EEG power distribution was assessed in internationally adopted post-institutionalized 18-month-olds as compared to age-matched non-adopted children and children internationally adopted from foster care. The association of this 18-month power distribution with indiscriminate friendliness and inhibitory control at 36 months was examined. As hypothesized, the post-institutionalized children had a relative concentration of EEG power in lower frequency bands compared to the non-adopted children. That is, the post-institutionalized children had higher relative theta power and lower absolute alpha power than the non-adopted children. This pattern of higher relative theta power and lower absolute alpha power was associated with indiscriminately friendly behavior at 36 months. The relative concentration of power in lower frequency bands also was linked to poorer inhibitory control on delay of gratification tasks at 36 months. Both internationally adopted groups were more likely than the non-adopted group to show indiscriminately friendly behavior. These results were not explained by measures of general deprivation or global cognitive ability. Each of these findings will be discussed, in turn.
Prior to this discussion, it is important to place the present sample of post-institutionalized children within the broader framework of post-institutionalized and institutionalized children whose brain activity patterns have been previously reported in the literature. The studies of neural development reviewed in the introduction included exclusively Eastern European children, often with an extended duration of institutionalization. The post-institutionalized children in this study were adopted at 12 months of age on average, and all of them were 16 months or younger at adoption. They may be at lower risk than children adopted following more prolonged periods of institutional care (Nelson, Zeanah, Fox, Marshall, Smyke, & Guthrie, 2007
). The foster care children were even younger, averaging only 8 months old at adoption. About 70% of the current post-institutionalized sample was from China. Eastern European children placed in institutional care are known to be at elevated risk of prenatal alcohol exposure and low birth weight (Johnson, 2000
), which are both risk factors for developing attention and behavior problems (e.g. Nanson & Hiscock, 1990
). Prenatal alcohol exposure has been linked with EEG abnormalities in human infants (Chernick, Childiaeva, & Ioffe, 1983
) and in animals (Cortese, Krahl, Berman, & Hannigan, 1997
; Kaneko, Riley, & Ehlers, 1993
). For Eastern European samples with a high risk of prenatal alcohol exposure, it is difficult to tell if neural abnormalities are due to prenatal experience, institutional rearing, or some combination. While children adopted from China also could have prenatal risks, this may be less common. In the current sample, prenatal alcohol exposure was suspected by half of the adoptive parents of children from Eastern Europe but by none of the adoptive parents of children from China. Shorter duration of deprivation, lower prenatal risk, and international diversity are strengths of the current sample because they permit characterization of the specific effects of a brief period of deprivation on early neural and behavioral development.
The excess of relative theta power observed in the post-institutionalized children is consistent with the hypoactivation model that has been posited in previous studies of the effects of institutional rearing on neural development (Marshall et al., 2004
; Moulson, Westerlund, et al., 2009
; Parker et al., 2005
). The generalization of this pattern consistent with hypoactivation to this relatively low risk sample strengthens the case that chronic neural hypoactivation may be associated broadly with a history of early deprivation, as opposed to reflecting some idiosyncrasy of the genetic characteristics or prenatal or postnatal experience of children reared in Eastern European institutions. The group differences in relative and absolute power strikingly parallel the group differences Marshall et al. (2004)
reported for currently institutionalized children as compared to non-adopted children. The currently institutionalized children in their study and the post-institutionalized children in this study both had higher relative theta power and lower absolute alpha power compared to non-adopted children. Electrical activity in higher frequency bands is associated with a more alert state and with faster and more active processing, so a relative reduction of power in these higher frequency bands suggests the brains of children with a history of deprivation and disruptions in care may be hypoactivated. This hypoactivation may persist for at least some period following adoption into a more stimulating environment.
The post-institutionalized group had been with their families an average of 6 months, so EEG abnormalities persisted for at least 6 months following removal from the institutional rearing environment. This finding is consistent with Marshall et al.’s (2008)
follow-up, in which it took 24 to 36 months after removal from the institutional setting for the atypical power distribution to begin to ameliorate compared to still-institutionalized children. The foster care group in the current study, who had been with their families for 10 months on average, were intermediate to the non-adopted and post-institutionalized groups with regard to relative theta power, which may be consistent with a gradual shift in EEG patterns following adoption. It should be noted that the foster care group still had lower absolute alpha power than the non-adopted group. It appears that neural activation patterns have some capacity to adjust following early deprivation, but the course is a protracted one. As Marshall et al.’s follow-up (2008)
did not include a never-institutionalized comparison group, it is not known if the group removed from institutional care had reached the point that they approximated the power distribution of never-institutionalized children, or if there were constraints on this plasticity.
While the neurodevelopmental mechanisms underlying the links between early relational deprivation and an atypical power distribution are not yet known, it is possible that the lack of individualized attention from a stable, responsive caregiver delays or derails aspects of neural development. Drawing on evolutionary biology, Shonkoff (2010)
proposes a biodevelopmental framework, in which the infant brain expects to develop in the context of certain species-typical environmental characteristics, including ample contingent social interaction with a stable caregiver, and that these experiences are necessary for brain architecture to develop normally (Shonkoff, 2010
). EEG becomes concentrated in higher frequency bands with development, reflecting neurodevelopmental processes such as myelination (John et al., 1980
). We speculate that for institutionalized children, the lack of social interaction with a primary caregiver may interfere with neurodevelopment, resulting in a relative excess of low frequency power. We further speculate that the partial amelioration of these EEG abnormalities following placement in foster care in Marshall et al.’s (2008)
sample could be explained by the increase in one-on-one social interaction that the children experienced, which could have facilitated neurodevelopmental processes that were stalled or derailed while the children were institutionalized.
The current data does not allow differentiation between the maturational lag and sensitive period models. These models are incompatible, as the maturational lag model implies open-ended neural plasticity whereas the sensitive period model specifies limited plasticity to adapt to the post-adoption environment. Either model could fit with cortical hypoactivation in children with a history of institutional rearing: Hypoactivation could be temporary and likely to ameliorate following removal from the institutional environment, or it could be chronic and permanent. Following internationally adopted children over several years after adoption with repeated EEG measurements would allow examination of the developmental course of EEG power distributions. Even if cortical activation eventually rebounds to normal levels, one question to consider in future research is the developmental effect of having experienced an extended period of cortical hypoactivation. It is possible that the neural abnormalities underlying an atypical EEG power distribution might shape the developing child’s brain and behavior in the early years of life in such a way as to contribute to enduring attention problems, even if the power distribution itself eventually returned to a developmentally typical pattern.
In the ADHD literature, a relative excess of low frequency power is associated with attention problems (Barry et al., 2003
). The persistence of this same neural abnormality in post-institutionalized children suggests a possible neural basis for the enduring attention problems often observed in these children. In the current study, children with less relative beta at 18 months had poorer inhibitory control at 36 months, and an excess of relative theta power at 18 months predicted the presence of indiscriminately friendly behaviors at 36 months. Thus, a relative excess of slow wave power was associated not only with attention deficits but also with indiscriminate friendliness. This finding provides initial evidence of neurodevelopmental correlates of a persistent socioemotional problem exhibited by some children with a history of early social deprivation. The association of indiscriminate friendliness with cortical hypoactivation, a neural pattern commonly observed in children with ADHD, tallies with reports associating indiscriminate friendliness with attention deficits in internationally adopted children (Bruce et al., 2009
; Roy et al., 2004
The prevalence of attention deficits in the current sample was unknown. Children are unlikely to be diagnosed with ADHD as early as 36 months, and attention regulation abilities are still developing at this age. On the one aspect of attention assessed in the current study, inhibitory control, the post-institutionalized children did not differ from the non-adopted children. While disordered attention was not evident in this sample, which was low risk compared to previously-studied post-institutionalized samples, the association of hypoactivation with indiscriminate friendliness suggests pathways through which disinhibited social behaviors may become organized in development. The observed indiscriminately friendly behaviors were markedly developmentally inappropriate violations of social boundaries. For example, when the stranger entered the room for the first time, one child exclaimed, “I missed you!” Several children touched the stranger’s knee or grabbed her hand. While indiscriminate friendliness was coded as present or absent due to its low incidence (occurring in about 20% of both internationally adopted groups), some children exhibited as many as three inappropriate personal questions or comments and three initiations of physical contact within the 10 minute interaction.
Hypoactivation is not sufficient to result in indiscriminate friendliness. Children with ADHD and no history of early deprivation and disruptions in care typically are not described as exhibiting indiscriminately friendly behaviors. However, early deprivation and early disruptions in care appear to predispose children both to hypoactivation and to indiscriminate friendliness. Further research is needed to determine if cortical hypoactivation predicts individual differences in behavioral outcomes among children who have experienced adverse early care environments.
Accounting for the heterogeneity of outcomes in children who have experienced deprivation, neglect, and disruptions in care is a central challenge as the field moves forward. The measures of preadoption risk in the current study did not support the idea of a risk gradient or dose-response relationship to explain individual differences in relative and absolute power among the internationally adopted children. Parent report of early care risk factors and prenatal risk factors was unrelated to EEG, though this should not be taken as evidence that pre-adoption experiences are unimportant. The dearth of reliable information about children’s preadoption histories is a problem endemic to research on internationally adopted children, and the current study is no exception. The children came from a variety of institutions and foster care homes in several countries, and direct measures of the quality of care in these settings were not available. Adoptive parent report was not based on first-hand observation, was likely incomplete, and could be colored by the parent’s perception of the child’s current functioning. Age at adoption and growth at adoption are more objective, though rough, estimates of exposure to deprivation, and these measures were not related to EEG power. However, the adopted children as a group were not growth delayed and were all adopted before 18 months of age. To determine if EEG power is related to malnourishment or duration of deprivation, a higher risk sample would be needed. While the adopted children had lower nonverbal cognitive ability, this measure was unrelated to EEG power or to indiscriminate friendliness, suggesting that atypical power distribution and indiscriminate friendliness were not simply indicators of global developmental delays. Marshall et al. (2008)
reported that EEG measures did not mediate the relation between age at placement and developmental quotient in their sample of post-institutionalized children in foster care.
Progress in accounting for heterogeneity will depend both on acquiring more reliable and detailed information about the pre-adoption environment and on moving toward a consideration of genetic factors. Partnering with adoption agencies or individual institutions in the future may provide better estimates of the quality and characteristics of care in the pre-adoption environments. Work of this sort is beginning (Groark et al., 2005
; Zeanah et al., 2003
), though this will be challenging to put into practice. Obtaining measures of targeted genetic polymorphisms also will be challenging but potentially very useful. Genetics may play a role in individual differences in the vulnerability of the developing brain to adverse early care environments and the degree of neural plasticity in response to the post-adoption environment (for example see Stevens, Kumsta, Kreppner, Brookes, Rutter, & Sonuga-Barke, 2009
To discriminate specific effects of institutional rearing from effects that would generalize to other forms of adversity, a comparison group of children internationally adopted from foster care was included. Like the post-institutionalized children, the foster care children had experienced abandonment and early care disruptions, but they had spent little or no time in institutional settings. While the foster care children did not differ from either of the other two groups in the relative power distribution, they had lower absolute alpha power than the non-adopted children. Indeed, the foster care children looked very similar to the post-institutionalized children with regard to absolute alpha power, with both adopted groups having lower absolute alpha power than the non-adopted children in central, parietal, and temporal scalp regions. The presence of EEG abnormalities in the foster care children, who were adopted at an average of 8 months old, is testament to the vulnerability of this developing system. Foster care children were just as likely as post-institutionalized children to exhibit indiscriminately friendly behaviors at 36 months. Indiscriminate friendliness occurred in about one in five of the post-institutionalized and foster care children; in contrast, none of the non-adopted children exhibited indiscriminately friendly behaviors. The presence of indiscriminate friendliness in both internationally adopted groups is consistent with results Bruce et al. (2009)
reported for six- and seven-year-old children.
The prevalence of EEG abnormalities and indiscriminate friendliness in the foster care children indicates that these neural and behavioral deficits are not specific to institutional care histories but reflect a broad range of adverse early care experiences. Both groups experienced abandonment and relational disruptions in the early years of life. Little information is available as to the quality of foster care in the various countries, so it is possible that some of the children experienced deprivation or neglect while in foster care. If possible, it would be helpful to obtain better descriptive information about international foster care environments, though there are numerous barriers to this type of research. At a minimum, these children experienced relational disruption in the form of the loss of a stable primary caregiver, the foster parent, at the time of adoption. A pattern of EEG abnormalities quite similar to that seen in the post-institutionalized and foster care groups has been observed in impoverished, high risk Latin American children (Harmony et al., 1988
; Otero, 1994
; Otero et al., 2003
), indicating that psychosocial deprivation can have developmental effects on EEG. Documenting indiscriminate friendliness in foster care children, Bruce et al. (2009)
emphasized the importance of including comparison groups, such as children internationally adopted from foster care and maltreated/neglected children, in studies of post-institutionalized children’s behavioral development. The current findings underscore this recommendation, and suggest the need for these comparison groups in studies of post-institutionalized neural development, as well. The resulting data would clarify whether all these children are simply on a continuum of deprivation, with corresponding effects on neural and behavioral development, or whether certain abnormalities may be specifically associated with the institutional rearing environment.
The current study has several limitations. As has already been noted, parents may not have been able to provide complete or reliable information about their children’s pre-adoption experiences, so it was not possible to disentangle the influence of specific prenatal and early care factors on neural development. A low-density EEG array was used, which has limited spatial resolution. Use of a high-density array in future studies would allow for fine-grained analyses of regional patterns of EEG power. There was a predominance of females in the postinstitutionalized sample, though there were no gender differences on any of the variables of interest. Finally, the children were too young for most measures of attention regulation at 36 months. Executive functions are only just beginning to emerge at 36 months, and develop extensively throughout the preschool years and beyond (Diamond & Taylor, 1996
). The current study did include delay of gratification tasks as age-appropriate measures of one aspect of attention regulation, inhibitory control, but a comprehensive assessment of multiple domains of attention regulation was not developmentally appropriate for this age group.
In sum, the findings from this study provide initial evidence that the relative excess of theta power which has been observed in currently institutionalized children persists in post-institutionalized children several months after adoption, and is not limited to children of Eastern European origin. This atypical power distribution, which also is characteristic of ADHD, predicted both indiscriminate friendliness and poor inhibitory control. These findings complement and extend previous research associating institutional rearing with neural abnormalities consistent with cortical hypoactivation. This study identifies longitudinal electrophysiological correlates of indiscriminate friendliness, and suggests that the same pattern of hypoactivation underlies both poorer inhibitory control and indiscriminate friendliness, consistent with behavioral studies relating indiscriminate friendliness to attention regulation difficulties (Bruce et al., 2009
; Roy et al., 2004
). The deficit in high-frequency absolute power and the presence of indiscriminate friendliness in children internationally adopted from foster care hint that these neural and behavioral abnormalities are not limited to children reared in institutions, but also may characterize other children with a history of relational deprivation. Replicating these findings and employing more specific neuroimaging methods will be critical to further characterize neurodevelopmental links between early relational deprivation and indiscriminate friendliness. It would be helpful to collect multiple electrophysiological and neuroimaging measures from the same sample, to see whether the various measures which have been interpreted as hypoactivation co-occur and whether they have shared behavioral correlates. It may be worthwhile to examine the EEG power distribution in other populations who have experienced disruptions of care, such as children in the U.S. foster care system. While the current study raises more questions than it answers, results highlight the need for more research on the impact of institutionalization and other disruptions of care on developing neural systems and how those neural systems may in turn shape behavioral development.