The primary goal of this study was to determine which cognitive processes differentiated children who experienced early institutional deprivation and neglect. Post-institutionalized internationally adopted children differed from both groups of comparison children on tests of visual memory and attention, as well as visually-mediated learning and inhibitory control. Yet, these children performed at developmentally appropriate levels on similar tests where auditory processing was also involved. These children also performed well on tests of executive processes involving rule acquisition and manipulation and planning.
This study was not designed to show precisely which neural circuits are affected by early experience, but the tasks that PI children had difficulty with do provide a useful guide for specifying neuroanatomical substrates that can be more directly examined in future studies. Below, we briefly highlight areas of brain circuitry associates with these tasks. Performance on the Memory for Faces task reflects an interaction between prefrontal cortex (PFC) and stimulus-specific visual cortical association areas that mediate visual working memory. The neurophysiological models of visual working memory developed in the nonhuman primate also holds for humans, based upon event-related fMRI (ER-fMRI) studies of facial delay-recognition task similar to the one used in the present study (Druzga & D’Esposito, 2003
). Memory tasks such as the one used in the present study involve both visual memory and visual perception. But there is not yet agreement in the field about the neural bases of these processes. Some data suggest that visual memory and visual perception are associated with common neural substrates (Slotnick, 2004
), whereas other data suggest that right medial temporal-lobe structures are critically involved in retention, but not in the perception, of new faces (Crane & Milner, 2002
Spatial Working Memory is a test of the child’s ability to retain spatial information and to manipulate remembered items in working memory and also assesses heuristic strategy. The task is considered a sensitive measure of frontal lobe dysfunction based upon studies of nonhuman primates and patients with frontal lobe damage (Owen et al., 1990
; Owen et al., 1995
;Owen, Morris, et al., 1996
; Passingham, 1985). Owen, Evans, & Petrides (1996)
used positron emission tomography with magnetic resonance imaging to demonstrate the existence, within the human brain, of two functionally distinct subdivisions of the lateral frontal cortex, which subserve different aspects of spatial working memory. When the spatial working memory task required the organization and execution of a sequence of spatial moves retained in working memory, significant changes in blood flow were observed in ventrolateral frontal cortex (area 47) bilaterally. By contrast, when the task required active monitoring and manipulation of spatial information within working memory, additional activation foci were observed in mid-dorsolateral frontal cortex (areas 46 and 9). Both of these processing stages were required to successfully complete a spatial working memory task (Owen, Evans, et al., 1996
). Another study also linked poor performance on the CANTAB Spatial Working Memory task in children to reduced dorsolateral prefrontal cortex using fMRI (Luna et al., 2002
It is difficult to link performance on tests of Visual Attention to distinct neural systems. A recent study used ER-fMRI to measure brain activity as subjects oriented visual attention to an upcoming target. This activation was lateralized to the left hemisphere and reflected a widely distributed network that included (a) structures in parietal and temporal cortices and thalamus usually associated with selective attention, (b) ventral-stream object processing structures in occipital, inferior-temporal, and parahippocampal cortex, and (c) structures in medial-and dorsolateral-prefrontal cortex associated with cognitive control (Arrington et al., 2000
). In visual attention tasks, subjects will undoubtedly make errors and need to reorient to targets. This same study revealed that brain areas specific to attentional reorientation were right-lateralized and included posterior temporal and inferior parietal regions, as well as prefrontal regions that likely subserve control processes related to inhibition of inappropriate responding (Arrington et al., 2000
). In sum, selective visual attention results from distributed brain activity that includes maintenance of the selected object’s representation accompanied by suppression of response to ignored objects (Duncan, 1993
; Farah, 1990
; Phafet et al., 1990), with control of these processes mediated by the medial dorsolateral prefrontal cortex (DL PFC).
Paired Associates Learning is a stringent test for visual episodic memory and associative learning (Sahakian & Owen, 1992
). To perform well, children had to learn the locations of a progressively increasing number of abstract stimuli. Although such a complex behavioral task undoubtedly draws upon widely distributed neural systems, ER-fMRI suggests that successful performance on this type of task relies heavily upon medial temporal lobe connections to the frontal lobe (Aizenstein et al., 2000
). Similarly, the Knock and Tap test cannot be mapped onto discrete circuitry. The test measures the child’s ability to inhibit immediate impulses evoked by visual stimuli that conflict with a verbal direction. The child learns a pattern of motor responses and then must maintain that cognitive set and inhibit the impulse to imitate the examiner’s action.
Taken together, the present data suggest delayed maturation of select aspects of frontal circuitry, and perhaps reduced functional connectivity of frontal cortex with other neocortical and subcortical regions, plays a key role in scholastic difficulties among children who experienced early institutionalized deprivation and neglect. Indeed, regions of the PFC have long been associated with cognitive processes similar to the ones assessed in this study (Fletcher & Henson, 2001
; Owen et al., 1996
). Studies in nonhuman primates, lesion studies, as well as functional neuroimaging studies in humans, have documented that DLPFC is crucial for maintaining and manipulating information in ways assessed by the tasks used here (Carlson et al., 1998
; Fuster, 2000
; Goldman-Rakic, 1988
; McCarthy et al., 1994
; Owen, Evans, &Petrides, 1996
; Pierrot-Deseilligny et al., 1995
; Sweeney et al., 1996
The distinction between the performance of PI and EA children suggests (but does not prove) that the ontogenesis of the prefrontal cortex also includes an extensive postnatal interval. Such an interpretation is consistent with animal studies which reveal, for example, that the thickness of the prefrontal cortex of the rat brain is not maximal until post natal day 20, which marks the beginning of the postweaning period (e.g. roughly equivalent to adolescence in humans; Vincent et al., 1995). Indeed, PI children are often noted to have problems in attention regulation and emotional control, functions presumably influenced by the development of the PFC and its distributed systems (see review by Gunnar, 2001
; Shallice et al., 2002
). Consistent with this view, Sanchez et al. (1998)
studied rhesus monkeys that were socially deprived between 2 and 12 months of age. These monkeys exhibited cognitive deficits that had also been noted in earlier studies (e.g., Harlow et al., 1971
). Sanchez’s MRI studies revealed that the animals’ performance on executive function tasks was correlated with decreased neuronal development of prefrontal, medial temporal, and amygdala substrates. Studied two years later, these monkeys exhibited increased abnormalities in the prefrontal cortex that was related to the monkeys’ performance on learning and working memory tasks (Sanchez et al., 2003). In a separate study, Mathew et al. (2003)
reported neuropathological alterations in the prefrontal cortex of adult macaques with early adverse experience.
There are a number of features of the present study that are important to consider in interpreting these data. First, as described earlier, we excluded children with clear developmental delays or indications of fetal alcohol exposure, which would have artificially exaggerated group performance deficits. By avoiding a situation where a subset of PI children may be experiencing global cognitive delays, we were also able to detect specific patterns of processing deficits. In general, executive function tasks are sensitive to perturbations in children’s lives, but effects on these tasks are not specific to certain situations or conditions. If we observed broad or diffuse cognitive deficits in the PI sample, it would not be possible to rule out general attentional, IQ, motivational, motor, or emotional problems as driving children’s performance. Yet, in the present study we observed that on a majority of tasks, PI children displayed performance equivalent to their peers, which permits stronger interpretation of those specific areas where deficits emerged. Second, this sample of children represents families who volunteered to participate in research; it may be the case that parents who believed their children were doing particularly well or poorly were more likely to participate. Yet, such sampling issues—if they exist—do not readily explain the pattern of results observed in this study. In addition, our unusual sampling procedures (see Hellerstedt et al., 2008
) likely resulted in a group of children that are both diverse and representative.
The study of children reared in atypical situations requires opportunistic approaches that are also fraught with interpretive challenges. Our requirement that the EA group be adopted before 8 months of age and that these children had to spend less than 2 months in institutional care meant that none of the EA children were drawn from Eastern Europe, where adoption processes take more time. Most of the EA children spent most of their pre-adoptive lives in foster care overseas, an option that did not exist in Eastern Europe between 1990 and 1998, when the children that we tested were adopted. It is likely that prenatal conditions were less optimal for children who end up being placed in orphanage or institutional care overseas than for children born and raised in their families of origin in the United States. In part, the inclusion of a group of children adopted internationally with little or no institutional experience partly addressed this problem. We obtained birth weight data on the majority of both EA and NA children, and found, as might be expected, that the EA children were lower in birth weight than the NA children. Although we were only able to obtain birth weight data on 41% of the PI children, there was no evidence that birth weight differentiated PI from EA children. While we must be cautious in interpretation of these data because we lack evidence on the reliability of the information and are missing substantial data for the PI children, the pattern of data suggest that EA and PI children tended to experience prenatal environments that were impoverished. This tends to clarify, but not resolve, the issue of whether pre versus postnatal environmental impacts influenced the outcomes we examined.
In terms of the tasks administered to children, it is critical that measurement involves a sufficient level of task difficulty relative to the ability level of participants. In this regard, the specific tasks used in this study are particularly useful. For example, the test of spatial working memory ability and paired associates learning systematically varies the working memory load, which increases the amount of information that needs to be remembered and the number of trials over which it needs to be maintained. The children’s pattern of performance across the tasks that we administered did not reveal clear performance deficits on auditory memory and attentional tasks. One possibility is that the deficits observed here are a function of how much information needs to be kept active in working memory over time, and how precisely that information needs to be encoded. At the same time, firm conclusions about neural activity cannot be made based solely on behavioral data. However, these data do underscore the need to employ specific assessments that have been used in imaging and lesion studies and which may allow more fine-grained analysis of the impact of institutional neglect on neurobehavioral development.
Why did the PI children perform better on tasks that relied primarily on auditory, as compared with visual, information? One possibility is that visual development is more vulnerable to post-natal influences. The auditory system starts functioning during the last trimester of gestation (Birnholz & Benaceraff, 1983), whereas the visual system does not start functioning until after birth. Thus, both visual and auditory functional
development reflect experience-dependent processes; the difference is that auditory experience starts before visual experience, when the brain is at a different point in its development (Cf., Saffran, Werker, & Werner, 2006; Kellman & Arterberry, 2006). Sloutsky and colleagues (Robinson & Sloutsky, 2004
; Sloutsky & Napolitano, 2003
) have demonstrated that young children, unlike adults, exhibit auditory dominance. This may reflect earlier maturation of the auditory system relative to the visual system. It may also be the case that attentional processes more easily engage some stimulus properties. For example, auditory stimuli are serial, transient events that must be perceived quickly whereas visual stimuli are presented episodically for longer periods of time. Thus, attentional systems may allocate more resources to transient relative to stable stimuli. Similarly, Posner, Nissen, and Klein (1976)
proposed that attention to visual stimuli must be learned, whereas attention to auditory stimuli is more automatic. Also consistent with the argument that post-natal experience is more likely to influence visual processing, Maurer and colleagues (1999)
have demonstrated that the neural circuitry responsible for adults’ face expertise is not pre-specified, but requires early visual experience (see also Nelson, 2001; Pascalis, de Haan, & Nelson, 2005). Because infants have poor visual acuity, their cortices are only exposed to low spatial frequency. Thus, early exposure to visual information sets up the neural architecture for more complex visual processing. These studies have demonstrated that when visual input is delayed by as little as two months, permanent visual deficits result (Le Grand et al., 1999
; Le Grand, Mondloch, Maurer, and Brent, 2003
; Maurer et al., 1999
Models of the role of experience in neural development, and the mounting information on molecular processes in neural plasticity, indicate that neural activities (i.e., activity-dependent processes) are critical to brain development (see Fox, Levitt, & Nelson, 2008
). This implies that in addition to the stimuli available in the environment, active engagement of the environment may be essential in order for some aspects of cognitive development to occur. While these opportunities abound in typical human rearing environments, institutionalized child rearing may restrict the kinds of dynamic experiences and input necessary for some aspects of neurobehavioral development. It is hoped that the more we understand about the specific aspects of neurodevelopment impacted by early deprivation, the more we can focus on identifying targeted intervention and training experiences that would optimize these children’s outcomes.