The formation of social attachments is a critical component of human relationships. Infants begin to bond to their caregivers from the moment of birth, and these social bonds continue to provide regulatory emotional functions throughout adulthood. It is difficult to examine the interactions between social experience and the biological origins of these complex behaviors because children undergo both brain development and accumulate social experience at the same time. We had a rare opportunity to examine children who were reared in extremely aberrant social environments where they were deprived of the kind of care-giving typical for our species. The present experiment in nature provides insight into the role of early experience on the brain systems underlying the development of emotional behavior. These data indicate that the vasopressin and oxytocin neuropeptide systems, which are critical in the establishment of social bonds and the regulation of emotional behaviors, are affected by early social experience. The results of this experiment suggest a potential mechanism whose atypical function may explain the pervasive social and emotional difficulties observed in many children who have experienced aberrant care-giving. The present findings are consistent with the view that there is a critical role for early experience in the development of the brain systems underlying basic aspects of human social behavior.attachment ͉ emotion ͉ oxytocin ͉ vasopressin ͉ child abuse T he social attachments formed between human infants and their caregivers begin very early in postnatal life and play a critical role in children's survival and healthy adaptation. Typically, adults provide infants with a social environment that is fairly consistent. Caregivers learn how to recognize and respond to the infants' needs, thereby creating predictable contingencies in the environment; these regularities, in turn, make the infant's environment secure and conducive to further social learning (1, 2). Multiple perceptual, sensory, cognitive, and affective systems must become synchronized so that a social bond can develop between an infant and caregiver; this bond is then reflected in the child's adaptive behavioral responses to the environment. The goal of this experiment was to address a fundamental evolutionary and developmental question: To what extent are the neurobiological systems that regulate affiliative behaviors dependent on the social experiences afforded to most infants by their caregivers?It is difficult to evaluate the effects of early social experience on the organization of the developing brain because, within seconds of postnatal life, the human infant experiences a vast amount of emotional input. In this regard, the maturation of the brain is confounded with the accumulation of social experience. One way to address this problem is to experimentally manipulate the social environment. Although this approach is successful with nonhuman animals, such studies are neither possible nor desirable to undertake with human children. There...

To examine the effects of early emotional neglect on children's affective development, we assessed children who had experienced institutionalized care prior to adoption into family environments. One task required children to identify photographs of facial expressions of emotion. A second task required children to match facial expressions to an emotional situation. Internationally adopted, postinstitutionalized children had difficulty identifying facial expressions of emotion. In addition, postinstitutionalized children had significant difficulty matching appropriate facial expressions to happy, sad, and fearful scenarios. However, postinstitutionalized children performed as well as comparison children when asked to identify and match angry facial expressions. These results are discussed in terms of the importance of emotional input early in life on later developmental organization.Over the last decade, the adoption of children across nations has increased substantially. In the United States alone, such adoptions now exceed 20,000 children per year (Immigration and Naturalization Service [INS], 2002). Today, approximately 85% of international adoptees have spent some or all of their lives in institutional, as opposed to family, care where the children have experienced combinations of physical and social deprivation (US State Department, 1999). Although the deprivation experienced by these children is often impossible to precisely quantify, it is apparent that these environments fall below the quality needed to sustain normal behavioral development, as evidenced by the rate at which children arrive in their adoptive homes with poor health, growth failure, and developmental delays (Johnson, 2000a;Johnson, Miller, Iverson, Thomas, Franchino, Dole, Kiernan, Georgieff, & Hostetter, 1992;Miller, 2000). Current estimates are that institutionalized infants and toddlers loose about 1 month of linear growth for every 3 months in institutional care, with behavioral development exhibiting similar dramatic reductions (Gunnar, 2001;Johnson, 2000b).Institutionally reared children have captured attention for decades. Early research on these children emphasized the deprivation of maternal care, although as Rutter (1981) rightly noted, not only maternal stimulation, but also many other types of stimulation needed for normal development is deficient in institutional environments. Thus, the study of these children addresses both basic science issues about the role of early experience on brain development and also applied issues about the kinds of interventions that are likely to support and foster optimal development for these children. Indeed, early studies revealed that postinstitutionalized (PI) children showed marked improvements when removed from orphanage settings and placed in family environments; nonetheless, persistent developmental differences in these children could be detected long after adoption, including deficits in emotional and social development (Fisher, Ames, Chisholm, & Savoie, 1997;Hodges & Tizard, 1989...

Human and non-human animal studies reveal that early experiences with caregivers shape children's ability to regulate their responses to stress. To understand the effects of early deprivation on the regulation of the hypothalamic-pituitary-adrenal axis following social interactions, we examined urinary cortisol levels in a group of internationally adopted children who had experienced institutional care, and thus, species-atypical attachment relationships, early in life prior to adoption. Cortisol regulation was assessed both basally and following standardized interpersonal interactions between the child and his/her mother and the child and an unfamiliar adult. Post-institutionalized children showed prolonged elevations in cortisol levels following the mother, but not the stranger, interaction. More severe neglect was associated with the highest basal cortisol levels and the most impaired cortisol regulation following the mother interaction. These results suggest that early social deprivation may contribute to long-term regulatory problems of the stress-responsive system, and that these differences are most evident within the context of ongoing, close interpersonal relationships.

Integrative studies of genetics, neurobiology and behaviour indicate that polymorphism in specific genes contributes to variation observed in some complex social behaviours. The neuropeptide arginine vasopressin plays an important role in the regulation of a variety of social behaviours, including social attachment of males to females, through its action on the vasopressin 1a receptor (V1aR). In socially monogamous prairie voles (Microtus ochrogaster), polymorphism in the length of microsatellite DNA within the regulatory region of the gene (avpr1a) encoding the V1aR predicts differences among males in neural expression of V1aRs and partner preference under laboratory conditions. However, understanding the extent to which V1aR mediates variation in prairie vole social and reproductive behaviour observed in nature requires investigating the consequences of avpr1a polymorphism and environmental influences under ecologically relevant conditions. We examined the relationship between avpr1a length polymorphism and monogamy among male prairie voles living in 0.1 ha enclosures during a time similar to their natural lifespan. We found no evidence that avpr1a genotype of males predicts variation in social monogamy measured in the field but some indices of social monogamy were affected by population density. Parentage data indicated that a male's avpr1a genotype significantly influenced the number of females with which he sired offspring and the total number of offspring sired. Total brain concentrations of V1aR mRNA were not associated with either male behaviour or avpr1a genotype. These data show that melding ecological field studies with neurogenetics can substantially augment our understanding of the effects of genes and environment on social behaviours.

Post-institutionalized Chinese and Eastern European children participated in two emotion understanding tasks. In one task, children selected facial expressions corresponding to four emotion labels (happy, sad, angry, scared). The second task required children to match facial expressions to stories describing situations for these emotions. While both post-institutionalized groups scored lower than the never-institutionalized children, those from China performed better than those from Eastern Europe. Post-institutionalized children's performance was predicted by their age at adoption.

Children who experience early caregiving neglect are very likely to have problems developing and maintaining relationships and regulating their social behavior. One of the earliest manifestations of this problem is reflected in indiscriminate behavior, a phenomenon where young children do not show normative wariness of strangers or use familiar adults as sources of security. To better understand the developmental mechanisms underlying the emergence of these problems, this study examined whether institutionally reared children, who experienced early social neglect, had difficulty associating motivational significance to visual stimuli. Pairing stimuli with motivational significance is presumably one of the associative learning processes involved in establishing discriminate or selective relationships with others. We found that early experiences of neglectful caregiving were associated with difficulties in acquiring such associations, and that delays in this developmental skill were related to children's social difficulties. These data suggest a way in which early social learning experiences may impact the development of processes underlying emotional development.

In the present work, we developed a database of nonlinguistic sounds that mirror prosodic characteristics typical of language and thus carry affective information, but do not convey linguistic information. In a dichotic-listening task, we used these novel stimuli as a means of disambiguating the relative contributions of linguistic and affective processing across the hemispheres. This method was applied to both children and adults with the goal of investigating the role of developing cognitive resource capacity on affective processing. Results suggest that children's limited computational resources influence how they process affective information and rule out attentional biases as a factor in children's perceptual asymmetries for nonlinguistic affective sounds. These data further suggest that investigation of perception of nonlinguistic affective sounds is a valuable tool in assessing interhemispheric asymmetries in affective processing, especially in parceling out linguistic contributions to hemispheric differences.

To study how perceptual asymmetries in the recognition of emotion reflect developmental changes in processing affective information, a fused rhyming dichotic word test with positive, negative, and neutral stimuli was administered to adults and children. Results suggested that the hemisphere in which affective information is initially processed affects the strength of perceptual asymmetry and that children's perceptual processing of emotional information is constrained by limited computational resources. Another experiment ruled out effects of volitional shifting of attention to emotional stimuli. These data further confirm that emotional processing involves integration of neural systems across brain regions, including distributed systems that support arousal and recognition. General developmental factors, such as processing capacity, contribute to the coordination of multiple systems responsible for processing emotional information.