Elsevier

Psychoneuroendocrinology

Volume 27, Issues 1–2, January–February 2002, Pages 199-220
Psychoneuroendocrinology

Social regulation of the cortisol levels in early human development

https://doi.org/10.1016/S0306-4530(01)00045-2Get rights and content

Abstract

Other papers in this special edition provide evidence to implicate activity of the limbic hypothalamic–pituitary–adrenocortical (L–HPA) system in the etiology of drug and alcohol abuse. Furthermore, studies in rodents and primates suggest that responsivity and regulation of this system later in life may be shaped by social experiences during early development. Cortisol is the major hormonal product of the L–HPA system in humans. Although it provides only a partial understanding of the activity of this neuroendocrine axis, its regulation may bear importantly on human growth and development. We review developmental studies of cortisol and behavior in human children, birth to approximately 5 years of age. We describe the development of social buffering of cortisol responses that produces a functional analogue of the rodent stress hyporesponsive period by the time children are about 12 months of age. We further describe the sensitivity of cortisol activity to variations in care quality among infants and toddlers, along with evidence that children with negative emotional temperaments may be most likely to exhibit elevations in cortisol under conditions of less than optimal care. Finally, the few studies of cortisol activity under conditions of neglectful and abusive care of young children are considered, noting that these often have yielded evidence of reduced rather than increased cortisol levels.

Introduction

Activity of the limbic hypothalamic–pituitary–adrenocortical (L–HPA) system has been implicated in the etiology of drug and alcohol abuse. Furthermore, studies in rodents and primates suggest that responsivity and regulation of this system later in life may be shaped by social experiences during early development (Levine, 1994, Suomi, 1991). Caregivers play important roles in regulating activity of the L–HPA system during development. In rodents, licking and grooming by the dam and the delivery of milk into the gut maintain the adrenal hyporesponsive period, a period between postnatal days 4 and 14 when it is difficult, although not impossible, to elevate glucocorticoid levels (Suchecki et al., 1993). In non-human primates, the presence of the mother serves to buffer activity of the L–HPA axis, allowing the infant to express distress behaviorally in ways that help to elicit maternal care without producing concomitant elevations in cortisol (Bayart et al., 1990). In humans, recent theoretical reviews propose that adverse experiences early in life predispose individuals to affective pathology in part through affecting activity of the L–HPA system (Graham et al., 1999, Heim et al., 1997). These reviews have cited a number of retrospective studies suggesting that adults who suffered emotional loss (e.g., loss of a parent), maladaptive relationships with attachment figures, or maltreatment during childhood exhibit heightened levels of corticotropin-releasing hormone (CRH) and/or evidence of dysregulation of the L–HPA axis. Little attention has been paid in these reviews to the human developmental literature on the social regulation of cortisol production by the L–HPA system. This literature will be reviewed briefly here. Our focus will be on postnatal studies, although it is recognized that the prenatal period may be important for the development of reactivity and regulation of the L–HPA system (Barbazanges et al., 1996, Schneider and Moore, 2000).

Section snippets

Measurement

Studies of the L–HPA system of young children are hampered by the need to use non-invasive measures. Corticotropin-releasing hormone (CRH) has never been assessed in healthy children because it involves sampling of cerebrospinal fluid. Several researchers have examined adrenocorticotropin hormone (ACTH) activity which requires blood sampling (e.g., Dahl et al., 1991), but such studies typically have not been performed with infants and preschoolers. Plasma sampling has been used in a number of

Developmental changes

Basal concentrations of cortisol change over the course of development. At birth, cortisol binding globulin (CBG) levels are low, resulting in low levels of total cortisol (bound and unbound) in plasma (Hadjian et al., 1975). Nonetheless, salivary concentrations, reflecting the unbound fraction of the hormone, tend to be as high in newborns as in adults (Gunnar, 1992). Newborns do not show the adult rhythm in cortisol production, but rather exhibit two peaks 12 hours apart that are not

Lowering cortisol below home baseline levels

Although elevations in cortisol are typically the focus of research on this system, it has been frequently noted that the system can respond bidirectionally (Frankenhaeuser, 1979, Handlon et al., 1962, Levine and Coover, 1976). Using home baseline levels as a benchmark, a number of studies with infants and preschool-aged children have yielded evidence that cortisol levels readily can be lowered below baseline. Studies, typically conducted in the morning hours, have revealed that cortisol levels

Developmental changes in cortisol response

Rodents enter a period between 4 and 14 days when it is difficult to elevate glucocorticoids (Rosenfield et al., 1992). Humans also appear to dampen their cortisol response to stressors over the first year of life (Gunnar et al., 1996b, Larson et al., 1998, Ramsay and Lewis, 1994). The functional effect seems similar to that observed in the rodent; although, as the mechanisms are not understood, at this point this should be considered an analogous, not homologous phenomena. Furthermore, while

Quality of care and cortisol responsivity

In rodents, maternal licking and grooming and arched back nursing appear to maintain low levels of glucocorticoids (Caldji et al., 1998, Rosenfield et al., 1992, Suchecki et al., 1993). In non-human primates, the presence of the mother, even if the infant cannot physically contact her, provides a powerful buffer, reducing elevations in cortisol to stressors like capture, handling, and separation (Bayart et al., 1990). As will be described, in humans, the quality of care the child receives from

Peer relations and cortisol levels in group care settings

By the preschool years, children become highly motivated to make friends and play with other children (Hartup, 1979). Peer relations, however, are complex and challenging to young children as playing nicely with others requires cognitive and behavioral skills that are just developing in the preschool years. These skills include controlling inappropriate behavior, explaining oneself using words and adjusting the explanation based on the listener's response, maintaining play themes over

Daycare quality and rising cortisol levels over the day

For 3- to-5-year old children in full-day center-based childcare, larger increases from morning to afternoon are observed in centers of poorer quality (Lane et al., 2000, Tout et al., 1998). Similarly, changes in cortisol levels over the morning hours at childcare have been shown to correlate with adult:child ratios and group size — standard indices of childcare quality (Legendre and Kortinus, 1996). Family-based childcare typically involves both fewer children and adults, and thus may be less

High risk children and families

The studies described above generally involved what would be considered low risk children and families. As one moves from such low risk samples to higher risk samples, the limitations of only measuring cortisol become apparent. The L–HPA often maintains normal cortisol levels in response to chronic stressors; while pituitary levels of adrenocorticotropin hormone (ACTH) often reveal significant effects of chronic stress. (Heim et al., 2000). The capacity of the L–HPA system to maintain cortisol

Summary and conclusions

During early development in humans, cortisol activity is sensitive to social regulation. Under conditions of sensitive and responsive caregiving, the high cortisol responsivity of the newborn diminishes and it becomes difficult to provoke increases in cortisol to many stressors by the end of the first year of life. Presumably this functional glucocorticoid hyporesponsiveness develops as children learn to expect that their attachment behaviors (e.g., proximity seeking) and distress reactions

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