard2018; Gianino & Tronick, Reference Gianino and Tronick1988; Hofer, Reference Hofer1994; Katz & Hunter, Reference Katz and Hunter2007; Pratt et al., Reference Pratt, Singer, Kanat-Maymon and Feldman2015). Over time, and as caregivers adapt their behaviors to the child’s changing needs, children undergo a shift from full reliance on caregivers to provide external regulation of their emotions in infancy to greater reliance on their own intrinsic capacity of self-regulation later in development (Grolnick et al., Reference Grolnick, McMenamy and Kurowski2006; Thompson & Goodman, Reference Thompson, Goodman, Kring and Sloan2009). It is theorized that it is via this protracted socialization, which unfolds across development and occurs in tandem with fluctuations in other sources of social buffering, that caregivers influence their children’s mental health and emotional well-being. The daily involvement of caregivers in their children’s emotional lives directly influences children’s development of psychobiological underpinnings of emotion regulation (Callaghan & Tottenham, Reference Callaghan and Tottenham2016; Gee, Reference Gee2016; Tan et al., Reference Tan, Oppenheimer, Ladouceur, Butterfield and Silk2020; Tottenham, Reference Tottenham2015).
Though the role of parents in the emotional lives of children has universally important implications for child development across contexts (Morris et al., Reference Morris, Silk, Steinberg, Myers and Robinson2007), caregiving influences on the development of emotion regulation may have a particularly salient impact in the context of children’s exposure to adversity due to the centrality of emotion regulation in processes of risk and resilience. Here we define resilience as positive mental health outcomes in the context of exposure to adversity; we consider resilience to be situated within a broader socioecological context and to be a dynamic and multifaceted process that is both influenced by and acts upon multiple systems (Masten et al., Reference Masten, Lucke, Nelson and Stallworthy2021). Emotion regulation, or an individual’s ability to affect what emotions they experience, and when and how they experience and express these emotions (Gross, Reference Gross1998), has been highlighted as a key transdiagnostic factor linking exposure to adversity and psychopathology (e.g., Ehring & Quack, Reference Ehring and Quack2010; Heleniak et al., Reference Heleniak, Jenness, Vander Stoep, McCauley and McLaughlin2016; Kim & Cicchetti, Reference Kim and Cicchetti2010; Villalta et al., Reference Villalta, Smith, Hickin and Stringaris2018). Numerous studies have underscored that exposure to childhood adversity is linked with prototypically maladaptive coping strategies (Compas et al., Reference Compas, Connor-Smith, Saltzman, Thomsen and Wadsworth2001)—for example, exposure to community violence, peer victimization, and parental loss are associated with higher levels of rumination (Heleniak et al., Reference Heleniak, Jenness, Vander Stoep, McCauley and McLaughlin2016, Reference Heleniak, King, Monahan and McLaughlin2018; McLaughlin et al., Reference McLaughlin, Hatzenbuehler and Hilt2009; McLaughlin & Hatzenbuehler, Reference McLaughlin and Hatzenbuehler2009), and meta-analytic findings show an association between maltreatment and lower levels of emotion regulation across domains, as well as increased reliance on prototypically maladaptive strategies (Aldao & Christensen, Reference Aldao and Christensen2015) such as avoidance and suppression (Gruhn & Compas, Reference Gruhn and Compas2020). Despite demonstrated links between adversity exposure and reliance on potentially maladaptive emotion regulation strategies at a group level, empirical evidence supports that, on an individual level, prototypically adaptive emotion regulatory processes following adversity may represent a mechanistic process of resilience. Across multiple cross-sectional and prospective samples representing youth exposure to a diverse range of adversities, reliance on maladaptive emotion regulation strategies and emotional reactivity have been found to mediate the association between youth exposure to trauma and the development of psychopathology (Heleniak et al., Reference Heleniak, Jenness, Vander Stoep, McCauley and McLaughlin2016; Kim & Cicchetti, Reference Kim and Cicchetti2010; Kim-Spoon et al., Reference Kim-Spoon, Cicchetti and Rogosch2013; Weissman et al., Reference Weissman, Bitran, Miller, Schaefer, Sheridan and McLaughlin2019).
Here we propose that caregiving influences in the context of children’s emotional lives—and on children’s development of corticolimbic circuitry and emotion regulation—are a primary mechanism by which caregivers promote resilience following exposure to adversity. While the focus of the current review is on the role that caregivers play in children’s emotional lives, we note that there are numerous, interdependent ways that caregiver involvement in the lives of children influences children’s responses to adversity—and therefore shapes processes of risk and resilience (see Williamson et al., Reference Williamson, Creswell, Fearon, Hiller, Walker and Halligan2017 for a review). For example, in the wake of exposure to adversity, caregivers have central roles to play in providing physical safety, establishing and maintaining routines, obtaining psychological treatment and medical care, and detecting risk to minimize exposure to subsequent trauma. Rather than being completely distinct caregiving influences, we view these as complementary and dependent on one another. For example, it is challenging for a caregiver to optimally support their child’s emotional development when facing housing or food insecurity, limited access to resources, and ongoing threats to physical and psychological safety.
In the sections that follow, within the context of a model by which children’s brain and behavioral development mediates the association between adversity exposure and children’s mental health, we examine the effects of caregiving on the link between adversity exposure and children’s brain and behavioral development (i.e., a moderated mediation model; Fig. 1). Here we conceptualize adversity broadly—including but not limited to physical abuse, sexual abuse, neglect, serious accidental injury, community violence, natural disaster, and forced displacement. Specifically, we delineate how caregivers impact children’s emotional functioning in the context of adversity from a multisystemic perspective—focused on behavioral, psychological, and neurobiological processes—and, further, synthesize evidence for associations between these processes and resilience following adversity. In addition, we review empirical work that has underscored important developmentally specific effects of caregiving involvement in the emotional lives of children following adversity. We conclude by highlighting the importance of considering caregiving influences on children’s emotional lives in both intervention and policy settings.
Mechanisms by which caregivers influence children’s trajectories of resilience following exposure to adversity
A substantial body of literature has focused on caregiving influences on children’s responses to trauma, highlighting several key ways that caregivers promote resilience via involvement in the emotional lives of offspring (Appleyard & Osofsky, Reference Appleyard and Osofsky2003; Gewirtz et al., Reference Gewirtz, Forgatch and Wieling2008; Williamson et al., Reference Williamson, Creswell, Fearon, Hiller, Walker and Halligan2017; Wilson et al., Reference Wilson, Lengua, Meltzoff and Smith2010). Drawing upon this literature, a meta-analysis of 14 studies comprising 4,010 participants that examined the impact of both positive and negative parenting practices on children’s development of posttraumatic stress-related symptomatology following trauma exposure concluded that negative parenting behaviors (e.g., hostility, overprotection) accounted for 5.3% of the variance in children’s symptom development whereas positive parenting behaviors (e.g., warmth) accounted for 2% of the variance in children’s symptom development (Williamson et al., Reference Williamson, Creswell, Fearon, Hiller, Walker and Halligan2017). These findings suggest that parents appear to exert a relatively small effect on children’s mental health-related outcomes following adversity exposure, though the magnitude of these estimates is constrained by the focus of this meta-analysis on broad domains of parenting rather than more detailed mechanistic processes, as well as its focus on posttraumatic stress disorder (PTSD) as the sole clinical outcome of interest. Despite these constraints, these findings invite more detailed understanding of the specific ways that parental involvement in the emotional lives of children in the wake of exposure to adversity has the potential to inform prevention and intervention efforts aimed at reducing the onset of trauma-related symptomatology. In the present review, we focus on several specific mechanisms by which caregiver involvement in the emotional lives of children following adversity may promote resilience. We highlight caregivers’ attachment relationships with children as an ever-present basis of parental influences on child development in the context of adversity, and focus on caregiver promotion of generally benevolent environments and inputs in childhood, parental emotion socialization, including parental assistance with execution of specific emotion regulation strategies, and parental buffering of stress, as mechanisms by which caregiving is likely to influence children’s developmental trajectories following exposure to adversity.
Child–caregiver attachment relationships as the basis of caregiver influences
From birth, caregiver–child attachment relationships form the basis of a child’s exploration of the world, and function as a critical lens through which children filter information about their environment and experiences (Bowlby, Reference Bowlby1969). Secure attachment with caregivers facilitates caregivers’ support of critical tasks of typical development (see Gee & Cohodes, Reference Gee and Cohodes2021 for a review) (Fig. 2). During infancy, children learn that primary caregivers are responsive to their needs and that caregiving behaviors are both predictable and associated with safety, with caregivers transitioning from being a source of comfort and protection to taking on more complex roles in facilitating infants’ increasing exploration of their environment (Lieberman et al., Reference Lieberman, Ippen and Van Horn2015). During the transition to toddlerhood, caregivers continue to solidify their association with predictability and safety as children navigate strong—and at times conflicting—desires for both exploration and independence, as well as safety and security in their close contact with parents (Lieberman et al., Reference Lieberman, Ippen and Van Horn2015). Later, throughout early and middle childhood, caregivers scaffold children’s exploration of physical and social environmental inputs as children develop increasingly complex schemas about the social and physical world, all while serving as a primary source of external regulation of children’s emotions (Kopp, Reference Kopp1989; Morris et al., Reference Morris, Silk, Steinberg, Myers and Robinson2007). During the transition to adolescence, although the potency of caregivers’ role as a source of external regulation wanes in some contexts as offspring become increasingly independent and other attachment figures (e.g., peers, romantic partners) begin to play a greater role in social buffering processes (Gee, Reference Gee2016; Hostinar et al., Reference Hostinar, Sullivan and Gunnar2014), caregivers continue to play important roles in socializing coping behaviors and guiding adaptive behavior (Butterfield et al., Reference Butterfield, Siegle, Lee, Ladouceur, Forbes, Dahl, Ryan, Sheeber and Silk2019; Rogers et al., Reference Rogers, Perino and Telzer2020).
In this developmentally salient and evolving manner, caregiver–child attachment relationships form the backdrop of children’s increasing exploration, independence, and accomplishment of tasks of development. These processes are ubiquitous in both typical development and in the context of adversity, and evidence suggests that caregivers leverage attachment relationships to promote resilience following exposure to adversity, with the quality of a child’s attachment largely governing caregivers’ capacity to support children following adversity exposure (Lieberman, Reference Lieberman2004; Lieberman et al., Reference Lieberman, Van Horn and Ozer2005; Lieberman et al., Reference Lieberman, Chu, Horn and Harris2011; Lieberman & Pawl, Reference Lieberman and Pawl1988). Further, recent theoretical work highlights that specific patterns in caregiving behavior—namely the co-occurrence of predictability and safety—may be particularly salient inputs during infancy and toddlerhood, and may prime a caregiver’s ability to serve as a source of external regulation later in development by directly impacting neural circuitry supporting emotion regulation (Gee & Cohodes, Reference Gee and Cohodes2021). We argue that these critical elements of caregiving in the earliest periods of development not only facilitate optimal caregiver inputs in infancy and toddlerhood but also enable ideal input from caregivers across development. In the context of exposure to adversity, caregivers are likely to be able to take advantage of prior establishment of themselves as predictable—and as harbingers of safety—to facilitate greater parental attenuation of the impact of adversity via the numerous pathways described below.
One outstanding question pertains to the degree to which aversive caregiving has the potential to undermine parental influences on children’s recovery following adversity. As exposure to any form of trauma can influence nearly all aspects of children’s functioning and development, and result in a broad set of beliefs and altered cognitions regarding a generalized lack of safety in the world, children’s exposure to both trauma that involves a caregiver in a perpetrating role (e.g., perpetration of maltreatment, neglect) and trauma that does not directly involve a caregiver (e.g., medical trauma, natural disaster) has the potential to “shatter the protective shield” of parental attachment (Lieberman & Amaya-Jackson, Reference Lieberman and Amaya-Jackson2005). For example, even when caregivers do not perpetrate trauma, children may come to view their caregivers as inconsistent or unpredictable sources of protection and safety in the context of a risky environment. Therefore, caregiver-child attachment relationships—the very mechanism by which parents support children in the aftermath of adversity—may be compromised by adversity (Bernstein & Freyd, Reference Bernstein and Freyd2014).
However, the degree to which adversity in the context of the caregiver–child relationship disrupts a child’s orientation to a caregiver as a source of stability and safety may vary by developmental stage. Specifically, there is increasing evidence that, in the earliest stages of development, offspring prefer cues related to their caregivers, even when these cues have an inherently aversive quality. This absence of avoidance learning is believed to facilitate formation of attachment relationships even in the context of adversity (Gee, Reference Gee2020; R. Perry & Sullivan, Reference Perry and Sullivan2014). Specifically, young children were more likely to approach conditioned stimuli acquired in the presence of their caregiver, and, conversely, to avoid stimuli acquired in the absence of their caregiver (Tottenham et al., Reference Tottenham, Shapiro, Flannery, Caldera and Sullivan2019). These findings directly parallel evidence from the rodent literature that offspring approach aversive stimuli when paired with a maternal cue during a period of development when maternal presence dampens affective reactivity in rodent offspring (Moriceau & Sullivan, Reference Moriceau and Sullivan2006). This pronounced attraction to caregiver-related cues—even in the context of adversity—in the earliest stages of development may facilitate attachment and promote close physical proximity between caregivers and offspring despite adversity. The degree to which this pattern has broad ecological validity to a range of trauma exposures and across development remains unclear, and failure to establish safety and predictability in the context of caregiving relationships in infancy and toddlerhood may alter the degree to which caregivers can enact optimal influences on children’s emotional lives later in development, particularly in the context of adversity (Gee & Cohodes, Reference Gee and Cohodes2021; R. Perry & Sullivan, Reference Perry and Sullivan2014).
Caregiver promotion and maintenance of broadly benevolent childhood environments and predictable routines in the context of family life
One primary way in which caregivers may promote resilience is via the establishment and maintenance of a home environment that yields beneficial inputs for children following adversity. In addition to extensive empirical work highlighting associations between childhood adversity and the development of psychopathology, substantial work has highlighted broad and general promotive childhood experiences that may mitigate the impact of adversity (Crandall et al., Reference Crandall, Miller, Cheung, Novilla, Glade, Novilla, Magnusson, Leavitt, Barnes and Hanson2019, Reference Crandall, Broadbent, Stanfill, Magnusson, Novilla, Hanson and Barnes2020; Narayan et al., Reference Narayan, Rivera, Bernstein, Harris and Lieberman2018; Wright et al., Reference Wright, Masten, Narayan, Goldstein and Brooks2013). In a major study assessing the impact of benevolent childhood experiences (BCEs) on later development of trauma-related psychopathology, endorsement of a higher number of BCEs (e.g., having good neighbors, having an opportunity to have fun) was found to be associated with lower levels of psychopathology and, critically, to offset the impact of adverse childhood events on the development of psychopathology later in life (Narayan et al., Reference Narayan, Rivera, Bernstein, Harris and Lieberman2018). These findings, based on the establishment of the BCEs questionnaire (Narayan et al., Reference Narayan, Rivera, Bernstein, Harris and Lieberman2018), are in line with previous evidence that parental maintenance of a positive home environment—and broad and general promotive and protective factors—are a primary mechanism by which caregivers support children’s resilient functioning in the context of exposure (e.g., Collishaw et al., Reference Collishaw, Pickles, Messer, Rutter, Shearer and Maughan2007; Doom et al., Reference Doom, Seok, Narayan and Fox2021; K. Howell et al., Reference Howell, Graham-Bermann, Czyz and Lilly2010; Morris et al., Reference Morris, Hays-Grudo, Zapata, Treat and Kerr2021), possibly via the impact of positive parenting practices and beneficial environments on children’s symptomatology via promotion of children’s emotion regulation (K. Howell et al., Reference Howell, Graham-Bermann, Czyz and Lilly2010).
One particular element of family environments that has received considerable attention is caregiver maintenance of consistent home routines and practices, yielding a sense of predictability for youth (Greeff & Wentworth, Reference Greeff and Wentworth2009; Williamson, Hiller et al., Reference Hiller, Meiser-Stedman, Lobo, Creswell, Fearon, Ehlers, Murray and Halligan2018). Caregiver maintenance of family routines following children’s exposure to adversity has been linked to reduced child symptomatology (Boyce, Reference Boyce and B.1981; Foy, Reference Foy1992). Extending this work to the COVID-19 pandemic, a predictable home environment buffered the impact of exposure to COVID-19-related stress on children’s mental health during the pandemic (Glynn et al., Reference Glynn, Davis, Luby, Baram and Sandman2021), with parental maintenance of family routines also emerging as a specific moderator of the association between exposure to COVID-related stress and youth symptomatology (Cohodes et al., Reference Cohodes, Kribakaran, Odriozola, Bakirci, McCauley, Hodges, Sisk, Zacharek and Gee2021) and family-level resilience (Bates et al., Reference Bates, Nicholson, Rea, Hagy and Bohnert2021). Though additional empirical work is required to elucidate specific mechanisms by which predictable home routines confer resilience during or following exposure to adversity, it is possible that predictable home routines signal predictable caregiver involvement in the emotional lives of children—as sources of external emotion regulation and active participants in the daily socialization of emotion—and therefore exert influences on child symptomatology via promotion of child regulation.
Caregiver socialization of children’s emotions
Gottman’s parental meta-emotion philosophy (Gottman et al., Reference Gottman, Katz and Hooven1996) proposes that caregivers’ beliefs about their children’s emotions—including the degree to which they are aware of, accepting of, and directly involved in coaching their children’s emotions—manifests in behavioral responses to children’s displays of negative emotions. Parental meta-emotion philosophy predicts numerous outcomes in offspring, including the development of psychopathology (see Gottman et al., Reference Gottman, Katz and Hooven1997 for a review). In the context of adversity exposure, parental emotion coaching, in particular—or the degree to which parents engage in assisting their children in identifying the emotions they are experiencing, show respect for their children’s emotions, and actively engage in helping children cope with emotion-eliciting situations (Gottman et al., Reference Gottman, Katz and Hooven1996, Reference Gottman, Katz and Hooven1997)—has been highlighted as a buffer of children’s development of symptomatology following exposure to a range of stressors (Cohodes et al., Reference Cohodes, Chen and Lieberman2017; Cohodes et al., Reference Cohodes, Kribakaran, Odriozola, Bakirci, McCauley, Hodges, Sisk, Zacharek and Gee2021; Fogarty et al., Reference Fogarty, Wood, Giallo, Kaufman and Hansen2019; Greene et al., Reference Greene, McCarthy, Estabrook, Wakschlag and Briggs-Gowan2020; V. Johnson & Lieberman, Reference Johnson and Lieberman2007; L. Katz et al., Reference Katz, Stettler and Gurtovenko2015; L. F. Katz & Windecker-Nelson, Reference Katz and Windecker-Nelson2006), including stress exposure in the context of a global pandemic (Cohodes et al., Reference Cohodes, Kribakaran, Odriozola, Bakirci, McCauley, Hodges, Sisk, Zacharek and Gee2021; Lobo et al., Reference Lobo, Lunkenheimer, Lucas-Thompson and Seiter2021). Of note, additional empirical work suggests that parental emotion awareness, acceptance, and coaching affect children’s outcomes following exposure via encouragement of children’s own intrinsic emotion regulation capacities in the context of negative emotion (B. H. Ellis et al., Reference Ellis, Alisic, Reiss, Dishion and Fisher2014; Wu et al., Reference Wu, Feng, Yan, Hooper, Gerhardt and Ku2020). These findings—suggesting a primary mechanism by which caregiver involvement in the emotional content of a stressor may impact children’s behavior, and, resultingly, children’s development of trauma-related symptomatology—are consistent with prominent etiological models of childhood PTSD highlighting caregivers’ capacity to affect children’s tendency to engage in negative reappraisals of the event and use of maladaptive coping and regulation strategies (Cobham et al., Reference Cobham, McDermott, Haslam and Sanders2016; Ehlers et al., Reference Ehlers, Mayou and Bryant2003; Ehlers & Clark, Reference Ehlers and Clark2000; Meiser-Stedman, Reference Meiser-Stedman2002; Stallard & Smith, Reference Stallard and Smith2007; Williamson et al., Reference Williamson, Creswell, Butler, Christie and Halligan2016). For example, a longitudinal empirical investigation of children’s mental health following natural disasters demonstrated that parent–child interactions characterized by negative parental appraisals of a traumatic event, as well as promotion of avoidant coping behaviors, were associated with increased child symptomatology, and further, suggest that this association is likely driven by the effect of parental appraisals and coping responses on children’s development of their own maladaptive coping strategies (Hiller et al., Reference Hiller, Meiser-Stedman, Lobo, Creswell, Fearon, Ehlers, Murray and Halligan2018).
Highly related to parental emotion coaching, parental availability for discussion of stressful events may attenuate the impact of adversity exposure on children’s development of symptomatology (Carpenter et al., Reference Carpenter, Elkins, Kerns, Chou, Greif Green and Comer2017; Cohodes et al., Reference Cohodes, Kitt, Baskin-Sommers and Gee2021; Stallard et al., Reference Stallard, Velleman and Baldwin2001). Parents who report providing children with frequent opportunities to discuss their feelings about recent stress exposure in an age-appropriate manner may buffer children’s development of stress-related psychopathology via direct impacts on the valence of a child’s appraisal of an event (Williamson et al., Reference Williamson, Halligan, Coetzee, Butler, Tomlinson, Skeen and Stewart2018; Williamson et al., Reference Williamson, Hiller, Meiser-Stedman, Creswell, Dalgleish, Fearon, Goodall, McKinnon, Smith and Wright2018). In addition, parents may affect the content of children’s narratives about their adversity exposure (Fivush et al., Reference Fivush, Hazzard, McDermott Sales, Sarfati and Brown2003), in the service of buffering harmful impacts of adversity on children’s development of symptomatology (Kilmer & Gil-Rivas, Reference Kilmer and Gil-Rivas2010).
Recent advances in measurement of caregiver emotion socialization (Cohodes et al., Reference Cohodes, Preece, McCauley, Rogers, Gross and Gee2021) have facilitated assessment of the degree to which caregivers support children’s emotion regulation at the strategy-specific level. In the context of exposure to stress, a recent study examined parental assistance with prototypically adaptive and maladaptive emotion regulation studies as a potential moderator of the impact of family-level COVID-related stress exposure on children’s development of internalizing and externalizing symptomatology. Results suggest that caregiver assistance with prototypically adaptive emotion regulation strategies (i.e., acceptance) buffered the impact of exposure to COVID-related stress, while assistance with prototypically maladaptive strategies (e.g., rumination) exacerbated its impact (Cohodes et al., Reference Cohodes, McCauley, Preece, Gross and Gee2022). Though this line of work is emerging, the impact of caregiver emotion socialization on children’s mental health in the context of adversity exposure likely varies by the specific emotion regulatory processes that caregivers support.
Neurobiological mechanisms associated with caregiving influences on children’s emotional functioning
A growing literature in developmental neuroscience has identified neurobiological processes by which caregiving influences children’s emotional functioning (Callaghan & Tottenham, Reference Callaghan and Tottenham2016; Farber et al., Reference Farber, Gee and Hariri2022; Gee, Reference Gee2020; Tan et al., Reference Tan, Oppenheimer, Ladouceur, Butterfield and Silk2020; Tottenham, Reference Tottenham2020), providing mechanistic insight into the ways that caregivers promote resilience following adversity. Affective learning and regulation are broadly supported by corticolimbic circuitry, which involves connections between the prefrontal cortex and subcortical structures involved in emotion processing (Kovner et al., Reference Kovner, Oler and Kalin2019). Among key regions in this circuitry, the amygdala plays a central role in detecting emotionally salient stimuli in the environment and in guiding behavior in response to affect. The hippocampus is involved in emotional learning and memory. The medial prefrontal cortex (mPFC) is critical for regulating the amygdala and emotional reactivity. Paralleling dynamic changes in emotion processing across childhood and adolescence, this circuitry undergoes protracted development (Bloom et al., Reference Bloom, VanTieghem, Gabard-Durnam, Gee, Flannery, Caldera, Goff, Telzer, Humphreys, Fareri, Shapiro, Algharazi, Bolger, Aly and Tottenham2022; Casey et al., Reference Casey, Heller, Gee and Cohen2019; Gee et al., Reference Gee, Bath, Johnson, Meyer, Murty, van den Bos and Hartley2018; Hare et al., Reference Hare, Tottenham, Galvan, Voss, Glover and Casey2008).
Cross-species evidence shows that caregivers influence the development of corticolimbic circuitry, with an especially prolonged period of influence in humans (Callaghan et al., Reference Callaghan, Sullivan, Howell and Tottenham2014; Tottenham, Reference Tottenham2015). While studies of youth exposed to caregiving-related adversity have contributed some of the strongest evidence of caregiving influences on neurodevelopment (Nelson & Gabard-Durnam, Reference Nelson and Gabard-Durnam2020; Sheridan et al., Reference Sheridan, Fox, Zeanah, McLaughlin and Nelson2012; Tottenham, Reference Tottenham2012), a growing literature has pointed to associations between typical variation in caregiving behaviors and offspring brain development (Farber et al., Reference Farber, Gee and Hariri2022; Tan et al., Reference Tan, Oppenheimer, Ladouceur, Butterfield and Silk2020). Many of these studies have focused on aspects of caregiving related to warmth (versus harshness or hostility) and sensitivity (i.e., the extent to which a caregiver is attuned and responsive to their child). During childhood, caregiver sensitivity is associated with amygdala volume and microstructure of the amygdala and hippocampus (A. Lee et al., Reference Lee, Poh, Wen, Tan, Chong, Tan, Gluckman, Fortier, Rifkin-Graboi and Qiu2019), and negative caregiving behavior is associated with amygdala activation and functional connectivity to affective stimuli (Pozzi et al., Reference Pozzi, Simmons, Bousman, Vijayakumar, Bray, Dandash, Richmond, Schwartz, Seal, Sheeber, Yap, Allen and Whittle2019). In addition, maternal hostility and regulation at age 3 were associated with children’s corticolimbic function at ages 7–8 (Kopala-Sibley et al., Reference Kopala-Sibley, Cyr, Finsaas, Orawe, Huang, Tottenham and Klein2020), suggesting that caregiving in the earliest years of development may prime the development of corticolimbic circuitry. During adolescence, findings suggest sustained impact of caregiving behaviors. For example, parental warmth and support were associated with lower amygdala reactivity to fearful faces among adolescents (Romund et al., Reference Romund, Raufelder, Flemming, Lorenz, Pelz, Gleich, Heinz and Beck2016), and harsher parenting was associated with reduced ventrolateral prefrontal engagement during peer rejection among adolescents at risk for anxiety disorders (Guyer et al., Reference Guyer, Jarcho, Pérez-Edgar, Degnan, Pine, Fox and Nelson2015). Evidence suggests these associations between caregiving and brain function have important implications for mental health. Among adolescents, higher parental warmth was associated with lower symptoms of anxiety and depression 2 years later via effects on subgenual anterior cingulate activation (Butterfield et al., Reference Butterfield, Silk, Lee, Siegle, Dahl, Forbes, Ryan, Hooley and Ladouceur2020). Together, these findings suggest that harsher parenting is associated with weaker prefrontal control in certain contexts requiring regulation (e.g., Guyer et al., Reference Guyer, Jarcho, Pérez-Edgar, Degnan, Pine, Fox and Nelson2015), whereas caregiver warmth and sensitivity are generally associated with lower reactivity in regions such as the amygdala in negatively valenced contexts (e.g., Kopala-Sibley et al., Reference Kopala-Sibley, Cyr, Finsaas, Orawe, Huang, Tottenham and Klein2020; Pozzi et al., Reference Pozzi, Simmons, Bousman, Vijayakumar, Bray, Dandash, Richmond, Schwartz, Seal, Sheeber, Yap, Allen and Whittle2019; Romund et al., Reference Romund, Raufelder, Flemming, Lorenz, Pelz, Gleich, Heinz and Beck2016), as well as lower internalizing symptoms (e.g., Butterfield et al., Reference Butterfield, Silk, Lee, Siegle, Dahl, Forbes, Ryan, Hooley and Ladouceur2020).
Regulatory influences: Caregiver buffering of neural function and behavior
Consistent with the idea that caregivers can promote resilience by influencing the neurobiological processes supporting regulation, evidence suggests that supportive caregiving can buffer the effects of numerous types of adversity on hypothalamic-pituitary-adrenal (HPA) axis function, corticolimbic circuitry, and epigenetic aging (Brody et al., Reference Brody, Yu, Chen, Beach and Miller2016, Reference Brody, Yu, Nusslock, Barton, Miller, Chen, Holmes, McCormick and Sweet2019; Brown et al., Reference Brown, Schlueter, Hurwich-Reiss, Dmitrieva, Miles and Watamura2020; Gunnar & Donzella, Reference Gunnar and Donzella2002; Kahhalé et al., Reference Kahhalé, Barry and Hanson2023; Stevens et al., Reference Stevens, van Rooij, Stenson, Ely, Powers, Clifford, Kim, Hinrichs, Tottenham and Jovanovic2021; Whittle et al., Reference Whittle, Vijayakumar, Simmons, Dennison, Schwartz, Pantelis, Sheeber, Byrne and Allen2017). Paralleling evidence that caregivers play a central role in guiding children’s emotional learning (Tottenham et al., Reference Tottenham, Shapiro, Flannery, Caldera and Sullivan2019; van Rooij et al., Reference van Rooij, Cross, Stevens, Vance, Kim, Bradley, Tottenham and Jovanovic2017) and helping to regulate children’s emotions and stress (Cohodes et al., Reference Cohodes, Chen and Lieberman2017; Cohodes et al., Reference Cohodes, Kribakaran, Odriozola, Bakirci, McCauley, Hodges, Sisk, Zacharek and Gee2021; Compas et al., Reference Compas, Connor-Smith, Saltzman, Thomsen and Wadsworth2001; Eisenberg et al., Reference Eisenberg, Cumberland and Spinrad1998), cross-species research has demonstrated that caregivers serve an external regulatory function as corticolimbic circuitry is developing (Callaghan & Tottenham, Reference Callaghan and Tottenham2016; Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2014; Gee, Reference Gee2016; Gunnar & Donzella, Reference Gunnar and Donzella2002; Hofer, Reference Hofer1994; C. L. McCoy & Masters, Reference McCoy and Masters1985). Consistent with findings in rodents and macaques (Moriceau & Sullivan, Reference Moriceau and Sullivan2006; Sanchez, Reference Sanchez2006), research in humans has shown that caregiver presence can buffer children’s responses to stress by dampening cortisol reactivity (Hostinar et al., Reference Hostinar, Johnson and Gunnar2015) and amygdala reactivity (Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2014). In a study of caregiver buffering at the neural and behavioral levels, children and adolescents performed an emotional go/no-go task of inhibitory control in an affective context twice in the laboratory, once in the presence of their mother and once in the presence of a stranger. During an fMRI scan, participants viewed faces of their mother and of a stranger. Consistent with parental regulation of behavior, children showed better inhibitory control (i.e., fewer false alarms) when seated next to their mother than a stranger in the laboratory. Children showed lower amygdala reactivity when viewing their mother’s face than when viewing a stranger’s face. Moreover, exposure to the mother’s face, relative to the stranger’s face, phasically induced a pattern of stronger inverse mPFC-amygdala functional connectivity that is typically observed at older ages and that has been associated with greater regulation in prior work (e.g., Banks et al., Reference Banks, Eddy, Angstadt, Nathan and Phan2007). In this study, caregiver buffering at the neural level was associated with individual differences in behavior, such that children whose parents buffered more strongly at the neural level exhibited better inhibitory control in their parent’s presence (Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2014). Of note, the effects of caregiver buffering observed in this study were specific to childhood and were not evident for adolescents in this study, which may be indicative of a relatively reduced dependence on external regulation in some affective contexts during adolescence. Together, these findings suggest that modulation of the HPA axis and frontoamygdala circuitry is one primary way that caregivers confer external regulation while regulatory systems are still developing during childhood.
Despite increasing independence from their caregivers as youth mature, caregivers continue to play an important role in scaffolding regulation during adolescence. However, at both behavioral and neural levels, the nature of this role appears to change in a manner consistent with the developing skills and unique needs of adolescents (Telzer et al., Reference Telzer, van Hoorn, Rogers and Do2018). Demonstrating the prevailing role of parents in guiding offspring behavior via external regulation in adolescence—and the potentially increased importance of parents in appetitive social contexts that may induce a propensity for risk taking, a series of studies has shown that the presence of a parent can redirect adolescents toward safer behavior and stronger regulation in rewarding social contexts (Guassi Moreira & Telzer, Reference Guassi Moreira and Telzer2018; Qu et al., Reference Qu, Fuligni, Galvan and Telzer2015; Rogers et al., Reference Rogers, Perino and Telzer2020; Telzer et al., Reference Telzer, Ichien and Qu2015). As one example, compared with younger youth, older youth showed more disinhibition toward appetitive than aversive stimuli in social contexts. However, parental presence buffered this effect, such that there was no age-related difference when the parent was present (Rogers et al., Reference Rogers, Perino and Telzer2020). With increasing age, adolescents exhibited greater mPFC activation and frontoamygdala connectivity in socially appetitive contexts when in their parent’s presence, suggesting a prefrontal mechanism supporting the regulatory effects of caregivers during adolescence. In addition to the buffering effects of caregiver presence, caregivers appear to support adolescents’ emotional well-being by socializing coping behaviors (e.g., A. S. Anderson et al., Reference Anderson, Watson, Reising, Dunbar, Bettis, Gruhn and Compas2021; Liga et al., Reference Liga, Inguglia, Gugliandolo, Ingoglia and Costa2020). Building upon these behavioral findings, a recent study found that parental socialization of coping behaviors modulates adolescent mental health via modulation of neural circuitry implicated in affective regulation. Specifically, parents’ use of reframing and problem-solving statements during a parent–adolescent interaction was associated with adolescents’ insula and perigenual cingulate activation in response to affective stimuli. Among adolescents with anxiety disorders, parents’ socialization of prototypically adaptive coping strategies was associated with lower use of disengaged coping in adolescents’ daily life via these patterns of neural activation (Butterfield et al., Reference Butterfield, Siegle, Lee, Ladouceur, Forbes, Dahl, Ryan, Sheeber and Silk2019). Together, these findings suggest that adolescence may be an especially important time for caregivers’ scaffolding of adaptive coping and safe behavior in the context of social challenges, which commonly arise in more appetitive contexts, during adolescence.
Ontogeny of caregiver buffering and individual differences
Understanding how caregiving cues facilitate regulation—and how these experiences become biologically embedded to influence the development of children’s intrinsic regulatory capacity—can provide insight into the ways that caregivers foster resilience following adversity. We have previously proposed that effective caregiver buffering requires the pairing of predictability and safety in children’s experience of caregiver cues (Gee & Cohodes, Reference Gee and Cohodes2021). Specifically, children’s interactions with caregivers provide opportunities to experience caregiver buffering and to learn about the degree to which their caregiver’s presence is associated with the attenuation of fear (Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2014; Moriceau & Sullivan, Reference Moriceau and Sullivan2006). Through these repeated interactions, consistent—and predictable—experiences of caregiver regulation (e.g., via physical presence and related attenuation of physiological reactivity) (Callaghan & Tottenham, Reference Callaghan and Tottenham2016) reinforce the association between caregiver presence and safety. A growing body of cross-species evidence indicates that the predictability of caregiving signals acts on corticolimbic circuitry (Glynn & Baram, Reference Glynn and Baram2019), with demonstrated effects on mPFC-amygdala connectivity (Granger et al., Reference Granger, Glynn, Sandman, Small, Obenaus, Keator, Baram, Stern, Yassa and Davis2021; Guadagno et al., Reference Guadagno, Kang, Devenyi, Mathieu, Rosa-Neto, Chakravarty and Walker2018) and amygdala reactivity (Malter Cohen et al., Reference Malter Cohen, Jing, Yang, Tottenham, Lee and Casey2013). Across time, repeated co-activation of the amygdala and mPFC via parental presence may contribute to the development of this circuit and internalization of regulatory capacities (Callaghan & Tottenham, Reference Callaghan and Tottenham2016; Gee, Reference Gee2016). Evidence in humans shows that frontoamygdala connectivity to affective stimuli predicts frontoamygdala connectivity at rest 2 years later, suggesting that repeated co-activations during development may shape the more stable architecture of this circuit later in life (Gabard-Durnam et al., Reference Gabard-Durnam, Gee, Goff, Flannery, Telzer, Humphreys, Lumian, Fareri, Caldera and Tottenham2016). Indeed, environmental experiences that co-activate regions within a circuit can shape long-term changes in connectivity during adulthood (Gabard-Durnam et al., Reference Gabard-Durnam, Gee, Goff, Flannery, Telzer, Humphreys, Lumian, Fareri, Caldera and Tottenham2016; Kelly & Castellanos, Reference Kelly and Castellanos2014), which may be especially likely for early caregiver influences given heightened neuroplasticity and neural sensitivity to caregiving experiences early in development. Over time, such neurobiological scaffolding may be a mechanism by which the external regulation provided by caregivers becomes internalized as youth mature and become more independent.
Although group-level effects of caregiver modulation of offspring neural function and regulatory behavior have been identified during childhood and adolescence, there is important variability in these effects across individuals. Consistent with the idea that early caregiver–child attachment lays the foundation for subsequent caregiving influences on children’s emotional functioning (Sroufe, Reference Sroufe2005), individual differences in caregiver buffering have emerged as a function of attachment security in several studies. Specifically, children who reported greater security in their relationship with their caregiver showed greater caregiver-related attenuation of amygdala reactivity (B. Callaghan et al., Reference Callaghan, Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2019; Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2014). In addition, in a study of adolescents, attachment history (i.e., attachment classification assessed during early childhood) moderated the effects of caregiver presence on regulatory behavior and neural functioning in response to affective cues, such that the buffering effect of caregiver presence was stronger among adolescents with a history of insecure attachment (relative to those with a history of secure attachment) (Rogers et al., Reference Rogers, Chen, Kwon, McElwain and Telzer2021). While future work is needed to better understand the relation between attachment and caregiver buffering across a range of contexts and developmental stages, broadly, these findings reinforce that individual youth are differentially sensitive to caregiving experiences (e.g., Schriber & Guyer, Reference Schriber and Guyer2016) and highlight the importance of considering individual differences in the nature of caregiver–child relationships. Namely, children’s individual profiles of caregiving adversity (e.g., frequency and chronicity of disrupted attachment relationships, history of caregiver betrayal) are likely to directly inform individuals’ capacity to optimally benefit from caregivers’ external regulation, which may have important implications for the development of psychopathology following adversity.
Caregiver buffering following adversity
Consistent with the idea that early experiences with caregivers may shape subsequent experiences of social buffering (Gee & Cohodes, Reference Gee and Cohodes2021; Hostinar et al., Reference Hostinar, Sullivan and Gunnar2014), across species, early caregiving adversity is associated with weaker effects of caregiver buffering later in development across species. Even though the evolutionary drive to establish attachment relationships persists even in the context of threatening cues (R. Perry & Sullivan, Reference Perry and Sullivan2014), animal studies demonstrate that caregiving adversity interferes with caregiver buffering. Specifically, pups exposed to maternal maltreatment (e.g., rough handling of pups, stepping on pups) do not show the expected pattern of suppression of fear-related behavior in the presence of their mother during infancy, and, further, did not appear to benefit from maternal buffering to the same degree as their non-maltreatment exposed counterparts during the adolescent period with regard to their fear-related behavior (Opendak et al., Reference Opendak, Robinson-Drummer, Blomkvist, Zanca, Wood, Jacobs, Chan, Tan, Woo, Venkataraman, Kirschner, Lundström, Wilson, Serrano and Sullivan2019; Robinson-Drummer et al., Reference Robinson-Drummer, Opendak, Blomkvist, Chan, Tan, Delmer, Wood, Sloan, Jacobs, Fine, Chopra, Sandler, Kamenetzky and Sullivan2019). Similarly, among non-human primates, infant maltreatment is associated with less effective maternal buffering of cortisol reactivity (Sanchez et al., Reference Sanchez, McCormack and Howell2015). In the context of human development, a recent study examined caregiver buffering of amygdala reactivity among youth who were previously exposed to caregiver deprivation via institutionalized care and later adopted into stable families. Findings suggest that, on average, children exposed to caregiver deprivation early in life do not benefit from caregiver buffering of amygdala reactivity (Callaghan et al., Reference Callaghan, Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2019). However, there is substantial variability in this effect and 40% of youth who previously experienced caregiving-related adversity did show reduced amygdala reactivity to caregiver cues. Paralleling findings related to individual differences in responses to caregiver buffering in typical development (i.e., among youth who did not experience caregiving adversity), greater caregiver–child attachment security was associated with stronger caregiver buffering of amygdala reactivity (Callaghan et al., Reference Callaghan, Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2019). Importantly, youth who appeared to respond to caregiver buffering despite a history of caregiving adversity also had lower levels of anxiety-related symptomatology up to 3 years later, suggesting that caregiver buffering of amygdala reactivity may be a mechanism by which caregivers promote resilience among youth at elevated risk of psychopathology due to their exposure to adversity.
Moreover, these findings highlight malleability in buffering effects following early caregiving disruptions. Despite the absence of consistent safety-related caregiving cues in the first few years of life, children exposed to early caregiver adversity who showed caregiver-related attenuation of amygdala reactivity benefited from having learned to associate their adoptive caregivers with safety during a later developmental stage (B. Callaghan et al., Reference Callaghan, Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2019). Consistent with this idea, evidence from rodent studies shows that exposure to subsequent augmented caregiving following caregiving-related adversity is associated with neurodevelopmental changes that support adaptive responses to stress (e.g., Singh-Taylor et al., Reference Singh-Taylor, Molet, Jiang, Korosi, Bolton, Noam, Simeone, Cope, Chen, Mortazavi and Baram2018). Thus, although optimal patterns of early caregiver inputs may prime corticolimbic circuitry to be more receptive to caregiver modulation later in life, high-quality care following adversity may foster plasticity in youths’ capacity to benefit from subsequent caregiver buffering. Consistent with these ideas, in our conceptual model, caregiving influences can indeed stem from caregivers who have been associated with adversity. In the context of caregiving-related adversity, there is more likely to be disruption in the extent to which a child associates a caregiver with safety and predictability (Gee & Cohodes, Reference Gee and Cohodes2021). Thus, benevolent influences of a caregiver who previously perpetrated adversity or was associated with adversity are more complicated than caregiver influences that have consistently been associated with safety and predictability. However, often with significant support and intervention (Lieberman & Van Horn, Reference Lieberman and Van Horn2008), the potential for buffering and benevolent caregiving experiences still exists.
The role of developmental timing of adversity exposure and sensitive periods in caregiving influences
Dynamic changes in plasticity and neurodevelopment across childhood and adolescence have broad implications for how caregiving experiences shape children’s emotional functioning and foster resilience following adversity. During sensitive periods of heightened plasticity, the brain is more amenable to environmental influences (Knudsen, Reference Knudsen2004; Werker & Hensch, Reference Werker and Hensch2015) and experiences can lead to a series of developmental cascades that can have downstream effects—both positive and negative—on mental health (Davidson & McEwen, Reference Davidson and McEwen2012; Masten & Cicchetti, Reference Masten and Cicchetti2010). Such periods can render children particularly vulnerable to caregiving disruptions, but can also confer unique opportunities for intervention and buffering effects of augmented caregiving (Gee & Casey, Reference Gee and Casey2015).
Cross-species evidence suggests that the period spanning infancy and toddlerhood may represent a sensitive period during which caregiver inputs that are predictable and associated with safety may be particularly important for establishing a foundation for later caregiver modulation of corticolimbic circuitry and emotional functioning (Fig. 2). The absence of stable, nurturing caregiving early in life disrupts corticolimbic development across species. For example, early caregiver deprivation is associated with altered connectivity between the amygdala and mPFC in mice (F. K. Johnson et al., Reference Johnson, Delpech, Thompson, Wei, Hao, Herman, Hyder and Kaffman2018), rats (Yan et al., Reference Yan, Rincón-Cortés, Raineki, Sarro, Colcombe, Guilfoyle, Yang, Gerum, Biswal, Milham, Sullivan and Castellanos2017), non-human primates (B. R. Howell et al., Reference Howell, Ahn, Shi, Godfrey, Hu, Zhu, Styner and Sanchez2019), and humans (Gee et al., Reference Gee, Gabard-Durnam, Flannery, Goff, Humphreys, Telzer, Hare, Bookheimer and Tottenham2013; Herzberg et al., Reference Herzberg, McKenzie, Hodel, Hunt, Mueller, Gunnar and Thomas2021). Disruptions to stable, supportive caregiving have particularly strong influences when they occur early in life, relative to later stages of development (Nelson & Gabard-Durnam, Reference Nelson and Gabard-Durnam2020; Tottenham, Reference Tottenham2012), suggesting that this developmental period may reflect a sensitive period driven by experience-expectant mechanisms. Some of the strongest evidence for an early sensitive period related to species-expected caregiving comes from the Bucharest Early Intervention Project (BEIP), a randomized controlled trial that randomly assigned children in institutionalized care to either be placed in foster care or to remain in institutionalized care (Nelson et al., Reference Nelson, Zeanah, Fox, Marshall, Smyke and Guthrie2007). Findings suggest that youth exposed to caregiver deprivation in the context of institutionalized care show more secure attachment, more normative stress responses, and more normative neurodevelopmental trajectories following placement into a foster care intervention prior to 24 months of age, relative to peers who were placed after 24 months of age (McLaughlin et al., Reference McLaughlin, Fox, Zeanah and Nelson2011, Reference McLaughlin, Sheridan, Tibu, Fox, Zeanah and Nelson2015; Vanderwert et al., Reference Vanderwert, Zeanah, Fox and Nelson2016). While studies of caregiving disruptions in humans involve complex adversities (e.g., parental deprivation, maltreatment) characterized by both the absence of species-expected inputs and the presence of extreme stress (which may, themselves, alter the timing of sensitive periods [see Gabard-Durnam & McLaughlin, Reference Gabard-Durnam and McLaughlin2020 for a review]), this evidence suggests that the first 2 years of life may be a potential sensitive period during which the absence of key aspects of species-expected caregiving inputs—such as the repeated co-occurrence of predictability and safety—may exert a particularly strong effect on neurodevelopment and longer-term emotional functioning.
Emerging evidence suggests that adolescence may represent another developmental window with increased potential for positive influences of supportive caregiving. Adolescence is a unique period for neurodevelopment and socioemotional functioning, with a broad array of challenges and opportunities (Andersen, Reference Andersen2003; Fuhrmann et al., Reference Fuhrmann, Knoll and Blakemore2015; F. S. Lee et al., Reference Lee, Heimer, Giedd, Lein, Šestan, Weinberger and Casey2014; Sisk & Gee, Reference Sisk and Gee2022). Despite exposure to increased stressful life events and the onset of many stress-related psychiatric disorders during adolescence (Kessler et al., Reference Kessler, Berglund, Demler, Jin, Merikangas and Walters2005; McLaughlin et al., Reference McLaughlin, Greif Green, Gruber, Sampson, Zaslavsky and Kessler2012), adolescents may be especially poised to benefit from positive caregiver influences following early-life adversity. As one example, a recent study using longitudinal data from the BEIP identified adolescence as a period of heightened sensitivity to the caregiving environment (Colich et al., Reference Colich, Sheridan, Humphreys, Wade, Tibu, Nelson, Zeanah, Fox and McLaughlin2021). Higher caregiving quality in adolescence was associated with greater reward responsivity and executive functioning, as well as lower internalizing and externalizing problems; further, these associations were strongest at age 16, relative to ages 8 and 12. These findings suggest that positive caregiving experiences during adolescence may be especially helpful to promote resilience among children exposed to earlier adversity and complement recent evidence that stress response systems may undergo a period of increased plasticity during adolescence. Specifically, adolescents who experienced caregiver deprivation early in life but were later adopted into stable families showed evidence of recalibration of the HPA axis with pubertal development (DePasquale et al., Reference DePasquale, Donzella and Gunnar2019, Reference DePasquale, Herzberg and Gunnar2021; Gunnar et al., Reference Gunnar, DePasquale, Reid, Donzella and Miller2019). As such, increased plasticity of the HPA axis during adolescence may promote recalibration to current environmental inputs, such that supportive caregiving environments may have an outsize impact on psychobiological development during this period. Of note, the role of pubertal recalibration on the longer-term development of socioemotional processes is not yet fully understood and recent longitudinal analyses suggest that recalibration may actually be associated with poorer long-term adjustment (N. B. Perry et al., Reference Perry, DePasquale, Donzella and Gunnar2020, Reference Perry, Donzella and Gunnar2022). Future research will be important to further examine the optimal nature of an adolescent environment that facilitates recalibration, as well as its potential neural and behavioral consequences.
In addition to the role of developmental timing itself in the effects of adversity and caregiving experiences (Gee & Casey, Reference Gee and Casey2015; Lupien et al., Reference Lupien, McEwen, Gunnar and Heim2009; McCrory et al., Reference McCrory, De Brito, Kelly, Bird, Sebastian, Mechelli, Samuel and Viding2013; Sabatini et al., Reference Sabatini, Ebert, Lewis, Levitt, Cameron and Mirnics2007; Teicher et al., Reference Teicher, Samson, Anderson and Ohashi2016; Tottenham & Sheridan, Reference Tottenham and Sheridan2009), developmental timing intersects with key features of experience to shape neurodevelopment and emotional functioning. The extent to which a caregiver is involved in children’s experiences of adversity—whether through connection to the adversity itself or through supporting children’s coping in its aftermath—is likely to be especially impactful during developmental periods of heightened sensitivity (Cohodes et al., Reference Cohodes, Kitt, Baskin-Sommers and Gee2021; Gee & Casey, Reference Gee and Casey2015). Caregivers may be involved in adversity exposures in a variety of ways, including via direct involvement (e.g., caregiver perpetration of abuse or neglect) or parent–child dyadic exposure to adversity (e.g., shared exposure to domestic violence). Exposure to adversity that involves deviations from species-expected caregiving (e.g., caregiver perpetration of maltreatment) has the potential to disrupt the caregiver–child attachment relationship and to hinder the efficacy of caregiver buffering following adversity (Lieberman, Reference Lieberman2004). Consistent with this idea, several studies have found that, relative to children exposed to non-caregiver-related adversity, children who experienced caregiver-related adversity showed greater symptomatology, as well as difficulties with affect regulation and interpersonal relationships (Cook et al., Reference Cook, Spinazzola, Ford, Lanktree, Blaustein, Cloitre, DeRosa, Hubbard, Kagan, Liautaud, Mallah, Olafson and van der Kolk2005; D’Andrea et al., Reference D’Andrea, Ford, Stolbach, Spinazzola and Kolk2012). In addition, in this vein, children exposed to adversity characterized by maladaptive family functioning were more likely to develop mental health problems than children exposed to adversities not characterized by maladaptive family functioning (McLaughlin et al., Reference McLaughlin, Green, Gruber, Sampson, Zaslavsky and Kessler2010). These findings have important implications for the ways that caregivers might support children’s emotional functioning following exposure to adversity and highlight the importance of interventions that support families with ongoing threats to caregiving relationships or in which a caregiver’s own traumatic exposure affects their capacity to be involved in children’s emotional functioning in an adaptive way. Given the essential role of attachment in development and emotional functioning (Bowlby, Reference Bowlby1969; Cassidy & Shaver, Reference Cassidy and Shaver2002), such caregiver-involved adversity may have an especially pronounced impact on mental health in childhood, and delineating interactions between the timing of adversity and features such as caregiver involvement may directly inform interventions (Cohodes et al., Reference Cohodes, Kitt, Baskin-Sommers and Gee2021).
Implications for treatment
Here we propose that caregivers’ engagement with children’s emotional development is a primary mechanism by which caregivers promote children’s resilience in the context of adversity. Further, attachment relationships form the basis of the numerous specific ways that caregivers exert this influence across development (Sroufe, Reference Sroufe2005). Given the potential for adversity exposure to negatively impact attachment relationships, exposure to adversity may undermine the very caregiving influences that have the potential to buffer children from the deleterious sequelae of these exposures (Lieberman & Amaya-Jackson, Reference Lieberman and Amaya-Jackson2005). Therefore, bolstering caregiver–child attachment relationships—and, in turn, a caregiver’s ability to support children’s emotion regulation—is a key treatment target for youth exposed to adversity (Dozier et al., Reference Dozier, Roben, Caron, Hoye and Bernard2018; Lieberman et al., Reference Lieberman, Van Horn and Ozer2005). Relational interventions such as Child–Parent Psychotherapy (Lieberman et al., Reference Lieberman, Van horn and Ippen2005), Trauma-Focused Cognitive Behavioral Therapy (Cohen et al., Reference Cohen, Mannarino, Berliner and Deblinger2000; Cohen et al., Reference Cohen, Mannarino and Iyengar2011), the Child and Family Traumatic Stress Intervention (Berkowitz et al., Reference Berkowitz, Stover and Marans2010), Parent–Child Interaction Therapy (Thomas & Zimmer-Gembeck, Reference Thomas and Zimmer-Gembeck2012), and Attachment-Based Family Therapy (Diamond et al., Reference Diamond, Creed, Gillham, Gallop and Hamilton2012) that center dyadic processes between caregivers and children and focus on restoring optimal caregiving inputs for children following adversity (e.g., establishment or reestablishment of safety in the context of family life) are likely to promote children’s ability to benefit from caregiving in the context of trauma (e.g., Lieberman et al., Reference Lieberman, Van horn and Ippen2005; Lieberman & Van Horn, Reference Lieberman and Horn2011). Importantly, the appropriate relational intervention program will ultimately depend on a particular child’s history of adversity exposure—and the past and current family context—and will be influenced by factors such as whether caregivers have engaged in maltreatment or neglect.
Consistent with the increasing emphasis on precision medicine-based intervention for youth and families exposed to adversity (Aschbacher et al., Reference Aschbacher, Cole, Hagan, Rivera, Baccarella, Wolkowitz, Lieberman and Bush2022), delineating how children’s specific profiles of adversity exposure and developmental stage relate to emotional learning and regulation is likely to inform optimized approaches to intervention (Gee et al., Reference Gee, Sisk, Cohodes and Bryce2022) (Fig. 3). For example, interventions can be tailored based on an individual’s profile of exposure to adversity across multiple dimensions (Cohodes et al., Reference Cohodes, Kitt, Baskin-Sommers and Gee2021; Cohodes et al., Reference Cohodes, McCauley, Pierre, Hodges, Haberman, Santiuste, Rogers, Wang, Mandell and Gee2023; Nikolaidis et al., Reference Nikolaidis, Heleniak, Fields, Bloom, VanTieghem, Vannucci, Camacho, Choy, Gibson, Harmon, Hadis, Douglas, Milham and Tottenham2022), based on specific patterns of caregiver–child interactions (Kitt et al., Reference Kitt, Lewis, Galbraith, Abend, Smith, Lebowitz, Pine and Gee2022), or based on specific caregiver-level factors such as parental symptomatology following dyadic exposure to adversity (Hagan et al., Reference Hagan, Browne, Sulik, Ippen, Bush and Lieberman2017). We specifically highlight the importance of considering family-level processes in treatment selection and optimization given the multifaceted influence of caregivers on resilience-related processes reviewed here (Garner et al., Reference Garner, Yogman and Child2021). While variability in numerous factors could characterize an individual’s exposure to adversity and their caregiving experiences, the following dimensions may be especially important for understanding the optimal role of caregivers in promoting youth’s resilience and optimizing interventions to support caregiving influences: (a) adversity: extent to which a caregiver was involved in adversity; extent to which adversity was characterized by threat, deprivation, or unpredictability; developmental timing of the adversity; (b) caregiving: extent to which caregiver is associated with safety or predictability, caregiver warmth, caregiver sensitivity. Notably, the literatures on caregiving-related adversity and associations between caregiving and brain development have focused on a wide array of caregiving-related behaviors (e.g., emotion socialization, assistance with emotion regulation, predictability of caregiving or home routines, caregiver warmth, etc.). The influence of specific caregiving-related behaviors is likely to be child- and context-specific; thus it will be important for clinical assessment to involve delineation of the ways that particular caregiving behaviors are associated with children’s resilience in order to optimize intervention.
Building upon current efforts to chart sensitive periods of affective development and to identify patterns of experience-driven plasticity (L. Gabard-Durnam & McLaughlin, Reference Gabard-Durnam and McLaughlin2020; McLaughlin & Gabard-Durnam, Reference McLaughlin and Gabard-Durnam2022) is likely to enhance intervention approaches (Gee & Casey, Reference Gee and Casey2015) and the potential to optimally support and repair stress-related alterations to neurobiological systems underlying emotion regulation (Sisk & Gee, Reference Sisk and Gee2022). Specifically, caregivers’ role in buffering offspring neural and behavioral regulation changes from childhood to adolescence (Gee et al., Reference Gee, Gabard-Durnam, Telzer, Humphreys, Goff, Shapiro, Flannery, Lumian, Fareri, Caldera and Tottenham2014; Rogers et al., Reference Rogers, Perino and Telzer2020); therefore, there are likely developmental stage-specific changes in the optimal role of caregivers in promoting resilience following adversity, with important implications for developing targeted interventions. For example, consistent with the tasks of development specific to infancy and toddlerhood, evidence suggests that children who experienced adversity in the first 5 years of life benefit from dyadic parent–child interventions focused on scaffolding opportunities to reaffirm caregivers’ associations with safety and predictability, and to support children’s emerging understanding of caregivers’ capacity for repair (Gee & Cohodes, Reference Gee and Cohodes2021; Lieberman et al., Reference Lieberman, Ippen and Van Horn2015). As another relevant example, accumulating evidence suggests opportunities during adolescence for reshaping of biological systems underlying the stress response for youth exposed to early adversity in the context of a transition to enhanced caregiving quality (Colich et al., Reference Colich, Sheridan, Humphreys, Wade, Tibu, Nelson, Zeanah, Fox and McLaughlin2021; DePasquale et al., Reference DePasquale, Donzella and Gunnar2019, Reference DePasquale, Herzberg and Gunnar2021; Gunnar et al., Reference Gunnar, DePasquale, Reid, Donzella and Miller2019). Despite the promise of these findings to inform the selection and timing of specific interventions, the role of pubertal recalibration in longer-term socioemotional functioning is not yet fully understood and recent longitudinal analyses suggest that recalibration may be associated with poorer adjustment in the longer term (N. B. Perry et al., Reference Perry, DePasquale, Donzella and Gunnar2020, Reference Perry, Donzella and Gunnar2022). The consideration of these developmental processes—alongside heterogeneity in individual- and family-level factors related to adversity—may inform when and for whom specific interventions have the potential to be maximally effective for shaping or reshaping caregiving influences on youth resilience (Cohodes et al., Reference Cohodes, Kitt, Baskin-Sommers and Gee2021; Gee et al., Reference Gee, Sisk, Cohodes and Bryce2022; Ghosh Ippen et al., Reference Ghosh Ippen, Harris, Van Horn and Lieberman2011; Sisk & Gee, Reference Sisk and Gee2022).
Finally, evidence suggests that supportive caregiving is a viable treatment target (Chu et al., Reference Chu, Ippen and Lieberman2021), and, further, that the neural mechanisms underlying caregiving influences on emotional development in the context of adversity can indeed be modified through psychotherapeutic intervention. As one example, a randomized controlled trial of a supportive parenting intervention for families living in poverty found that family participation in the Strong African American Families (SAAF) Program moderated the association between length of exposure to conditions of poverty and amygdala and hippocampal volumes among young adults. Specifically, whereas longer exposure to poverty during adolescence was associated with amygdala and hippocampal volume reduction among young adults whose families participated in the control condition (i.e., provision of informational brochures), this association was not detected among young adults whose families participated in SAAF (Brody et al., Reference Brody, Gray, Yu, Barton, Beach, Galván, MacKillop, Windle, Chen and Miller2017). These findings suggest that supportive caregiving may buffer the risk of developing psychopathology in the context of adversity exposure (in this case, exposure to poverty), specifically via modulation of corticolimbic circuitry. Similarly, a recent study examined neurobiological changes associated with an early attachment intervention (Attachment and Biobehavioral Catch-Up (ABC) Dozier & Bernard, Reference Dozier and Bernard2019) for children exposed to caregiving-related adversity early in life. Children whose families engaged in ABC (relative to the control condition) showed greater activation of neural regions implicated in social cognition (e.g., hippocampus) to parental cues; further, the degree of parental cue-related activation was associated with more adaptive psychosocial functioning (Valadez et al., Reference Valadez, Tottenham, Tabachnick and Dozier2020). Taken together, these studies suggest that corticolimbic circuitry can be effectively modified in the context of psychosocial intervention focused on caregiving, and that targeted intervention has the potential to promote resilience following adversity by bolstering optimal caregiver influences on the developing brain and behavior. Building upon this promising line of work, delineating how psychosocial interventions may impact the neural bases of caregiver modulation of affective functioning across development will continue to shed light on ideal interventions for youth exposed to adversity. For example, identifying evidence-based interventions that facilitate the recovery of caregivers’ capacity to provide optimal external regulation for youth following missed opportunities for provision of predictable, safe caregiver cues during early sensitive periods, or how dyadic or family-based interventions may exert distinct neurodevelopmental effects relative to individual treatments, will further inform efforts to optimize treatments for youth with adversity-related psychopathology (Gee & Cohodes, Reference Gee and Cohodes2021).
Implications for policy
Developmental science has a notable history of influencing policy and fostering structural changes to better support youth and families. Findings from the BEIP (Nelson et al., Reference Nelson, Zeanah, Fox, Marshall, Smyke and Guthrie2007) that demonstrated the consequences of parental deprivation and the importance of early intervention influenced societal shifts away from institutionalized care. Scientific knowledge of brain development and adolescent behavior has influenced numerous cases in the juvenile justice system (Casey et al., Reference Casey, Taylor-Thompson, Rubien-Thomas, Robbins and Baskin-Sommers2020; A. O. Cohen & Casey, Reference Cohen and Casey2014; Steinberg, Reference Steinberg2017). Research on child development has been central to policymaking related to poverty reduction (Noble et al., Reference Noble, Magnuson, Gennetian, Duncan, Yoshikawa, Fox and Halpern-Meekin2021) and paid family leave (Brito et al., Reference Brito, Werchan, Brandes-Aitken, Yoshikawa, Greaves and Zhang2022).
Building directly on the research discussed here, theoretical and empirical advances in understanding the mechanisms by which caregivers promote resilience among youth exposed to adversity can inform public policy and public health-related efforts that prioritize the well-being of youth and families. Research reviewed thus far highlights the major impact of caregiving-related disruptions on child mental health due to the fact that, intrinsic to this experience, children can be deprived of a primary mechanism of buffering and support. Relatedly, this empirical literature highlights the immense burden of repair when caregiving relationships are severed in contexts such as forced family separation, parental incarceration, or humanitarian crises like war or political violence. Here we outline specific recommendations for policymakers based on current understanding of the ways in which caregivers promote resilience following youth exposure to adversity.
First, the establishment and preservation of attachment relationships is essential to children’s well-being and should be prioritized. Given the profound and lasting impact that caregiving-related adversity can have on the developing brain and behavior—and the central role of caregivers in buffering children from the deleterious mental health impacts of exposure to adversity—policy should focus on supporting caregivers and preventing ruptures to children’s attachment relationships. Second, while children can show remarkable capacity for resilience following adversity, policy must ensure that the burden of coping with adversity does not fall on individual youth and their families, particularly given disproportionate effects of adversity exposure and barriers to mental healthcare for families of lower-income and minoritized racial and ethnic backgrounds (R. E. Anderson et al., Reference Anderson, Jones, Saleem, Metzger, Anyiwo, Nisbeth, Bess, Resnicow and Stevenson2021; Condon et al., Reference Condon, Dettmer, Gee, Hagan, Lee, Mayes, Stover and Tseng2020; Shonkoff et al., Reference Shonkoff, Slopen and Williams2021). Rather, changes should be enacted at the level of society and systems to maximally support children and their families. Indeed, consistent with the idea that resilience depends on multilevel interactions between multiple systems in society (Masten et al., Reference Masten, Lucke, Nelson and Stallworthy2021), evidence demonstrates that intervening at the family, community, or broader societal level is often most effective for promoting favorable outcomes following adversity (Feder et al., Reference Feder, Torres, Southwick and Charney2019; Gee, Reference Gee2021b; Sapienza & Masten, Reference Sapienza and Masten2011). Third, systems-level change should be enacted to eliminate systemic infliction of trauma on youth and families (Gee, Reference Gee2022; Kribakaran et al., Reference Kribakaran, Cohodes and Gee2023). While interventions can mitigate harm, addressing the broader societal forces that give rise to trauma is essential to prevention.
As an example of the policy-related implications of empirical research documenting the impacts of caregiving-related adversity, evidence of the consequences of caregiver–child separation and the essential role of caregivers in buffering children from the negative effects of adversity (Cohodes et al., Reference Cohodes, Kribakaran, Odriozola, Bakirci, McCauley, Hodges, Sisk, Zacharek and Gee2021; Sidamon-Eristoff et al., Reference Sidamon-Eristoff, Cohodes, Gee and Peña2022) directly informed immigration policy related to the detention and forced separation of migrant families at the United States-Mexico border resulting from the United States government’s “Zero Tolerance Policy” (Gee & Cohodes, Reference Gee and Cohodes2019; Gee, Reference Gee2021b), as well as the ruling that the U.S. government must provide access to mental health care for all separated families (Jordan, Reference Jordan2019). Despite reports of harm (Brabeck et al., Reference Brabeck, Lykes and Hunter2014; Hampton et al., Reference Hampton, Raker, Habbach, Deda, Heisler and Mishori2021; MacLean et al., Reference MacLean, Agyeman, Walther, Singer, Baranowski and Katz2019; Sidamon-Eristoff et al., Reference Sidamon-Eristoff, Cohodes, Gee and Peña2022) and calls for structural changes to prevent the infliction of trauma against migrant children in the United States (Cohodes et al., Reference Cohodes, Kribakaran and Gee2020; Kribakaran & Gee, Reference Kribakaran and Gee2020; Kribakaran et al., Reference Kribakaran, Cohodes and Gee2023; Pompa, Reference Pompa2019), migrant children and families continue to face separation, detention, exploitation, and deportation at alarming rates in the United States (Montoya-Galvez, Reference Montoya-Galvez2022).
Developmental scientists have a unique and important role to play in informing broader discussions in society about adversity and youth well-being (Gee, Reference Gee2022). Researchers can contribute to these ongoing discussions and policymaking by conducting rigorous science on childhood adversity, including on the central role of caregivers and families in promoting resilience, by sharing their findings in meaningful ways with broad audiences that go beyond the academic realm. In this work it is essential that our field works to center the voices of youth and families affected by adversity and embraces community-engaged research approaches that directly involve affected youth and their caregivers throughout the research process (Collins et al., Reference Collins, Clifasefi, Stanton, Straits, Gil-Kashiwabara, Rodriguez Espinosa, Nicasio, Andrasik, Wallerstein, Hawes, Miller, Nelson, Orfaly and Duran2018; DePrince et al., Reference DePrince, Alexander, Cook and Gudiño2022; Payán et al., Reference Payán, Zawadzki and Song2022). Moreover, scholars in many other fields are conducting critical and complementary work; informing policy that prioritizes youth mental health will require interdisciplinary collaborations and partnerships.
Advances in this science, with the eventual goal of translating findings into clinical practice and informing policy, will require continuous refinement of conceptual models of early adversity to reflect the broader socioecological contexts in which children develop (Cicchetti & Lynch, Reference Cicchetti and Lynch1993; Hyde et al., Reference Hyde, Gard, Tomlinson, Burt, Mitchell and Monk2020; D. C. McCoy, Reference McCoy2013). Moreover, understanding resilience and trajectories of mental health in the context of early adversity necessitates consideration of distinct ways of experiencing and understanding these adversities (Biel & Coates, Reference Biel and Coates2021; Danese & Widom, Reference Danese and Widom2020; Pollak & Smith, Reference Pollak and Smith2021), as well as an emphasis on eradicating harmful societal forces such as structural racism that perpetually contribute to inequities in adversity exposure and mental health (Anglin et al., Reference Anglin, Ereshefsky, Klaunig, Bridgwater, Niendam, Ellman, DeVylder, Thayer, Bolden, Musket, Grattan, Lincoln, Schiffman, Lipner, Bachman, Corcoran, Mota and van der Ven2021; Bailey et al., Reference Bailey, Krieger, Agénor, Graves, Linos and Bassett2017; G. C. Gee & Ford, Reference Gee and Ford2011; Wildeman & Wang, Reference Wildeman and Wang2017). Lastly, while adversity-related changes in neurobiology or behavior have often been framed as detrimental, such changes may be adaptive in the context of harsh or unpredictable environments (B. J. Ellis et al., Reference Ellis, Bianchi, Griskevicius and Frankenhuis2017; Frankenhuis et al., Reference Frankenhuis, Young and Ellis2020). Efforts to critically evaluate how we conceptualize adversity and effects on brain and behavioral development could both stimulate important scientific discoveries as well as shift the often dominant deficit-based narrative that can contribute to stigma of youth exposed to adversity (Gee, Reference Gee2021a; Hanson & Nacewicz, Reference Hanson and Nacewicz2021; Simmons et al., Reference Simmons, Conley, Gee, Baskin-Sommers, Barch, Hoffman, Huber, Iacono, Nagel, Palmer, Sheth, Sowell, Thompson and Casey2021). In conclusion, as developmental scientists, we have a collective responsibility to harness our knowledge of brain and behavioral development to improve the lives of youth—to affect systems-level change, to center the voices of youth, and, ultimately, to promote resilience among children and families.
Acknowledgments
The authors acknowledge and thank Nessa Bryce with Beyond Bounds Creative for the illustration in Figure 3 that depicts key concepts in this article.
Author contribution
Dylan Gee and Emily Cohodes contributed equally to this work.
Funding statement
This work was supported by the National Science Foundation (NSF) CAREER Award (BCS-2145372), National Institutes of Health (NIH) Director’s Early Independence Award (DP5OD021370), Brain and Behavior Research Foundation (National Alliance for Research on Schizophrenia and Depression; NARSAD) Young Investigator Award, Jacobs Foundation Early Career Research Fellowship, and the Society for Clinical Child and Adolescent Psychology (SCCAP; Division 53 of the American Psychological Association [APA]) Richard "Dick" Abidin Early Career Award and Grant to DGG; and an NSF Graduate Research Fellowship Program award (NSF DGE-1752134), the SCCAP (Division 53 of the APA) Donald Routh Dissertation Grant, the American Psychological Foundation Elizabeth Munsterberg Koppitz Child Psychology Graduate Fellowship, a Dissertation Funding Award from the Society for Research in Child Development, a Dissertation Research Award from the APA, an American Dissertation Fellowship from the American Association of University Women (AAUW), and a Scholar Award granted by the International Chapter of the Philanthropic Educational Organization (P.E.O. Foundation) to EMC. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH, NSF, or any other funding source.
Competing interests
None.