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The impact of childhood deprivation on adult neuropsychological functioning is associated with ADHD symptom persistence

Published online by Cambridge University Press:  18 May 2020

Dennis Golm
Affiliation:
Centre for Innovation in Mental Health, School of Psychology, University of Southampton, Southampton, UK
Sagari Sarkar
Affiliation:
Cognitive Neuroscience & Neuropsychiatry Section, University College London, London, UK
Nuria K. Mackes
Affiliation:
Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Graeme Fairchild
Affiliation:
Department of Psychology, University of Bath, Bath, UK
Mitul A. Mehta
Affiliation:
Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK
Michael Rutter
Affiliation:
MRC Social Genetic & Developmental Psychiatry Centre, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK
Edmund J. Sonuga-Barke
Affiliation:
Department of Child and Adolescent Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, London, UK Department of Child & Adolescent Psychiatry, Aarhus University, Aarhus, Denmark
Corresponding

Abstract

Background

Institutional deprivation in early childhood is associated with neuropsychological deficits in adolescence. Using 20-year follow-up data from a unique natural experiment – the large-scale adoption of children exposed to extreme deprivation in Romanian institutions in the 1980s –we examined, for the first time, whether such deficits are still present in adulthood and whether they are associated with deprivation-related symptoms of attention-deficit/hyperactivity disorder (ADHD) and autism spectrum disorder (ASD).

Methods

Adult neuropsychological functioning was assessed across five domains (inhibitory control, emotion recognition, decision-making, prospective memory and IQ) in 70 previously institutionalized adoptees (mean age = 25.3, 50% female) and 22 non-deprived UK adoptees (comparison group, mean age = 24.6, 41% female). ADHD and ASD symptoms were assessed using parent-completed questionnaires.

Results

Early institutionalization was associated with impaired performance on all tasks in adulthood. Prospective memory deficits persisted after controlling for IQ. ADHD and ASD symptoms were positively correlated. After controlling for ASD symptoms, ADHD symptoms remained associated with deficits in IQ, prospective memory, proactive inhibition, decision-making quality and emotion recognition. ASD symptoms were not independently associated with neuropsychological deficits when accounting for their overlap with ADHD symptoms. Multiple regression analysis revealed that the link between childhood deprivation and adult ADHD symptoms was statistically explained by deprivation-related differences in adult IQ and prospective memory.

Conclusions

These results represent some of the most compelling evidence to date of the enduring power of early, time-limited childhood adversity to impair long-term neuropsychological functioning across the lifespan – effects that are linked specifically to deprivation-related adult ADHD symptoms.

Type
Original Articles
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

The ERA young adult follow-up team is Edmund Sonuga-Barke, Mark Kennedy, Jana Kreppner, Nicky Knights, Robert Kumsta, Barbara Maughan and Wolff Schlotz.

References

Almas, A. N., Degnan, K. A., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2016). IQ At age 12 following a history of institutional care: Findings from the Bucharest early intervention project. Developmental Psychology, 52, 18581866.CrossRefGoogle ScholarPubMed
Altgassen, M., Kretschmer, A., & Kliegel, M. (2014). Task dissociation in prospective memory performance in individuals with ADHD. Journal of Attention Disorders, 18, 617624.CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57, 289300.CrossRefGoogle Scholar
Bick, J., Luyster, R., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2017). Effects of early institutionalization on emotion processing in 12-year-old youth. Development and Psychopathology, 29, 17491761.CrossRefGoogle ScholarPubMed
Birn, R. M., Roeber, B. J., & Pollak, S. D. (2017). Early childhood stress exposure, reward pathways, and adult decision making. Proceedings of the National Academy of Sciences, 114, 1354913554.CrossRefGoogle ScholarPubMed
Bland, A. R., Roiser, J. P., Mehta, M. A., Schei, T., Boland, H., Campbell-Meiklejohn, D. K., … Elliott, R. (2016). EMOTICOM: A neuropsychological test battery to evaluate emotion, motivation, impulsivity, and social cognition. Frontiers in Behavioral Neuroscience, 10, 117.CrossRefGoogle ScholarPubMed
Borhani, K., & Nejati, V. (2018). Emotional face recognition in individuals with attention-deficit/hyperactivity disorder: A review article. Developmental Neuropsychology, 43, 256277.CrossRefGoogle ScholarPubMed
Bos, K. J., Fox, N., Zeanah, C. H., & Nelson, C. A. (2009). Effects of early psychosocial deprivation on the development of memory and executive function. Frontiers in Behavioral Neuroscience, 3, 17.CrossRefGoogle ScholarPubMed
Carlisi, C. O., Norman, L., Murphy, C. M., Christakou, A., Chantiluke, K., Giampietro, V., … Rubia, K. (2017). Shared and disorder-specific neurocomputational mechanisms of decision-making in autism Spectrum disorder and obsessive-compulsive disorder. Cerebral Cortex, 27, 58045816.CrossRefGoogle ScholarPubMed
Clark, L., Li, R., Wright, C. M., Rome, F., Fairchild, G., Dunn, B. D., & Aitken, M. R. F. (2012). Risk-avoidant decision making increased by threat of electric shock. Psychophysiology, 49, 14361443.CrossRefGoogle ScholarPubMed
Colvert, E., Rutter, M., Beckett, C., Castle, J., Groothues, C., Hawkins, A., … Sonuga-Barke, E. J. S. (2008a). Emotional difficulties in early adolescence following severe early deprivation: Findings from the English and Romanian adoptees study. Development and Psychopathology, 20, 547567.CrossRefGoogle Scholar
Colvert, E., Rutter, M., Kreppner, J., Beckett, C., Castle, J., Groothues, C., … Sonuga-Barke, E. J. S. (2008b). Do theory of mind and executive function deficits underlie the adverse outcomes associated with profound early deprivation?: Findings from the English and Romanian adoptees study. Journal of Abnormal Child Psychology, 36, 10571068.CrossRefGoogle Scholar
Conners, C. K., Pitkanen, J., & Rzepa, S. R. (2011). Conners comprehensive behavior rating scale. In Cicchetti, D. & Cohen, D. J. (Eds.) Encyclopedia of clinical neuropsychology (pp. 678680). New York, NY: Springer.CrossRefGoogle Scholar
Criaud, M., Wardak, C., Ben Hamed, S., Ballanger, B., & Boulinguez, P. (2012). Proactive inhibitory control of response as the default state of executive control. Frontiers in Psychology, 3, 113.CrossRefGoogle ScholarPubMed
Diaz-Asper, C. M., Schretlen, D. J., & Pearlson, G. D. (2004). How well does IQ predict neuropsychological test performance in normal adults? Journal of the International Neuropsychological Society, 10, 8290.CrossRefGoogle ScholarPubMed
Dillon, D. G., Holmes, A. J., Birk, J. L., Brooks, N., Lyons-Ruth, K., & Pizzagalli, D. A. (2009). Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biological Psychiatry, 66, 206213.CrossRefGoogle ScholarPubMed
Doretto, V., & Scivoletto, S. (2018). Effects of early neglect experience on recognition and processing of facial expressions: A systematic review. Brain Sciences, 8, 10.CrossRefGoogle ScholarPubMed
Du Rietz, E., Cheung, C. H. M., McLoughlin, G., Brandeis, D., Banaschewski, T., Asherson, P., & Kuntsi, J. (2016). Self-report of ADHD shows limited agreement with objective markers of persistence and remittance. Journal of Psychiatric Research, 82, 9199.CrossRefGoogle ScholarPubMed
Field, A. P., & Wilcox, R. R. (2017). Robust statistical methods: A primer for clinical psychology and experimental psychopathology researchers. Behaviour Research and Therapy, 98, 1938.CrossRefGoogle ScholarPubMed
Fuermaier, A. B. M., Tucha, L., Koerts, J., Aschenbrenner, S., Westermann, C., Weisbrod, M., … Tucha, O. (2013). Complex prospective memory in adults with attention deficit hyperactivity disorder. PLos ONE, 8, e58338.CrossRefGoogle ScholarPubMed
Fuermaier, A. B. M., Tucha, L., Koerts, J., Weisbrod, M., Lange, K. W., Aschenbrenner, S., & Tucha, O. (2017). Effects of methylphenidate on memory functions of adults with ADHD. Applied Neuropsychology: Adult, 24, 199211.CrossRefGoogle ScholarPubMed
Geurts, H. M., van den Bergh, S. F. W. M., & Ruzzano, L. (2014). Prepotent response inhibition and interference control in autism Spectrum disorders: Two meta-analyses. Autism Research, 7, 407420.CrossRefGoogle ScholarPubMed
Goodman, J. B., Freeman, E. E., & Chalmers, K. A. (2019). The relationship between early life stress and working memory in adulthood: A systematic review and meta-analysis. Memory (Hove, England), 27, 868880.CrossRefGoogle ScholarPubMed
Guyer, A. E., Kaufman, J., Hodgdon, H. B., Masten, C. L., Jazbec, S., Pine, D. S., & Ernst, M. (2006). Behavioral alterations in reward system function: The role of childhood maltreatment and psychopathology. Journal of the American Academy of Child & Adolescent Psychiatry, 45, 10591067.CrossRefGoogle ScholarPubMed
Hanson, J. L., Albert, D., Iselin, A.-M. R., Carre, J. M., Dodge, K. A., & Hariri, A. R. (2016). Cumulative stress in childhood is associated with blunted reward-related brain activity in adulthood. Social Cognitive and Affective Neuroscience, 11, 405412.CrossRefGoogle ScholarPubMed
Hardt, J., & Rutter, M. (2004). Validity of adult retrospective reports of adverse childhood experiences: Review of the evidence. Journal of Child Psychology and Psychiatry, 45, 260273.CrossRefGoogle Scholar
Huizenga, H. M., van Bers, B. M. C. W., Plat, J., van den Wildenberg, W. P. M., & van der Molen, M. W. (2009). Task complexity enhances response inhibition deficits in childhood and adolescent attention-deficit/hyperactivity disorder: A meta-regression analysis. Biological Psychiatry, 65, 3945.CrossRefGoogle ScholarPubMed
IBM Corp. Released (2017). IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY: IBM Corp.Google Scholar
Kavanaugh, B. C., Dupont-Frechette, J. A., Jerskey, B. A., & Holler, K. A. (2017). Neurocognitive deficits in children and adolescents following maltreatment: Neurodevelopmental consequences and neuropsychological implications of traumatic stress. Applied Neuropsychology-Child, 6, 6478.CrossRefGoogle ScholarPubMed
Kennedy, M., Kreppner, J., Knights, N., Kumsta, R., Maughan, B., Golm, D., … Sonuga-Barke, E. J. S. (2016). Early severe institutional deprivation is associated with a persistent variant of adult attention-deficit/hyperactivity disorder: Clinical presentation, developmental continuities and life circumstances in the English and Romanian adoptees study. Journal of Child Psychology and Psychiatry, 57, 11131125.CrossRefGoogle ScholarPubMed
Kennedy, M., Kreppner, J., Knights, N. H., Kumsta, R., Maughan, B., Golm, D., … Sonuga-Barke, E. (2017). Adult disinhibited social engagement (DSE) in adoptees exposed to extreme institutional deprivation: An examination of its clinical status and functional impact. British Journal of Psychiatry, 211, 289295.CrossRefGoogle ScholarPubMed
Lin, P.-Z., Bai, H.-Y., Sun, J.-W., Guo, W., Zhang, H.-H., & Cao, F.-L. (2017). Association between child maltreatment and prospective and retrospective memory in adolescents: The mediatory effect of neuroticism. Child Abuse & Neglect, 65, 5867.CrossRefGoogle ScholarPubMed
Lipszyc, J., & Schachar, R. (2010). Inhibitory control and psychopathology A meta-analysis of studies using the stop signal task. Journal of the International Neuropsychological Society, 16, 10641076.CrossRefGoogle ScholarPubMed
Lozier, L. M., Vanmeter, J. W., & Marsh, A. A. (2014). Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis. Development and Psychopathology, 26, 933945.CrossRefGoogle ScholarPubMed
Luke, N., & Banerjee, R. (2013). Differentiated associations between childhood maltreatment experiences and social understanding: A meta-analysis and systematic review. Developmental Review, 33, 128.CrossRefGoogle Scholar
Mackes, N. K., Golm, D., Sarkar, S., Kumsta, R., Rutter, M., Fairchild, G., … Sonuga-Barke, E. J. S., & on behalf of the ERA Young Adult Follow-up team (2020). Early childhood deprivation is associated with alterations in adult brain structure despite subsequent environmental enrichment. Proceedings of the National Academy of Sciences, 117, 641649.CrossRefGoogle ScholarPubMed
McCrory, E. J., Gerin, M. I., & Viding, E. (2017). Annual research review: Childhood maltreatment, latent vulnerability and the shift to preventative psychiatry – the contribution of functional brain imaging. Journal of Child Psychology and Psychiatry, 58, 338357.CrossRefGoogle ScholarPubMed
McDermott, J. M., Troller-Renfree, S., Vanderwert, R., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2013). Psychosocial deprivation, executive functions, and the emergence of socio-emotional behavior problems. Frontiers in Human Neuroscience, 7, 167.CrossRefGoogle ScholarPubMed
McLennan, J. D. (2016). Understanding attention deficit hyperactivity disorder as a continuum. Canadian Family Physician, 62, 979982.Google ScholarPubMed
Mehta, M. A., Gore-Langton, E., Golembo, N., Colvert, E., Williams, S. C. R., & Sonuga-Barke, E. J. S. (2010). Hyporesponsive reward anticipation in the basal Ganglia following severe institutional deprivation early in life. Journal of Cognitive Neuroscience, 22, 23162325.CrossRefGoogle ScholarPubMed
Merz, E. C., McCall, R. B., Wright, A. J., & Luna, B. (2013). Inhibitory control and working memory in post-institutionalized children. Journal of Abnormal Child Psychology, 41, 879890.CrossRefGoogle ScholarPubMed
Meyer, H. C., & Bucci, D. J. (2016). Neural and behavioral mechanisms of proactive and reactive inhibition. Learning & Memory, 23, 504514.CrossRefGoogle ScholarPubMed
Miller, M., Ho, J., & Hinshaw, S. P. (2012). Executive functions in girls with ADHD followed prospectively into young adulthood. Neuropsychology, 26, 278287.CrossRefGoogle ScholarPubMed
Miranda-Casas, A., Baixauli-Fortea, I., Colomer-Diago, C., & Rosello-Miranda, B. (2013). Autism and attention deficit hyperactivity disorder: Similarities and differences in executive functioning and theory of mind. Revista De Neurologia, 57, S177S184.Google ScholarPubMed
Morton, J., Frith, U. (1995). Causal modeling: A structural approach to developmental psychopathology. In Developmental psychopathology, Vol. 1: Theory and methods wiley series on personality processes (pp. 357–3). Oxford, England: John Wiley & Sons.Google Scholar
Moulson, M. C., Shutts, K., Fox, N. A., Zeanah, C. H., Spelke, E. S., & Nelson, C. A. (2015). Effects of early institutionalization on the development of emotion processing: A case for relative sparing? Developmental Science, 18, 298313.CrossRefGoogle ScholarPubMed
Nelson, C. A., Westerlund, A., McDermott, J. M., Zeanah, C. H., & Fox, N. A. (2013). Emotion recognition following early psychosocial deprivation. Development and Psychopathology, 25, 517525.CrossRefGoogle ScholarPubMed
Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2019). How early experience shapes human development: The case of psychosocial deprivation. Neural Plasticity, 2019, 1676285.CrossRefGoogle ScholarPubMed
Norman, R. E., Byambaa, M., De, R., Butchart, A., Scott, J., & Vos, T. (2012). The long-term health consequences of child physical abuse, emotional abuse, and neglect: A systematic review and meta-analysis. ed. M. Tomlinson PLoS Medicine, 9, e1001349.CrossRefGoogle ScholarPubMed
Pani, P., Menghini, D., Napolitano, C., Calcagni, M., Armando, M., Sergeant, J. A., & Vicari, S. (2013). Proactive and reactive control of movement are differently affected in attention deficit hyperactivity disorder children. Research in Developmental Disabilities, 34, 31043111.CrossRefGoogle ScholarPubMed
Pearl, A. M., Edwards, E. M., & Murray, M. J. (2017). Comparison of self-and other-report of symptoms of autism and comorbid psychopathology in adults with autism spectrum disorder. Contemporary Behavioral Health Care, 2, 18.CrossRefGoogle Scholar
Petridou, E., Zavitsanos, X., Dessypris, N., Frangakis, C., Mandyla, M., Doxiadis, S., & Trichopoulos, D. (1997). Adolescents in high-risk trajectory: Clustering of risky behavior and the origins of socioeconomic health differentials. Preventive Medicine, 26, 215219.CrossRefGoogle ScholarPubMed
R Core Team (2016, 2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Raskin, S. (2009). Memory for intentions screening test: Psychometric properties and clinical evidence. Brain Impairment, 10, 2333.CrossRefGoogle Scholar
Rutter, M. (1998). Developmental catch-up, and deficit, following adoption after severe global early privation. Journal of Child Psychology and Psychiatry, 39, 465476.CrossRefGoogle ScholarPubMed
Rutter, M., Bailey, A., & Lord, C. (2003). SCQ. The social communication questionnaire. Torrance, CA: Western Psychological Services.Google Scholar
Rutter, M., Kreppner, J., Croft, C., Murin, M., Colvert, E., Beckett, C., … Sonuga-Barke, E. (2007). Early adolescent outcomes of institutionally deprived and non-deprived adoptees. III. Quasi-autism. Journal of Child Psychology and Psychiatry, 48, 12001207.CrossRefGoogle ScholarPubMed
Rutter, M., & O'Connor, T. G. (2004). Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. Developmental Psychology, 40, 8194.CrossRefGoogle ScholarPubMed
Sheppard, D. P., Bruineberg, J. P., Kretschmer-Trendowicz, A., & Altgassen, M. (2018). Prospective memory in autism: Theory and literature review. Clinical Neuropsychologist, 32, 748782.CrossRefGoogle ScholarPubMed
Sonuga-Barke, E. J. S., Cortese, S., Fairchild, G., & Stringaris, A. (2016). Annual research review: Transdiagnostic neuroscience of child and adolescent mental disorders – differentiating decision making in attention-deficit/hyperactivity disorder, conduct disorder, depression, and anxiety. Journal of Child Psychology and Psychiatry, 57, 321349.CrossRefGoogle ScholarPubMed
Sonuga-Barke, E. J., Kennedy, M., Kumsta, R., Knights, N., Golm, D., Rutter, M., … Kreppner, J. (2017). Child-to-adult neurodevelopmental and mental health trajectories after early life deprivation: The young adult follow-up of the longitudinal English and Romanian adoptees study. The Lancet, 389, 15391548.CrossRefGoogle Scholar
Sorensen, L., Sonuga-Barke, E., Eichele, H., van Wageningen, H., Wollschlaeger, D., & Plessen, K. J. (2017). Suboptimal decision making by children with ADHD in the face of risk: Poor risk adjustment and delay aversion rather than general proneness to taking risks. Neuropsychology, 31, 119128.CrossRefGoogle ScholarPubMed
Stevens, S. E., Sonuga-Barke, E. J. S., Kreppner, J. M., Beckett, C., Castle, J., Colvert, E., … Rutter, M. (2008). Inattention/overactivity following early severe institutional deprivation: Presentation and associations in early adolescence. Journal of Abnormal Child Psychology, 36, 385398.CrossRefGoogle ScholarPubMed
Talbot, K.-D. S., Mueller, U., & Kerns, K. A. (2018). Prospective memory in children with attention deficit hyperactivity disorder: A review. Clinical Neuropsychologist, 32, 783815.CrossRefGoogle ScholarPubMed
van Hulst, B. M., de Zeeuw, P., Vlaskamp, C., Rijks, Y., Zandbelt, B. B., & Durston, S. (2018). Children with ADHD symptoms show deficits in reactive but not proactive inhibition, irrespective of their formal diagnosis. Psychological Medicine, 48(15), 17.CrossRefGoogle Scholar
Vasileva, M., & Petermann, F. (2018). Attachment, development, and mental health in abused and neglected preschool children in foster care: A meta-analysis. Trauma, Violence, & Abuse, 19, 443458.CrossRefGoogle ScholarPubMed
Wade, M., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2019). Long-term effects of institutional rearing, foster care, and brain activity on memory and executive functioning. Proceedings of the National Academy of Sciences, 116, 18081813.CrossRefGoogle ScholarPubMed
Wechsler, D. (2011). Wechsler abbreviated scale of intelligence, second edition (WASI-II). San Antonio, TX: NCS Pearson.Google Scholar
Wilcox, R. R. (2016). Introduction to robust estimation and hypothesis testing (4th ed.). Waltham, MA: Academic Press.Google Scholar
Young, J. C., & Widom, C. S. (2014). Long-term effects of child abuse and neglect on emotion processing in adulthood. Child Abuse & Neglect, 38, 13691381.CrossRefGoogle ScholarPubMed
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The impact of childhood deprivation on adult neuropsychological functioning is associated with ADHD symptom persistence
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