The significant effect of childhood parental nurturance on hippocampal morphology is consistent with animal literature suggesting that early parenting experience affects later hippocampal development (Meaney et al., 1989
; Francis et al., 1999
; Liu et al., 1997
; Bredy et al, 2003
; Olson et al., 2006). However, the direction of the relationship, namely more nurturance associated with smaller hippocampi is, at least ostensibly, contrary to findings of enhanced neuronal survival in animals. However, this negative correlation may be less surprising in the context of pediatric literature. Although human studies of Post Traumatic Stress Disorder (PTSD) have generally documented smaller hippocampal volumes in adults experiencing pathologically high levels of stress (Bremner et al., 1997
; Stein, 1997
), pediatric PTSD studies show either equivalent or larger hippocampal volumes in children with PTSD compared with control subjects (De Bellis et al, 1999
; Carrion et al., 2001
; Tupler and DeBellis, 2006
). These findings are consistent with the negative relationship between hippocampal volume and the quality of parental care found in the present healthy sample.
Additional context for understanding the inverse relationship between early parental nurturance and hippocampal volume is provided by a recent MRI study (Gogtay et al., 2006
) on hippocampal development in normal human brain. This longitudinal study demonstrated a complex pattern of expansion and contraction of different subregions of the hippocampus, many of which follow inverse U-shaped developmental curves. Specifically, in the left middle hippocampus, the region where we found that early childhood parental nurturance negative correlated with adolescent hippocampal volume, the developmental curve (see region C in the left middle hippocampus at Figure 3 in Gogtay et al., 2006
) clearly showed that volume in this subregion increased from early childhood at age 4 to a peak during adolescence at about age 12, and subsequently decreased from adolescence to adulthood. The age range of adolescent participants in the present study fell in the decreasing part of curve. Moreover, meta-analysis of hippocampal morphology (Van Petten, 2004
) in developing brains has shown little change of absolute hippocampal volume between the ages of 4 and 18 in the context of continuous expansion of whole brain volume. In light of this evidence, the negative association between early childhood parental nurturance on adolescent hippocampal volume is at least consistent with accelerated hippocampal maturation for adolescents with a high level of parental nurturance or conversely a delay in hippocampal maturation for children with lower levels of parental nurturance.
Animal studies on environmental enrichment and maternal care both support the notion of hippocampal changes associated with early experience. However, the lack of relationship between environmental stimulation and hippocampal volume is consistent with prior animal studies showing that hippocampal neurogenesis is not necessary related to the behavioral effects of environmental enrichment (Meshi et al., 2006
). It is also possible that such effects are simply weaker than the effects of nurturance, or depend on aspects of environmental stimulation not well measured by the HOME or not sufficiently variable in our sample. Nevertheless, the unique predictive value of parental nurturance at age 4 in the present study suggests a more important role for warm parental care over cognitive stimulation for normal hippocampal development, especially during early childhood years. Particularly, our findings that the hippocampal volume is modulated by parental nurturance at age 4 but not age 8 are concordant with a recent study showing that the hippocampus was maximally sensitive to the effects of childhood sexual abuse occurring at age 3–5 years, but not at 6–8 or 9–10 years (Anderson et al., 2008). These results provide converging evidence supporting the hypothesis that brain structures susceptible to stress may have unique periods during which they are maximally sensitive to early stress during brain development (Teicher et al. 2006
A limitation of the present study was that the children in our study sample were all from African American families of low socioeconomic status (SES). SES is associated with many aspects of childhood experiences. Lower SES is associated with less environmental stimulation in the forms of toys, books, and recreational opportunities, as well as less maternal care from the family as a whole and less supportive parenting practice (Bradley et al., 2001
). Individuals with lower SES may be exposed to more stressful events in their lives (Dohrenwend, 1973
), have more health problems (Anderson and Armstead, 1995
), and differ in some aspects of neurocognitive development and function (Hackman & Farah, 2009
). Therefore, we cannot be certain whether the results obtained with this sample would generalize to children of different ethnicity or socioeconomic background. However, with over 17% of American children living below the poverty line according to the 2004 census, low SES is not abnormal or atypical in our society. Our results demonstrate that even within the low level of SES, the quality of parental nurturance at early childhood can alter hippocampal volume in adolescence. This finding is consistent with a recent report (Buss et al., 2007
) showing that maternal care modulates the relationship between prenatal risk and hippocampal volume in adults, with birth weight predicting hippocampal volume in adulthood only in female subjects with low levels of maternal nurturance. Future studies will be needed to further examine whether the same effects of parental nurturance on hippocampal volume can be observed in children from families of middle to higher SES.
Without manipulating or controlling for genetic relatedness, for example by studying adoptees, we cannot be certain that the relationships reported here between childhood experience and later brain morphology exactly reflect the effects of experience on brain development. Alternative patterns of causality could also be present. For example, children who have smaller hippocampi might also tend to receive higher levels of nurturance from their parents, or parents who innately provide greater nurturance might also tend to have genes that predispose their children to smaller hippocampi. Further research will be needed to provide more strict control to further clarify these alternatives. However, at present, although neither of the alternative scenarios can be ruled out, neither has any independent support. In contrast, animal research has shown that early experience actually exerts an effect on hippocampal development (Meaney et al., 1989
; Liu et al., 1997
; Francis et al., 1999
; Duffy et al., 2001
; Bredy et al, 2003
; Olson et al., 2006), which supports the present conclusion.
In conclusion, three aspects of the present results deserve emphasis. First, as expected from the animal literature but never before demonstrated in humans, variations in childhood experience of healthy human bears a significant relationship to brain structure. Second, the effect of childhood experience may be highly selective, with parental nurturance but not environmental stimulation being related to hippocampal morphology. Third, the timing of this relationship between childhood experience and hippocampal structure is consistent with the existence of a sensitive developmental period, with only the earlier measure of parental nurturance at age 4 predicting adolescent hippocampal volume. The present findings thus provide an important bridge between the study of normal neurocognitive development and early experience in humans, which has only been validated in animal models until this time.