This prospective study is the first to evaluate the effects of congruence between prenatal and postnatal levels of maternal depression on human infant development. We obtained support for the PAR model with our counterintuitive finding that infants thrive, at least on dimensions of critical psychomotor and mental development, when their prenatal and postnatal environments are congruent, even if the conditions of those environments are adverse (Kurstjens & Wolke, 2001
; Moehler et al., 2007
). Moreover, postpartum euthymia in mothers did not benefit the psychomotor and mental development of infants who had been exposed to maternal depressive symptoms in utero; this finding is consistent with the predictions of the PAR model. Specifically, infants’ mental and motor functions were relatively impaired when their mothers exhibited symptoms of depression during pregnancy but became euthymic during the first 3 months after birth. These results are consistent both with reports that exposure to incongruent prenatal and postnatal nutritional conditions increases infants’ risk of developing metabolic disease and with findings of adaptive advantages among infants exposed to matching prenatal and postnatal nutritional environments (Cleal et al., 2007
; Gluckman & Hanson, 2004
Our findings indicate that stability between the prenatal and the postnatal environments prepares the fetus for postnatal life and that this preparation confers an advantage in critical survival functions during early development. The progression from superior psychomotor ability to superior mental ability during the 1st year of life among infants in the two concordant groups might indicate both a short-term adaptive response and the selection of a special characteristic that may be critical for survival (Bateson et al., 2004
). Advanced psychomotor skills are advantageous early in development, when infants’ capacities for language and reasoning are undeveloped. As infants approach 1 year of age, they begin to use rudimentary language and reasoning, and it is reasonable to assume that advanced mental abilities increase infants’ opportunity for survival. It is possible that a progression of special skill advantages continues throughout the life span of infants such as those in our concordant groups and that accelerated psychomotor and mental development is replaced by advantages in other proficiencies.
The observed effects that were consistent with the PAR model were largely attributable to congruence between maternal depressive symptoms at midgestation (approximately 25 weeks) and postpartum. The human fetus may be especially sensitive or vulnerable to adversity during this period, as has been reported previously (Davis et al., 2005
; DiPietro, Novak, Costigan, Atella, & Reusing, 2006
; Glynn, Wadhwa, Dunkel Schetter, & Sandman, 2001
; Sandman, Davis, Buss, & Glynn, 2011
). Moreover, in a study of another large cohort of women, we found that biological and psychological symptoms of maternal depression at approximately 25 weeks’ gestation were the strongest predictors of postpartum depression (Yim et al., 2010
; Yim, Glynn, Dunkel Schetter, Chicz-DeMet, & Sandman, 2009
). These findings indicate that the fetus is most sensitive to maternal signals of adversity when those signals are the most predictive of future outcomes.
Without question, congruently favorable conditions before and after birth are beneficial for developing infants and children (Ainsworth, Blehar, Waters, & Wall, 1978
; Calkins, Graziano, Berdan, Keane, & Degnan, 2008
; Kochanska, Philibert, & Barry, 2009
). Our finding that congruently unfavorable circumstances can also convey adaptive advantages may be at odds with the predominant view of development, which assumes that early exposures to adversity are associated with significant lifelong costs to survival, growth, and reproduction. Other models of development, however, propose that early exposures to stress have beneficial consequences later in life. For instance, the stress-inoculation model
predicts that exposure to mild stress during early development promotes resilience in the face of stressful (i.e., congruent) circumstances later in life (Lyons & Parker, 2007
). The theory of biological sensitivity to context
(Ellis, Boyce, Belsky, Bakermans-Kranenburg, & van Ijzendoorn, 2011
) posits that early exposure to stress increases the lability of responses to subsequent adversity. This increased lability results in increased impairment after exposure to stress later in life but also an enhanced ability to benefit from supportive and protective features of the environment.
The debate about the adaptive consequences of early exposure to adversity, specifically in relation to the rate of maturation, is yet unresolved. According to one view, the delayed growth and reproduction following early exposure to adversity may be adaptive, given that delayed growth and reproduction will reduce nutritional requirements if resources are scarce during early development (Bogin et al., 2007
). There is some evidence, however, that early exposure to psychosocial adversity accelerates maturation, especially in the area of reproductive development. For example, exposures to psychosocial adversity during early development and again later in life are associated with accelerated sexual maturation in girls (Coall & Chisholm, 2003
; Nettle, Coall, & Dickins, 2010
). Researchers have argued that such early maturation maximizes the probability of reproduction and allows females to increase their number of offspring; in conditions of increased health risk, this greater number of offspring will ensure that more offspring survive.
Considering our findings in the context of this debate suggests competing explanations for the similarity between the concordant groups in our study. First, it is possible that the concordant-adversity group exhibited the accelerated maturation associated with early adversity but that the mental and motor advantages observed among infants in the concordant-favorability group reflected the benefits of relatively favorable prenatal and postnatal environments. Second, the similarities between the two concordant groups may have resulted from the same factors. If so, either both groups or neither group exhibited accelerated maturation. Subsequent follow-up studies of the subjects in these groups could determine whether either group exhibited the life-history costs typically associated with accelerated maturation. However, the improved motor and cognitive skills in the two concordant groups may have resulted not from accelerated maturation but rather from fetal prediction of and preparation for postnatal life. We believe that our findings support the conclusion that it was the congruence between prenatal and postnatal exposures to maternal depression, and not the exposure to maternal depression itself, that determined infants’ outcomes.
The precise mechanism by which a pregnant woman communicates her psychological state to her fetus is unknown. One possibility is that maternal stress and depression expose the fetus to elevated levels of stress hormones. The relation between psychosocial measures of adversity, including depression, and HPA activity during pregnancy was nonsignificant in our study and has been found to be low or nonsignificant in a number of other studies (Davis & Sandman, 2010
; Harville, Savitz, Dole, Herring, & Thorp, 2009
; Kramer et al., 2009
); these findings suggest that stress hormones alone are not the mechanism by which maternal signals of psychosocial adversity are communicated to the fetus.
Fetal exposure to maternal depression has been shown to be associated with increased methylation of the glucocorticoid receptor gene in neonates and with increased HPA responses to stress or adversity; this finding suggests that an epigenetic mechanism may underlie both the maternal communication of adversity to the fetus and the persistent influence of the exposure (Oberlander et al., 2008
). In addition, animal studies have indicated that specific patterns of maternal care during early development can alter the methylation of the nerve growth factor-inducible protein A (NGFI-A) binding site in a region of the Nr3c1 promoter responsible for the control of hippocampal glucocorticoid receptor expression; such findings support the possibility of this epigenetic effect and point to its direct implications for areas of the nervous system involved with mental development (Weaver et al., 2004
). These findings, and findings from other studies reporting a link between persisting altered expression of the brain-derived neurotrophic factor in the prefrontal cortex and exposure to early adversity (Roth et al., 2009
), suggest possible routes of maternal influence on fetal and early infant neurological development that have profound implications for infants’ adjustments to life challenges.