Originally Authored by Tory L. Larsen, Emily J. Helder, and Michael E. Behen in Journal of Clinical and Experimental Neuropsychology
Abstract
The incidence of non-right-handedness was assessed among a sample of international adoptees. Neurocognitive and behavioral correlates to handedness were also examined among participants. A sample of 139 international adoptees (54 males; mean age at testing = 111.4 months ± 32.9 months) underwent a comprehensive neuropsychological evaluation, assessing verbal and visual reasoning, language, memory, attention, impulse control, processing speed, academic functioning,manual dexterity, and behavioral functioning. Over 26% of participants reported non-right-handedness. Non-right- and right-handers did not differ on demographic or orphanage specific variables. The groups were found to significantly differ on behavioral indices of attention and several neurocognitive variables, including visual memory, verbal memory, and manual dexterity of the dominant hand, with non-right-handers having worse performance. Possible mechanisms for these findings are discussed.
Keywords: International adoption; Handedness; Attention; Neuropsychological outcome; Deprivation
Introduction
The primary aim of the present research was to examine the prevalence of non-righthandedness among internationally adopted children. Additionally, right-handed and nonright-handed participants were compared, with the goal of describing the neurocognitive and behavioral profile of non-right-handed, internationally adopted children. The current study builds from previous research evaluating handedness and associated cognitive and behavioral challenges in nonadopted samples as well as research examining neuroanatomical findings in internationally adopted children.
Research has shown that children who experience early deprivation (ED) are at greater risk for developmental and behavioral impairments (Behen, Helder, Rothermel, Solomon, & Chugani, 2008). Studies often focus on children who were reared in institutions as these children are often deprived of adequate care and stimulation throughout the vital months and years of early development. Rutter, Kreppner, and O’Conner (2001) compared seven domains of functioning in children adopted from Romania before the age of 42 months and nondeprived domestically adopted children. Four domains—attachment problems, inattention/overactivity, quasiautistic problems, and cognitive impairment—were significantly more common in the Romanian children who experienced ED in the institutions in which they were reared than in children adopted domestically in infancy. Furthermore, Behen et al. (2008) examined the complete neurocognitive profile of ED children post adoption. They found that, of the 54 adoptees considered “globally intact” with regard to intelligence, 46% showed at least one area with absolute impairment. The most common types of impairment observed were executive function impairment (24%), language impairment (18%), memory impairment (17%), manual dexterity deficit (11%), and impairment in at least one area of achievement (5%).
Of particular interest here are the consistent findings of significantly increased rates of an inattentive/overactive (I/O) behavioral phenotype in children reared from birth in institutions. High incidence of I/O-type behavior in institutional populations was originally reported by Goldfarb (1943) who observed that 60% of children raised institutionally were restless and hyperactive as compared to only 7% of those raised in foster homes. More recently, Stevens et al. (2008) found that children reared in Romanian institutions and later adopted to the UK had significantly higher levels of I/O at age 11 than children adopted from within the UK. Additionally, the Stevens study found that the risk of developing an I/O phenotype was related to the duration of institutional privation, with risk increasing as the length of privation increased over 6 months. However, no additional risk was added as the duration increased past 24 months. Stevens et al. suggest that the occurrence of I/O following ED may be related to alterations in brain organization and function caused by early stressful experiences and lack of typically expected environmental stimulation.
An increased incidence of non-right-handedness has also been observed in populations with histories of ED. In the Behen et al. (2008) sample, 26% of the children institutionally reared reported either left- or mixed-handedness. This is well above the incidence reported in the general population. Based on review of many earlier studies, Hardyck and Petrinovich (1977) estimated that 8–10% of the population is left-handed: a range that the author states contains wide variability, from those who use both hands equally well but prefer their left, to those who are totally left-handed. More recently, Rodriguez et al. (2010) measured handedness in a large birth cohort in Northern Finland (N = 7,871). These authors found that 9.1% of the cohort reported non-right-handedness, with 8.0% reporting lefthandedness and 1.1% reporting mixed-handedness. Thus, there is evidence that children who have experienced early deprivation are more likely to be mixed- or left-handed than the general population.
Non-right-handedness has been found to be associated with a variety of mental health problems in children and adolescents. For example, significant associations have been observed between non-right-handedness and psychosis-related mental health issues (van der Hoorn et al., 2010). Attention-deficit/hyperactivity disorder (ADHD) symptoms have also been reported to relate to non-right-handedness. Rodriguez and colleagues (2010) followed 7,871 individuals in the Northern Finland Birth Cohort 1986 from birth through 16 years of age and found that mixed-handed adolescents were at increased risk for difficulties with inattention and hyperactivity while righthanders and left-handers were not. Much of Rodriguez and colleagues’ work seems to point to the associations between mixed-handedness and ADHD symptoms, though an earlier study found a link between left-handedness and total DSM– IV-defined (Diagnostic and Statistical Manual of Mental Disorders–Fourth Edition; American Psychiatric Association, 1994) ADHD symptoms and hyperactivity–impulsivity specifically (Rodriguez & Waldenstrom, 2008). It should be noted, however, that the same study also found stronger links between mixed-handedness and these and other ADHD symptoms. Taking into consideration this evidence, the relationship between mixed-handedness and symptoms of ADHD has been relatively well established in nondeprived samples, but the relationship between left-handedness and similar symptoms seems less clear. The present research intends to further investigate the association between non-right-handed children and ADHD symptoms, specifically in a sample of international adoptees—a relationship that may be driven by early experienced deprivation.
Children reared in orphanages often lack typical, experience-expectant stimulation (especially with regard to social interaction and language), which may affect the neural pruning and organization process that occurs in early development (Nelson, 2007). For example, diffusion tensor imaging has shown that children who experienced ED have significantly more frontostriatal connections than normal control children (Behen et al., 2009). It is hypothesized that excess frontostriatal connections are pruned away in home-reared children who receive typical experience-expectant stimulation. Thus, it is possible that this lack of stimulation may result in anomalous organization and non-right-handedness. Non-right-handedness has been associated with atypical laterality in the brain (Geschwind & Behan, 1982). Although asymmetries relating to handedness would theoretically be expected in the motor cortex, the strongest associations can be made between handedness and asymmetries in the language-processing structures of the brain (Beaton, 1997; Toga & Thompson, 2003). Research using functional magnetic resonance imaging (fMRI) has shown that left- and mixed-handed people are more likely to display atypical lateralization of language than righthanders (Szaflarski et al., 2002). Utilizing fMRI, Szaflarski and colleagues (2002) found that 22% of non-right-handers showed symmetrical or strong right-hemisphere language lateralization, as compared to the 6% of right-handers who are reported to show similar lateralization patterns (Springer et al., 1999).
Although studies have examined the relationship between non-right-handedness and attention and learning problems in a nonadopted population (Rodriguez et al., 2010), to our knowledge no research has examined these associations in an ED population. Therefore, our aim for the present study is to assess the incidence of nonright-handedness in a sample of globally intact, internationally adopted children with histories of ED, as well as to determine whether non-righthandedness is associated with demographic or deprivation-specific (e.g., length of institutionalization) characteristics and neuropsychological functioning. We expected to see this increased incidence of non-right-handedness among our sample of adoptees. Furthermore, in line with Rodriguez et al.’s (2010) findings, we also expected to find that non-right-handers would show greater attention problems on both neuropsychological assessments and parent reports of behavioral functioning.
Method
Particpants
Participants consisted of 139 children (mean age at testing = 111.4 months, SD = 32.9 months, range = 39 to 216 months; 54 males/85 females) all of whom were raised from birth in institutions located in South/East Asia (China, Vietnam), Northern Asia (Russia, Kazakhstan), Eastern Europe (Armenia, Bulgaria, Poland, Romania, Slovakia, Ukraine), or Central/South America (Bolivia, Guatemala) and later adopted into the United States. All participants were separated from their biological mother at birth and were placed into orphanages immediately upon release from the hospital. Mean duration of time spent in the orphanage was 23.9 months (SD = 16.4 months, range = 2 to 81 months), and mean duration of time spent in the adoptive home was 85.6 months at the time of participation in the study (SD = 36.2 months, range = 3 to 211 months). Thirty-five percent (N = 49, mean length of time spent in the orphanage = 18.4 months) of the sample had been reared in South/East Asian orphanages, 34.5% (N = 48, mean length of time spent in the orphanage = 25.2 months) in North Asian orphanages, 27.3% (N = 38, mean length of time spent in the orphanage = 29.6 months) in Eastern European orphanages, and 2.2% (N = 3, mean length of time spent in the orphanage = 15 months) in Central/South American orphanages. Most adoptive parents were college educated (mother’s mean = 16.43 years, SD = 2.0 years, father’s mean = 16.52 years, SD = 2.6 years). Of the 139 participants, 24.5% (N = 34) reported left-handedness, 2.2% (N = 3) reported mixed-handedness, and 73.4% reported right-handedness. Given the small number of participants reporting mixed-handedness, participants were grouped as either right-handed (N = 102) or non-right-handed (N = 37).
These participants were recruited through community contacts previously established by several members of the Children’s Hospital of Michigan PET Center. These contacts included postadoptive service agencies serving families of children adopted internationally and newsletters for parents of internationally adopted children. Inclusion criteria for the early deprivation group were: age 6–18 years, English speaking, and regular school attendance by parent report. In order to minimize the occurrence of major confounding factors with known neurobiological effects, families expressing interest in participating underwent screening and were not included in the study if any of the following were present: (a) prematurity (<37 weeks), low birthweight (<2,500 g), or pre- or perinatal difficulties as indicated on medical records from the orphanage and/or adoptive parent report (Wolke & Meyer, 1999); (b) current or historical major medical problems (i.e., head injury, stroke, hearing loss) as indicated by parent report; (c) epilepsy; (d) evidence of focal neurological impairment on neurologic examination; and/or (e) evidence of exposure to alcohol and/or other substances during pregnancy. Evidence of alcohol exposure was assessed by a neurologist using the criteria outlined by L. C. Miller et al. (2006) with scores above 12 considered as high phenotypic suggestion of fetal alcohol syndrome. Furthermore, an additional exclusion criterion was a full-scale IQ of less than 2 standard deviations below the normal mean (<70) on the Wechsler Intelligence Scale for Children–Third Edition (WISC–III; Wechsler, 1991), as these children were classified as globally impaired. Twentythree children that were originally screened as possible participants were not included in the study sample (N = 139) due to these exclusion criteria.
Measures
A comprehensive battery of measures was administered to each participant that evaluated a wide variety of neuropsychological domains. Intelligence was assessed using the WISC–III (Wechsler, 1991). The Verbal Comprehension Index, Perceptual Organizational Index, Freedom from Distractibility Index, and Processing Speed Index were used in the current study to assess verbal reasoning, visual reasoning, working memory, and processing speed, respectively. Language functioning was assessed using the Clinical Evaluation of Language Fundamentals–III (CELF–III; Semel, Wiig, & Secord, 1995). The Receptive Language Index, composed of several subtests that require participants to complete tasks such as following verbal commands by pointing and categorizing words that are presented verbally, was used to assess receptive language. The Expressive Language Index, in which participants complete tasks such as generating sentences about pictures using a stimulus word or expressive fluency tasks, was used to assess expressive language. Memory was assessed utilizing the Wide Range Assessment of Memory and Learning (WRAML; Sheslow & Adams, 1990). The Verbal Memory Index (including list learning, story learning, and repetition of number and letter strings) was used to assess verbal memory. The Visual Memory Index (including memory for designs, pictures, and visual motor patterns) was used to assess visual memory. Attention and impulse control were assessed using the Gordon Diagnostic System (GDS; Gordon, 1983). This roughly 9-min task requires participants to respond with a button press to target stimuli while withholding a response to nontarget stimuli. The participant’s ability to correctly respond to target stimuli was used as a measure of sustained attention (Vigilance Hit Score), and their number of responses to nontarget stimuli was used as a measure of impulse control (Vigilance False Alarms Score). Academic achievement was measured using the Wide Range Achievement Test– III (WRAT–III; Wilkinson, 1993). A composite score of performance on academic tasks including single word reading, spelling of words, and math calculation tasks was used. Manual dexterity was assessed using the Grooved Pegboard (Matthews & Klove, 1964), a speeded task that requires participants to place key-shaped pegs into a pegboard with randomly positioned slots. Behavioral functioning was assessed by parent report, utilizing the Behavioral Assessment Scales for Children (BASC), parent report form (Reynolds & Kamphaus, 1992). This comprehensive questionnaire requires parents to rate the frequency of their child’s behavior on a 4-point Likert scale and contains items assessing a range of externalizing and internalizing difficulties. The BASC scores allow for comparison with ageand gender-matched controls with authors providing cutoffs for “at risk” and “clinically elevated” difficulties.
Procedure
All participants and their parents were seen during a single day appointment, which consisted of three parts: a neurological examination, a neuropsychological evaluation, and a parental interview. All of the children first received a standard neurological examination to assess for exclusionary criteria such as phenotypic evidence of alcohol exposure (see specific cutoffs above) and focal neurologic impairment, as well as to ascertain head circumference measurements. Following the neurological exam, participants received a complete neuropsychological evaluation, which covered all of the domains previously described. Each appointment also included a social–historical interview with the child’s adoptive parent(s) to gain information that they might have about the child’s birth status and preadoption medical history.
Results
Group Differences on Demographic Variables
Table 1 presents the differences between the righthanded and non-right-handed groups on various demographic variables. Chi-square tests showed that the groups did not significantly differ in terms of distributions for gender and region of adoption. Additionally, independent-samples t tests showed that the groups did not significantly differ in terms of other demographic characteristics, including current age, time spent in an orphanage, time spent in the adoptive home, body mass index, head circumference, and parent education.
Group Differences on Neurocognitive Profiles
T tests were used to assess the differences between the right-handed and non-right-handed groups on neurocognitive variables (see Table 2, top half). To control for multiple comparisons, a Bonferroni correction was used, and alpha levels were accordingly adjusted to .004. Additionally, due to significant Levene’s tests for the verbal memory domain, corrected values were reported. The right- and nonright-handed groups were found to significantly differ on both verbal and visual memory, t(70.22) = 3.266, p = .002, and t(138) = 2.96, p =.004, respectively. Examination of the means shows that the non-right-handed group did significantly worse than the right-handers on both memory indices. The groups also differed significantly on fine motor dexterity of the dominant hand, t(138) = 3.17, p = .002. Examination of the means again shows that the non-right-handed group did significantly worse than the right-handed group on the dominant hand motor task. The groups did not significantly differ at the adjusted level on any of the other neurocognitive variables, though several were significant at the traditional level of p <.05.
Group Differences on Behavioral Indices
T tests were used to assess the differences between the groups on nine parent-reported behavioral indices from the BASC (see Table 2, bottom half). Again a Bonferroni correction was used to control for multiple comparisons. Alpha levels were adjusted to .006. The Levene’s corrected values are reported for the depression domain due to lack of homogeneous variance between groups for this variable. Right- and non-right-handers were found to differ significantly on parent-reported attention problems, t(138) = –3.50, p =.001. Examination of the means revealed that attention problems in non-right-handed children were reported as worse than the attention problems in right-handed children. The right and non-right-handed groups did not significantly differ on any other behavioral variables.
Discussion
The primary aims of the present study were to assess the incidence of non-right-handedness in a sample of children with histories of early severe deprivation, as well as to determine whether non-right-handedness was associated with neuropsychological functioning. To our knowledge, this is the first study to examine the incidence and associations of non-right-handedness in an internationally adopted, ED sample. More than 26% of our sample reported non-right-handedness, well above the percentages reported by other studies examining more generalized populations (Hardyck & Petrinovich, 1977; Rodriguez et al., 2010). Comparison of right- and non-right-handed groups showed that they did not differ on any demographic (e.g., age, gender, body mass index) or deprivationspecific (e.g., length of time in orphanage) variables. This suggests that the differences in neurocognitive and behavioral functioning observed between the right-handed and non-right-handed participants are not due to extraneous factors, such as one group spending more time in depriving environments or less time in the enriched environment of the adoptive home.
Due to the relatively small size of our sample, and the rarity of mixed-handed individuals, we were not able to analyze mixed-handers and left-handers as independent groups. Only 2.2% (n = 3) of our adoptees presented as mixedhanded. This was a slightly higher percentage than Rodriguez et al. (2010) reported (1.1 %). However, Rodriguez and colleagues had a much larger sample of over 7,800 children. Thus, 1.1% still yielded 87 mixed-handed individuals—enough to analyze as a separate group. Keeping in mind our sample size issues, the present study did find that non-right-handedness is associated with several neurocognitive and behavioral difficulties.
Results revealed that non-right-handers performed worse than right-handers on assessments of verbal memory, visual memory, and fine motor dexterity of the dominant hand. Right- and non-right-handers did not significantly differ on the attention assessments in our battery, although such differences had been predicted. Examination of the means and standard deviations for the sustained attention and impulsivity variables shows that, although the non-right-handers performed worse on each variable, both right- and non-righthanders performed very poorly and had significant amounts of variability. Nevertheless, it is important to note that the trends are in the predicted direction. In the current study, however, the non-righthanders were found to have greater problems with attention on parent reports of behavior than righthanders. This corresponds well with Rodriguez et al.’s (2010) findings that mixed-handed individuals from a large birth cohort were at a greater risk for attention and hyperactivity problems than right-handers. Assessment of these behavioral problems in the Rodriguez study only involved parent and teacher reports; no direct assessments were used. Thus, the method in which non-right- and right-handers were found to differ with regards to attention problems in the current study closely mirrors the methods that Rodriguez et al. used. Several other variables, such as full-scale IQ, visual reasoning, working memory, processing speed, and nondominant fine motor dexterity, were significant at more traditional alpha levels, but did not meet significance at the more conservative alpha level that was chosen due to multiple comparisons.
To our knowledge, no previous studies have shown a link between non-right-handedness and memory deficits. The non-right-handers in our sample, however, showed significantly greater verbal and visual memory deficits than the right-handers. A possible explanation for this difference, however, comes from the specific assessment instrument that was used. The children in our sample were all tested using the Wide Range Assessment of Memory and Learning (WRAML). Some of the subtests that comprise both the verbal and visual memory indices have a very strong attention and working memory load. Dewey, Kaplan, and Crawford (1997) performed a principal components factor analysis on the WRAML in separate groups of individuals with ADHD, individuals with reading disability, and a control group. They found that an attention/concentration factor emerged for all three groups that contained the number/letter and sentence memory subtests, both of which were considered part of the verbal memory index. Furthermore, the newly revised WRAML–2 contains a separate attention/concentration index, which includes the number/letter memory and finger window (part of the visual memory index on the WRAML) subtests (Adams & Sheslow, 2003). Thus, it seems that more than half of the subtests that comprised the verbal and visual memory indices could be characterized as measuring attention and concentration more than memory per se. The differences we observed between non-rightand right-handers on these indices may then be explained by previous findings that have shown that non-right-handers have greater problems with attention than right-handers (Rodriguez et al., 2010).
The non-right-handed individuals in the present study were also found to significantly differ from the right-handers on manual dexterity of the dominant hand. Specifically, non-right-handers performed worse than right-handers on the motor task when asked to use only their dominant hand. Research focusing on survivors of childhood bacterial meningitis has shown that this population had an increased incidence of left-handedness (Ramadhani et al., 2006). Furthermore, the lefthanded survivors had worse neurodevelopmental outcomes than non-left-handed survivors and, of importance here, had slower manual speed of the dominant hand. The authors speculate that the brain damage caused by the meningitis causes a pathological shift in lateralization, so children who are “innately” right-handed actually give preference to their left hand. The same mechanism may be at work in the present research; the stresses of early severe deprivation may cause “innately” righthanded children to prefer their left hand. Since these individuals are not “innately” left-handed, they may demonstrate deficits on tests of manual dexterity when compared to right-handers who are “innately” right-handed.
The increased incidence of non-right-handedness in this sample is notable and may be related to abnormal neuroanatomical development. This abnormal development could theoretically be caused by a variety of factors. Previous research has suggested that the orphanage environment may result in the lack of experience/expectant behavior (motor, language, and social) that guides the pruning and apoptosis process, thus resulting in structural differences in the way that internationally adopted children’s brains develop (Behen et al., 2009; Eluvathingal et al., 2006; Govindan, Behen, Helder, Makki, & Chugani, 2009). Supporting this, other research in different samples has linked non-right-handedness with suspected early brain insults (i.e., J. W. Miller, Jayadev, Dodrill, & Ojemann, 2005). Additionally, the orphanage experience has been found to result in abnormalities in the stress response system (i.e., Gunnar, Morison, Chisholm, & Schuder, 2001), which has also been linked to neuroanatomical changes later in life (i.e., Bremner, Krystal, Southwick, & Charney, 1995). Also, maternal stress and depression symptoms during pregnancy has been linked to increased non-right-handedness and attention-deficit disorder symptoms in a prospective, population based study (Rodriguez & Waldenstrom, 2008).
Both non-right-handedness and an I/O phenotype may be related to similar processes of abnormal brain development. International adoptees may be at an increased risk of this atypical development because of the lack of expected stimulation that they experience in the early stages of life. Therefore, as Rodriguez et al. (2010) posited between mixed handedness and atypical cerebral lateralization, non-right-handedness may be an endophenotype (i.e., an intermediate phenotype) that connects abnormal brain development and problems with behavioral and neurocognitive variables.
In summary, children who experienced earlysevere deprivation and were later adopted showed an increased incidence of non-right-handedness that was related to several neurocognitive and behavioral deficiencies. Mechanisms for these findings may involve pre- and postnatal stress and insult, lack of expected environmental stimulation, and adverse neural-pruning processes. It is important here to note the limitations of the present research, the most prominent of which is the selfselection of our sample. Our participants were recruited through community connections with postadoptive service agencies; thus it is possible that the parents of our participants chose to participate in hopes that we could provide feedback regarding concerns that they had about their child’s development. However, our right-handed participants serve as somewhat of a control in that they were not adopted at older ages or had less time in their adoptive home. The other prominent limitation present here is our relatively small sample size. Because of this we were unable to examine mixed-handedness as its own variable—instead we had to combine both mixed- and left-handers into one “non-right-handed” category. Therefore, we were unable to fully investigate Rodriguez and colleagues’ (Rodriguez et al., 2010; Rodriguez & Waldenstrom, 2008) findings that impairments in non-right-handers are actually being driven nearly completely by mixed-handers.
Future research in international adoptees may be helpful in serving to replicate our results of increased incidence of left-handedness and also examine connections between handedness and neurocognitive and behavioral functioning using alternative assessment tools. These investigations should also utilize larger sample sizes so that the differences between mixed- and left-handers can be teased out more adequately. Additionally, future research that utilizes imaging techniques (such as diffusion tensor imaging) may be helpful in examining some of the hypothesized mechanisms for the observed differences.
References
Adams, W., & Sheslow, D. (2003). WRAML 2: Wide Range Assessment of Memory and Learning. Lutz, FL: Psychological Assessment Resources. American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.
Beaton, A. A. (1997). The relation of planum temporale asymmetry and morphology of the corpus callosum to handedness, gender, and dyslexia: A review of the evidence. Brain and Language, 60, 255–322.
Behen, M. E., Helder, E., Rothermel, R., Solomon, K., & Chugani, H. T. (2008). Incidence of specific absolute neurocognitive impairment in globally intact children with histories of early severe deprivation. Child Neuropsychology, 14, 453–469.
Behen, M. E., Muzik, O., Sapota, A. S., Wilson, B. J., Pai, D., Hua, J., et al. (2009). Abnormal fronto-striatal connectivity in children with histories of early deprivation: A diffusion tensor imaging study. Brain imaging and Behavior, 3, 292–297.
Bremner, J. D., Krystal, J. H., Southwick, S. M., & Charney, D. S. (1995). Functional neuroanatomical correlates of the effects of stress on memory. Journal of Traumatic Stress, 8, 527–553.
Dewey, D., Kaplan, B. J., & Crawford, S. G. (1997). Factor structure of the WRAML in children with ADHD or reading disabilities: Further evidence of an attention/concentration factor. Developmental Neuropsychology, 13, 501–506.
Eluvathingal, T. J., Chugani, H. T., Behen, M. E., Juhasz, C., Muzik, O., Maqbool, M., et al. (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics, 117, 2093–2100.
Geschwind, N., & Behan, P. (1982). Left-handedness: Association with immune disease, migraine, and developmental learning disorder. Proceedings of the National Academy of Sciences, USA, 79, 5097–5100.
Goldfarb, W. (1943). The effects of early institutional care on adolescent personality. Journal of Experimental Education, 12, 107–129.
Gordon, M. (1983). The Gordon Diagnostic System. DeWitt, NY: Gordon Systems.
Govindan, R. M., Behen, M. E., Helder, E., Makki, M. I., & Chugani, H. T. (2009). Altered water diffusivity in cortical association tracts in children with early deprivation identified with tract-based spatial statistics (TBSS). Cerebral Cortex, 20, 561–569.
Gunnar, M. R., Morison, S. J., Chisholm, K., & Schuder, M. (2001). Salivary cortisol levels in children adopted from Romanian orphanages. Development and Psychopathology, 13, 611–628.
Hardyck, C., & Petrinovich, L. F. (1977). Lefthandedness. Psychological Bulletin, 84, 385–404.
Matthews, C. G., & Klove, K. (1964). Instruction manual for the Adult Neuropsychology Test Battery. Madison, WI: University of Wisconsin Medical School.
Miller, J. W., Jayadev, S., Dodrill, C. B., & Ojemann, G. A. (2005). Gender differences in handedness and speech lateralization related to early neurologic insults. Neurology, 65, 1974–1975.
Miller, L. C., Chan, W., Litvinova, A., Rubin, A., Comfort, K., Tirella, L., et al. (2006). Fetal alcohol spectrum disorders in children residing in Russian orphanages: A phenotypic survey. Alcoholism, Clinical and Experimental Research, 30, 531–538.
Nelson, C. A. (2007). A neurobiological perspective on early human deprivation. Child Development Perspectives, 1, 13–18.
Ramadhani, M. K., Koomen, I., Grobbee, D. E., van Donselaar, C. A., van Furth, A. M., & Uiterwaal, C. S. (2006). Increased occurrence of left-handedness after severe childhood bacterial meningitis: Support for the pathological left-handedness hypothesis. Neuropsychologia, 44, 2526–2532.
Reynolds, C. R., & Kamphaus, R. W. (1992). Behavior Assessment System for Children. Circle Pines, MN: American Guidance Service.
Rodriguez, A., Kaakinen, M., Moilanen, I., Taanila, A., McGough, J. J., Loo, S., et al. (2010). Mixedhandedness is linked to mental health problems in children and adolescents. Pediatrics, 125, 340–348.
Rodriguez, A., & Waldenstrom, U. (2008). Fetal origins of child non-right-handedness and mental health. Journal of Child Psychology and Psychiatry, 49, 967–976.
Rutter, M. L., Kreppner, J. M., & O’Connor, T. G. (2001). Specificity and heterogeneity in children’s responses to profound institutional privation. British Journal of Psychiatry, 179, 97–103.
Sattler, J. (2001a). Assessment of children: Behavioral applications (4th ed.). San Diego, CA: Sattler Publications.
Sattler, J. (2001b). Assessment of children: Cognitive applications (4th ed.). San Diego, CA: Sattler Publications.
Semel, W., Wiig, E. H., & Secord, W. A. (1995). Clinical Evaluation of Language Fundamentals (3rd ed.). San Antonio, TX: The Psychological Corporation.
Sheslow, D., & Adams, W. (1990). Wide Range Assessment of Memory and Learning. Wilmington, DE: Wide Range.
Springer, J. A., Binder, J. R., Hammeke, T. A., Swanson, S. J., Frost, J. A., Bellgowan, P. S., et al. (1999). Language dominance in neurologically normal and epilepsy subjects: A functional MRI study. Brain, 122, 2033–2046.
Stevens, S. E., Sonuga-Barke, E. J., Kreppner, J. M., Beckett, C., Castle, J., Colvert, E., et al. (2008). Inattention/overactivity following early severe institutional deprivation: Presentation and associations in early adolescence. Journal of Abnormal Child Psychology, 36, 385–398.
Szaflarski, J. P., Binder, J. R., Possing, E. T., McKiernan, K. A., Ward, B. D., & Hammeke, T. A. (2002). Language lateralization in left-handed and ambidextrous people. Neurology, 59, 238–244.
Toga, A. W., & Thompson, P. M. (2003). Mapping brain asymmetry. Nature Reviews Neuroscience, 4, 37–48.
van der Hoorn, A., Oldehinkel, A. J., Ormel, J., Bruggeman, R., Uiterwaal, C. S., & Burger, H. (2010). Non-right-handedness and mental health problems among adolescents from the general population: The Trails Study. Laterality, 15, 304–316.
Wechsler, D. (1991). Wechsler Intelligence Scale for Children–Third Edition. San Antonio, TX: The Psychological Corporation.
Wilkinson, G. S. (1993). Wide Range Achievement Test 3. Wilmington, DE: Wide Range.
Wolke, D., & Meyer, R. (1999). Cognitive status, language attainment, and pre-reading skills of 6-year-old very preterm children and their peers. Developmental Medicine and Child Neurology, 41, 94–109.