We provide evidence for a neurodevelopmental mechanism linking early institutional rearing with hyperactivity and impulsivity, two core features of ADHD. Specifically, we find that differences in brain activity among young children raised in Romanian institutions relative to community control subjects explain, in part, differences in the prevalence of symptoms of ADHD between these groups at 54 months. This neurodevelopmental mechanism is specific to the development of the ADHD symptoms of hyperactivity and impulsivity and is unrelated to other types of psychopathology. These findings provide, to our knowledge, the first empiric demonstration of an underlying neurodevelopmental pathway that explains the association between institutionalization and subsequent psychiatric problems. This finding sheds light on pathophysiologic pathways to ADHD and has implications for understanding the effect of early experience on neurodevelopment.
ADHD symptomatology has been associated with increased low-frequency (theta) and decreased mid-frequency (alpha) and high-frequency (beta) brain activity in a number of previous studies (19
). Because the EEG has poor spatial resolution, it is unclear which specific brain structures are driving the pattern of findings described here. Although many possible explanations for this pattern exist, the consistently identified gray matter reductions in frontostriatal circuits among children with ADHD represent one potential explanation (40
). Several studies have observed reductions in cortical gray matter volume among children with ADHD (41
). For example, decreased volume in a variety of areas, most consistently in the prefrontal cortex and basal ganglia, have been documented among children with ADHD relative to control subjects (40
). Recent evidence suggests that cortical thinning in children with ADHD may be more widespread across the cortex (42
). These findings are consistent with our observation of elevated theta and reduced alpha power across several cortical regions. Alternatively, it has been posited that in ADHD, the pattern of brain activity observed in our study reflects a developmental delay in cortical maturation that results in greater relative theta activity (19
). In typically developing children, this pattern of EEG power is evident in earlier developmental stages; as children mature from infancy through middle childhood, their EEG is characterized by increasing power at higher-frequency components (28
). Longitudinal findings documenting a substantial delay in cortical maturation among children with ADHD compared with children without the disorder appear to support the developmental delay theory (41
). We extend these findings by providing evidence suggesting that aspects of neural functioning measured by the EEG, potentially reflecting cortical maturation, are sensitive to social and environmental context and may be delayed or stunted in deprived environments, leading to psychopathology.
The pattern of elevated low-frequency EEG power and decreased mid- to high-frequency power indicative of a delay in cortical development uniquely predicted hyperactivity and impulsivity in this study and was largely unrelated to inattention, anxiety, depression, or ODD. This finding is consistent with prior research documenting different profiles of brain activity among children with primarily inattentive ADHD compared with impulsive/hyperactive ADHD (19
). It should be noted, however, that alpha and theta relative power were marginally related to inattention. The lack of significant associations here may actually reflect problems with the measurement of inattention in early childhood. At 54 months, parents and guardians have observed the children in numerous situations that would differentiate them along the dimensions of activity level and impulsivity but considerably fewer situations that would differentiate them along the dimensions of sustained and focused attention. Because the latter dimensions become more obvious once children begin school, the associations between EEG power and inattention warrant reexamination when the children are older and parents or guardians have had more opportunities to observe inattentive behaviors. Importantly, the specificity of the identified neurodevelopmental pathway to ADHD symptomatology suggests that other mechanisms that have yet to be identified underlie the associations between institutional rearing and other psychiatric outcomes. However, because impulsivity and hyperactivity are associated with elevated risk for the subsequent development of other psychiatric problems such as oppositional defiant disorder and substance abuse (45
), this neurodevelopmental pathway may indirectly underlie the association between institutionalization and these psychiatric outcomes at later points in development, a possibility that remains to be examined in future research.
It is possible that differences in EEG profiles and ADHD symptomatology between children reared in institutions versus the community resulted from factors other than institutional care. However, evidence from other samples of institutionalized children indicates similar associations of institutionalization with ADHD (2
) and abnormal brain development (16
). Moreover, the foster care intervention had some ameliorative effects on EEG profiles in the BEIP (47
), suggesting that EEG differences resulted, at least in part, from institutionalization. Previous research suggests that children removed from institutional care before 6 months of age are at considerably lower risk for the development of ADHD than children placed later (2
), indirectly suggesting the presence of a very early sensitive period for the development of neural circuits underlying ADHD. The lack of intervention effects for ADHD symptoms in the BEIP is therefore unsurprising, given that none of the children were placed before 6 months. Importantly, the beneficial effects of foster care on EEG profiles were observed only among children removed from institutional care at the earliest ages (47
). Together, these lines of evidence suggest that EEG and ADHD group differences reflect true effects of institutionalization.
Identification of a neurodevelopmental pathway linking early experience to psychopathology has relevance for understanding the relations between other types of early-life deprivation and psychiatric disorders. Although institutional rearing represents an extreme environment, psychosocial deprivation and neglect are not uncommon among maltreated children (48
). Moreover, a similar pattern of increased low-frequency and decreased mid- to high-frequency EEG activity, as well as higher rates of ADHD, has been reported among children raised in poverty (51
). It is therefore possible that similar neurodevelopmental mechanisms underlie the associations of ADHD with neglect and child poverty. However, because institutional rearing deprives children of multiple domains of expected environmental experiences ranging from sensory stimulation to language exposure to the ability to form an attachment to a primary caregiver (12
), it remains unclear which environmental factors are associated with the atypical patterns of brain development found in institutionalized children. Identification of the specific aspects of environmental deprivation that predict neurodevelopmental abnormalities is imperative for targeting high-risk populations that would benefit from preventive intervention.
Findings must be interpreted in light of study limitations. First, although EEG power is an indicator of brain development that reflects observable changes as children develop (28
), we did not measure brain development per se given that the EEG was examined only at one time point. Second, we acknowledge that group differences in ADHD symptoms may have resulted, at least in part, from factors other than postnatal rearing environments, such as prenatal malnutrition or exposures to toxins (54
). We have no evidence to suggest that harmful prenatal exposures were more common in Romanian families who give their children over to institutional care, but this remains a possible alternative explanation for our findings. Although we cannot rule out genetic contributions to ADHD, most children in BEIP were placed in institutions at birth so that selective placement of children suspected of abnormalities is unlikely. Third, EEG assesses mass neural action, particularly in the cortex, such as the potentials of aligned pyramidal cells (56
). EEG profiles therefore provide a global assessment of brain development but contain limited information regarding localized functioning due to poor spatial resolution. Finally, because of the relatively small sample size, we examined psychiatric symptoms as outcomes rather than categorical diagnoses. Importantly, however, symptoms were assessed using a reliable structured diagnostic interview, which is the gold standard psychiatric assessment for young children (33
Atypical brain development related to institutionalization partially explains the association between institutional rearing and ADHD symptomatology. Deprivation in social and environmental conditions may become biologically embedded during early neurodevelopment and manifest as psychiatric problems later in life. Identification of neurodevelopmental mechanisms linking deprivation to psychopathology is critical for the development of interventions to reduce the mental health consequences of adverse early environments.