We investigated the influences of multiple types of ELS representing day-to-day detriments in the early care-taking environment – maternal depression, paternal depression, and family expressed anger – on later HPA functioning and its co-variation with mental health symptoms across a six-year period from childhood into adolescence. Consistent with an allostasis framework, which emphasizes the establishment of stable HPA functioning and the maintenance of that stability through change, we distinguished the trait-like component of HPA functioning from the epoch-specific HPA component which co-varies with episodic challenges – in this case, periodic increases in children’s mental health symptoms. Overall, results supported our hypotheses that ELS influences trait-like cortisol and its development as well as the covariation of epoch-specific cortisol with children’s concurrent mental health symptoms. Consistent with previous findings (Gunnar & Quevedo, 2007
; Knutsson et al., 1997
), children exposed to typical levels of ELS showed moderately high trait-like morning cortisol with moderately steep slopes across the day, and modest developmental change from age 9 to 15. These children similarly showed very modest swings in HPA activity around their trait-like basal functioning concurrent with episodic increases in mental health symptom severity. In comparison, children exposed to higher levels any of the three types of ELS evidenced alterations (varying in nature according to the type of ELS) in trait-like morning cortisol and diurnal rhythm, and greater developmental alterations from ages 9 to 15 years. Further, they evidenced substantially wider swings in epoch-specific HPA activity around their basal functioning concurrent with increases or decreases in mental health symptom severity across the four assessment periods.
Our investigation extends previous research demonstrating that ELS has profound effects on children’s HPA axis (reviewed in Gunnar & Vasquez, 2006
; Trickett et al., 2011
) by taking a longer-term prospective approach and distinguishing alterations in the trait-like component of HPA activity associated with basal functioning and its development from alterations related to the component that regulates responses to challenges. As part of the allostatic process (McEwen, 1998
), the HPA axis operates at an optimal level with efficient recovery from challenges, as illustrated here by the patterns of HPA functioning shown by children exposed to typical levels of ELS. However, patterns shown by children exposed to higher levels of ELS result in HPA alterations (either heightened or blunted) which are (a) sustained over time as trait-like levels and rhythms, and (b) show wider swings above and below the individual’s trait-like basal level. The additional energy required to regulate and counter-regulate these sustained alterations in trait-like HPA functioning as well as the repeated alterations associated with the episodic challenge of increased mental health symptoms may contribute, both separately and jointly, to the “wear and tear” on the body, eventually culminating as allostatic load (Lupien et al., 2006
The results of this investigation highlight the cumulative effects of multiple types of ELS on HPA functioning and development across the transition from childhood into adolescence. We found that cumulative exposure to early maternal depression and family expressed anger is particularly influential in defining children’s trait-like basal HPA functioning. Compared to children exposed to typical levels of these two types of ELS, children exposed to high levels of only one – either maternal depression or family expressed anger – evidenced lower trait-like morning cortisol and steeper slopes at age 9, with increases in morning levels over time such that by age 15, they evidenced comparable morning levels with lower levels across the remainder of the day. In contrast, children exposed to both types of ELS evidenced the highest morning cortisol and the flattest slopes at age 9, with decreases in morning levels and a continued flattening of the slope such that by age 15, they showed a pattern of increasing dysregulation of trait-like HPA functioning characterized by a very flat daytime rhythm (i.e., comparable morning levels with a lack of the typical decline across the day). The sustained HPA activation across the day shown by children exposed to multiple types of ELS is consistent with the pattern found in other studies of cumulative stress (Evans, 2003
; Flinn & England, 1995
). In addition, the longitudinal findings extend this work to suggest that, as part of an allostatic process, the “wear and tear” associated with sustained HPA activation may result over time in a down-regulation of HPA functioning (Miller et al., 2007
). Because we investigated this allostatic process only into early adolescence, it is not clear if the trajectory of down-regulation continues into adulthood. However, the findings suggest that the pattern of hypercortisolism often found in studies of maltreated children compared with the pattern of hypocortisolism often found in adults exposed to early maltreatment (Miller et al., 2007
) may reflect, in part, a continuation of the developmental process identified in this study.
The present results also contribute to our understanding of the roles of ELS in defining the later co-variation of children’s HPA functioning with mental health symptoms. Across all children, there was little evidence that HPA functioning was coupled with mental health symptoms. However, in addition to the cumulative effects of exposure to early maternal depression and family expressed anger on trait-like HPA functioning, children exposed to both types of ELS showed a further blunting of HPA activity when faced with the episodic challenge of increased mental health symptoms. In addition, we found domain-specific effects of each type of ELS. Children exposed only to early maternal depression showed an up-regulation in HPA activity with concurrent increases in symptom severity and a down-regulation with concurrent decreases in symptom severity. They also showed the widest swings in HPA activity (especially morning cortisol levels) around their basal functioning concurrent with increases and decreases in symptom severity. In contrast, children exposed only to family expressed anger showed a down-regulation in HPA activity with concurrent increases in symptom severity and an up-regulation with concurrent decreases in symptom severity. Other analyses showed that children exposed only to early paternal depression showed the same pattern of down-regulation in HPA activity with increases in symptom severity as that shown by children exposed to family expressed anger. Similar to other stress- or health-related outcomes (Koob & Le Moal, 2008a
; Weems & Carrion, 2009
), increases in mental health symptoms may create an allostatic state requiring the counter-regulatory opponent process (i.e., swings) of the HPA axis to aid in reestablishing functioning at basal levels. Although speculative, it is possible that the allostatic state may, over time, reset physiological set-points if mental health problems are persistent or recurrent (Koob & Le Moal, 2001
Our findings extend previous research which examines children’s current psychiatric status as a moderator of the association of ELS with alterations in HPA functioning (Ashman et al., 2002
; Cicchetti et al., 2010
; Tarullo & Gunnar, 2006
) in two major ways. First, the findings document that HPA activity and mental health symptoms co-vary over time, reframing the question to consider ELS as the moderator of those patterns of co-variation, or co-regulation. The expression of mental health symptoms may bring an additional stressor to the system (Ruttle et al., 2011
). It is also likely that cortisol and mental health symptoms work in a bi-directional manner, with each functioning in relation to the other, and possibly exacerbating the other. Second, different types of ELS have unique effects on the co-variation of HPA functioning with mental health symptoms. It is notable that there are domain-specific effects only on the covariation of HPA functioning with mental health symptoms, and not on trait-like HPA functioning. This suggests that very early in life, prior to the development of children’s cognitive and emotion regulation strategies, it is the accumulation or severity of ELS which most prominently influences the establishment of trait-like HPA functioning. However, as children grow older, they develop cognitive and emotion regulation strategies associated with exposure to each type of ELS (Cummings & Davies, 2002
; Goodman & Gotlib, 1999
) and, with repeated exposure, may establish preferential patterns of cognitions and emotions which might underlie the differential calibrations of the HPA axis we see when children are faced with the episodic challenge of increased mental health symptoms.
The patterns of differential calibration of the HPA axis to concurrent mental health symptoms found in this investigation are consistent with previous theory and research on the cognitions and emotions, as well as HPA activity, associated with exposure to maternal depression vs. family expressed anger. The wide swings in HPA activity in association with increases in symptom severity that were shown by children exposed to early maternal depression may reflect the potency of maternal care in the early care-taking environment. According to parental investment theory (Bjorklund & Kipp, 1996
), it is evolutionarily adaptive for a child to be emotionally, physiologically, and behaviorally attuned to the mother. This bond begins physically during pregnancy and through the infancy period (Uvnäs-Moberg, Arn, & Magnusson, 2005
) and continues throughout early development as children calibrate their development to the mother’s emotional and social cues. The up-regulation of HPA activity shown by children of depressed mothers when faced with increased symptom severity is consistent with a substantial literature demonstrating increased HPA responsivity in animals as well as human children exposed to deficits in early maternal care-taking (Gunnar & Quevedo, 2007
; Meaney & Szyf, 2005
; Sanchez, 2006
). These effects are mediated by deficits in mother-child interactions and consequent insecure attachments. When mothers are depressed, they exhibit deficits in communication, sensitivity, and attunement (Hwa-Froelich, Cook, & Flick, 2008
; Murray, Fiori-Cowley, Hooper, & Cooper, 1996
; Trampolini, Ungerer, & McMahon, 2008
) which impair the mother-child attachment relationship and negatively influence the child’s cognitive representations of the self and parents (Toth et al., 2009
). Less secure attachments to caregivers and more negative cognitive representations of self and others are associated with the development of less successful emotional- and self-regulatory strategies across childhood (Calkins & Hill, 2007
; Crugnola et al., 2011
; Kochanska, Philibert, & Barry, 2009
) that, in turn, impact the way in which physiological processes are regulated (Fox & Calkins, 2003
). In contrast, the down-regulation of HPA activity shown by children exposed to family expressed anger when they confront episodic increases in mental health symptom severity is consistent with studies showing that perceptions of uncontrollability are associated with lower morning cortisol, and perceptions of physical threat are associated with flatter cortisol slopes across the day (Miller et al., 2007
). Parental anger and conflict has been associated with children’s cognitive perceptions of threat and self-blame (Grych, Fincham, Jouriles, & McDonald, 2000
), perceptions moderated by levels of family cohesiveness (Lindahl & Malik, 2011
). Further, children exposed to contrived laboratory adult conflicts typically recognize and experience greater anger, sadness, and fear when faced with escalating conflict or conflicts about children (Koss et al., 2011
; Pollak, Messner, Kistler, & Cohn, 2009
), situations likely to be perceived as less controllable by the child.
Notably, our findings suggest that exposure to maternal vs. paternal depression represent very different experiences for the child’s psychobiology, possibly because paternal depression is more phenotypically similar to family expressed anger than to maternal depression. While females tend to display the more “classic” symptoms of depression including depressed mood, feelings of worthlessness, and social withdrawal, males with depression typically display higher levels of emotional restriction, aggression and irritability (Brownhill, Wilhelm, Barclay, & Schmied, 2005
; Winkler, Pjrek, & Kasper, 2005
). Given that children may experience the phenomenon of paternal depression in terms of increased levels of threat, children exposed to paternal depression may evidence patterns of HPA–mental health covariation similar to those displayed by children exposed to family expressed anger.
When interpreted within an allostasis framework, the results highlight the trade-offs of adaptive processes that permit an individual to meet the demands of their environment. Recent models of biological sensitivity to context (BSC; Boyce & Ellis, 2005
; Ellis, Essex, & Boyce, 2005
) and its extension to adaptive calibration (ACM; Del Giudice, Ellis, & Shirtcliff, 2011
) postulate that neurological and neuroendocrine systems reorganize and adapt to contextual and physiological perturbations. However, when individuals must adapt to a stressful environment, the alterations in HPA activity can incur a cost, promoting a degeneration of functioning and a cascade of change leading to differential developmental trajectories as maturation occurs (Cicchetti & Curtis, 2006
According to the ACM (Del Giudice et al., 2011
), there are profiles of children (along a continuum) defined by the level of their biological sensitivity to context. The first profile describes children who are biologically sensitive (high BSC) and thus, have an enhanced ability to encode and attend to salient social information. In a low stress environment, they are largely protected from physiological costs of such sensitivity and incur many benefits of being calibrated, or open, to positive social and emotional cues (e.g., empathy and prosocial behavior; Shirtcliff et al., 2009
). Our prior work distinguished large numbers of such sensitive youth within the WSFW (Ellis et al., 2005
); and in the present investigation, the HPA functioning of children exposed to typical levels of ELS is suggestive of this profile. Their moderate trait-like basal levels and diurnal rhythms, and moderate developmental trajectory suggest that their HPA axis maintained flexibility to change rhythmically across and day and to develop slowly across adolescence. The maintenance of flexibility, variability, and rhythmicity in HPA functioning are important healthy allostatic components (McEwen & Wingfield, 2003
). Further, when the challenge of mental health symptoms arise, sensitive children efficiently return to basal levels likely because they are physiologically open to the protective resources in their environment and use these environmental resources to their benefit to overcome mental health symptoms.
The second profile describes children who are exposed to moderate stress – here, only to maternal depression or family expressed anger – who adapt by developing “buffered” trait-like HPA functioning (low BSC). This permits them to be less attentive or focused on their environment, thereby minimizing costs associated with moderate chronic stress beginning very early in life. Children exposed to a single type of ELS demonstrated somewhat lower trait-like cortisol levels with moderately steep diurnal rhythms; across development, cortisol levels became somewhat higher but remained lower across most of the day. The most striking finding was that the coupling of HPA functioning with mental health symptoms was much tighter for these children, especially those exposed only to early maternal depression, and the direction of co-variation was dependent on the type and combination of ELS. This suggests that while children exposed to moderate ELS may develop a “buffered” pattern of trait-like HPA functioning for dealing with chronic stressors, they remain very responsive at least to the episodic challenge of increased mental health symptom severity. Because previous studies have not distinguished the trait-like component of HPA functioning from the epoch-specific component in a long-term prospective design, the meaning of these findings is unclear. It may be that because mental health symptoms reflect, in part, an individual’s cognitive and emotional biases developed earlier in life, the tight and domain-specific patterns of co-variation of symptoms and HPA function reflects differences in exposure to maternal depression vs. family expressed anger, as discussed above. It is notable, however, that despite the apparent allostatic state of the HPA axis during times of increased mental health symptoms, the HPA axis of youth experiencing a single type of ELS appears to be able to maintain diurnal rhythmicity and flexibility to change across development and manage mental health symptoms. When necessary, buffered youth have the physiological resources to cope with challenges.
The third profile appears physiologically similar to the “sensitive” profile, but the costs of maintaining a high BSC are keenly apparent when these children live in a high stress environment – here, both types of ELS. It is adaptive for children exposed to higher levels of stress to be vigilant and sensitive to contextual cues. High trait-like basal cortisol, which we observed, enhances attention to dangerous or unpredictable stimuli, with some physiological trade-offs. Most striking, however, our results show that children exposed to multiple forms of ELS evidenced flattened diurnal rhythms as early as age 9, and their diurnal rhythm became progressively flatter across development, and flatter still when mental health symptoms increased. These results suggest that the high sensitivity to environmental cues in high ELS children might increase their stress vulnerability primarily by dysregulating the diurnal rhythm. Flexibility and rhythmicity are important tenants of allostatic processes (McEwen, 1998
). Cortisol’s diurnal rhythm captures the confluence of intrinsic, biological forces with extrinsic, environmental forces working in concert within an individual on a daily cycle. Individuals exposed to multiple forms of ELS may evidence flattened diurnal rhythms because they are struggling to match their intrinsic physiological set-points with their contextual demands (Skinner, Shirtcliff, Haggerty, Coe, & Catalano, in press
). This mismatch of intrinsic and extrinsic forces occurs on a daily cycle, and appears to steadily worsen with time – both over the course of development and during times of increased mental health symptom expression. Thus, prolonged exposure to the cumulative effects of maternal depression and family expressed anger, and the addition of later mental health challenges, likely exerts “wear and tear” on the system, resulting in a down-regulation of HPA functioning over time (Ruttle et al., 2011
; Weems & Carrion, 2007
; Weems & Carrion, 2009
). For high BSC youth from a stressful environment, the cost of vigilance may culminate in a loss of both flexibility and rhythmicity. By exploring the effect of ELS degree and type on HPA functioning and the coupling of HPA functioning with mental health symptoms, we have made strides toward elucidating the unique processes by which typical functioning becomes atypical.
These findings must be considered in light of several potential limitations to inform future research. First, the possibility of a sampling bias within this population, and the non-representativeness of this sample of the larger U.S. population, must be kept in mind, especially regarding the range of ELS. This sample represents largely middle class, white, and, at least at the outset, intact families in a Midwestern state. However, we emphasize that our findings regarding the importance of considering multiple types of ELS and children’s concurrent psychiatric status support recent work with maltreated children (e.g., Cicchetti et al., 2010
), and extend it downward to more normative variations in ELS, which is an important tenet of developmental psychopathology. The study of typical and atypical development are mutually informative (Cicchetti, 1990
; Cicchetti & Sroufe, 2000
). Conceptually integrating this investigation with the ongoing research of children exposed to early maltreatment has the potential to advance our understanding of a wide range of processes in child development.
Second, while this study examined multiple types of ELS, there are many other types of stressors in the lives of young children which should be considered in future studies. Consistent with a multilevel approach (Cicchetti & Curtis, 2007
; Cicchetti & Rogosch, 2007
), it is particularly important to consider stressors at other levels of analysis. For example, the effects on children’s HPA functioning of the three types of ELS investigated in this study likely operate through deficits in the more intimate qualities of the parent-child relationship and associated attachments (Gunnar & Vasquez, 2006
). At another level, children experience stresses associated with the SES of the family into which they were born. Previous studies have demonstrated that, although SES is associated with maternal depression and family expressed anger, each of these levels of stressors exert independent effects on children’s HPA functioning (Davies et al., 2009
; Essex, Klein, et al., 2002
; Lupien, King, Meaney, & McEwen, 2001
). To more fully understand the allostatic process, it is important for future studies to incorporate stressors at multiple levels into longitudinal models of HPA functioning that distinguishes unique and joint effects of ELS on HPA axis development from responsivity to the challenges of life.
Third, although this investigation took a multi-level approach, we considered only the HPA axis as one of the several inter-related primary mediators of the allostatic process (Lupien et al., 2006
; McEwen, 1998
). Because of the near impossibility of inferring causation within complex developmental systems, it is important to investigate multiple variables and multiple levels of variables simultaneously (Cicchetti & Blender, 2004
; Cicchetti & Toth, 2009
). Future work should expand the multilevel approach employed in the present investigation to consider the complex interplay of multiple physiological systems (Hastings et al., in press
), as well as genetic and epigenetic effects (Gillespie, Phifer, Bradley, & Ressler, 2009
; McCrory et al., 2010
), aware that specific stressors may not affect all stress-related systems equally or in the same general direction or at the same time.
Our findings suggest several important implications for children exposed to different types of day-to-day detriments in the early caretaking environment, especially when facing the challenges associated with increases in mental health problems. Clearly, when exposure to ELS begins at birth (if not earlier) and is chronic throughout early childhood (and possibly beyond), it has substantial and long-term effects on children’s HPA functioning, suggesting the importance of very early preventive/intervention strategies. In addition, the broad effects of cumulative ELS, especially exposure to early maternal depression and family expressed anger, suggest that multilevel preventive/intervention strategies aimed at reducing maternal depression and promoting more positive family dynamics may be most effective. Given the centrality of early maternal caretaking, the findings also emphasize the importance of supporting mothers during this critical time in children’s development. Perhaps most important, by investigating the association of children’s HPA functioning with mental health symptoms as an allostatic process, the findings highlight that (a) allostatic states often emerge when children are experiencing increases in symptom severity; (b) the direction of the HPA axis alteration varies according to the child’s history of ELS; and (c) children exposed to ELS are most vulnerable to alterations in HPA functioning with increases in mental health symptom severity. Together, these findings make a compelling argument that any strategy aimed at intervening in the allostatic process to reduce the development of allostatic load during childhood and adolescence should consider these issues, and especially the heightened vulnerability of children exposed to ELS when they are experiencing increases in mental health symptoms.