Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-16T22:22:47.709Z Has data issue: false hasContentIssue false
  • English
  • Français

Disruptions of working memory and inhibition mediate the association between exposure to institutionalization and symptoms of attention deficit hyperactivity disorder

Published online by Cambridge University Press:  16 October 2015

F. Tibu ,
M. A. Sheridan ,
K. A. McLaughlin ,
C. A. Nelson ,
N. A. Fox  and
C. H. Zeanah
F. Tibu*
Affiliation:
Institute of Child Development, Bucharest, Romania
M. A. Sheridan
Affiliation:
University of North Carolina, Chapel Hill, USA
K. A. McLaughlin
Affiliation:
University of Washington, Seattle, USA
C. A. Nelson
Affiliation:
Harvard University, Boston, USA Boston Children's Hospital, Boston, USA
N. A. Fox
Affiliation:
University of Maryland, College Park, USA
C. H. Zeanah
Affiliation:
Tulane University, New Orleans, USA
*
* Address for correspondence: F. Tibu, Ph.D., Institute of Child Development, 17 Maresal Averescu Blvd. Complexul de Servicii Sociale Sfanta Ecaterina, Corp C, Etaj 1, Bucharest 011454, Romania. (Email: florin.tibu@idc.ro)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Young children raised in institutions are exposed to extreme psychosocial deprivation that is associated with elevated risk for psychopathology and other adverse developmental outcomes. The prevalence of attention deficit hyperactivity disorder (ADHD) is particularly high in previously institutionalized children, yet the mechanisms underlying this association are poorly understood. We investigated whether deficits in executive functioning (EF) explain the link between institutionalization and ADHD.

Method

A sample of 136 children (aged 6–30 months) was recruited from institutions in Bucharest, Romania, and 72 never institutionalized community children matched for age and gender were recruited through general practitioners’ offices. At 8 years of age, children's performance on a number of EF components (working memory, response inhibition and planning) was evaluated. Teachers completed the Health and Behavior Questionnaire, which assesses two core features of ADHD, inattention and impulsivity.

Results

Children with history of institutionalization had higher inattention and impulsivity than community controls, and exhibited worse performance on working memory, response inhibition and planning tasks. Lower performances on working memory and response inhibition, but not planning, partially mediated the association between early institutionalization and inattention and impulsivity symptom scales at age 8 years.

Conclusions

Institutionalization was associated with decreased EF performance and increased ADHD symptoms. Deficits in working memory and response inhibition were specific mechanisms leading to ADHD in previously institutionalized children. These findings suggest that interventions that foster the development of EF might reduce risk for psychiatric problems in children exposed to early deprivation.

Keywords

ADHDchildrenearly deprivationexecutive functioning
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 3 , February 2016 , pp. 529 - 541
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barkley, RA (1997). Behavioral inhibition, sustained attention, and executive function: constructing a unified theory of ADHD. Psychological Bulletin 121, 65–94.CrossRefGoogle Scholar
Barkley, RA (2001). The inattentive type of ADHD as a distinct disorder: what remains to be done. Clinical Psychology: Science and Practice 8, 489–493.Google Scholar
Baron, RM, Kenny, DA (1986). The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. Journal of Personality and Social Psychology 51, 1173–1182.CrossRefGoogle ScholarPubMed
Biederman, J, Milberger, S, Faraone, SV, Kiely, K, Guite, J, Mick, E, Ablon, S, Warburton, R, Reed, E (1995). Family-environment risk factors for attention-deficit hyperactivity disorder. A test of Rutter's indicators of adversity. Archives of General Psychiatry 52, 464–470.CrossRefGoogle ScholarPubMed
Bos, KJ, Fox, N, Zeanah, CH, Nelson, CA (2009). Effects of early psychosocial deprivation on the development of memory and executive function. Frontiers in Behavioral Neuroscience 3, 16.CrossRefGoogle ScholarPubMed
Brocki, K, Eninger, L, Thorell, L, Bohlin, G (2010). Interrelations between executive function and symptoms of hyperactivity/impulsivity and inattention in preschoolers: a two year longitudinal study. Journal of Abnormal Child Psychology 38, 163–171.CrossRefGoogle ScholarPubMed
Coghill, DR, Hayward, D, Rhodes, SM, Grimmer, C, Matthews, K (2014). A longitudinal examination of neuropsychological and clinical functioning in boys with attention deficit hyperactivity disorder (ADHD): improvements in executive functioning do not explain clinical improvement. Psychological Medicine 44, 1087–1099.CrossRefGoogle Scholar
Colvert, E, Rutter, M, Kreppner, J, Beckett, C, Castle, J, Groothues, C, Hawkins, A, Stevens, S, Sonuga-Barke, EJ (2008). Do theory of mind and executive function deficits underlie the adverse outcomes associated with profound early deprivation? Findings from the ERA study. Journal of Abnormal Child Psychology 36, 1057–1068.CrossRefGoogle Scholar
DePrince, AP, Weinzierl, KM, Combs, MD (2009). Executive function performance and trauma exposure in a community sample of children. Child Abuse and Neglect 33, 353–361.CrossRefGoogle Scholar
Eriksen, CW, Schultz, DW (1979). Information processing in visual search: a continuous flow conception and experimental results. Perception & Psychophysics 25, 249–263.CrossRefGoogle ScholarPubMed
Essex, MJ, Boyce, WT, Goldstein, LH, Armstrong, JM, Kraemer, HC, Kupfer, DJ (2002). The confluence of mental, physical, social, and academic difficulties in middle childhood. II. Developing the MacArthur health and behavior questionnaire. Journal of the American Academy of Child and Adolescent Psychiatry 41, 588–603.CrossRefGoogle ScholarPubMed
Fair, DA, Bathula, D, Nikolas, MA, Nigg, JT (2012). Distinct neuropsychological subgroups in typically developing youth inform heterogeneity in children with ADHD. Proceedings of the National Academy of Sciences USA 109, 6769–6774.CrossRefGoogle ScholarPubMed
Fan, J, McCandliss, BD, Sommer, T, Raz, A, Posner, MI (2002). Testing the efficiency and independence of attentional networks. Journal of Cognitive Neuroscience 14, 340–347.CrossRefGoogle ScholarPubMed
Fried, R, Hirshfeld-Becker, D, Petty, C, Batchelder, H, Biederman, J (2015). How informative is the CANTAB to assess executive functioning in children with ADHD? A controlled study. Journal of Attention Disorders 19, 468–475.CrossRefGoogle ScholarPubMed
Halperin, JM, Schulz, KP (2006). Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder. Psychological Bulletin 132, 560–581.CrossRefGoogle ScholarPubMed
Hostinar, CE, Stellern, SA, Schaefer, C, Carlson, SM, Gunnar, MR (2012). Associations between early life adversity and executive function in children adopted internationally from orphanages. Proceedings of the National Academy of Sciences USA 109, 17208–17212.CrossRefGoogle ScholarPubMed
Humphreys, KL, Gleason, MM, Drury, SS, Miron, D, Nelson, CA, Fox, NA, Zeanah, CH (2015). Effects of institutional rearing and foster care on psychopathology at age 12 years in Romania: follow-up of an open, randomised controlled trial. Lancet Psychiatry 7, 625–634.CrossRefGoogle Scholar
Johnstone, SJ, Roodenrys, S, Phillips, E, Watt, AJ, Mantz, S (2010). A pilot study of combined working memory and inhibition training for children with AD/HD. Attention Deficit Hyperactivity Disorders 2, 31–42.CrossRefGoogle ScholarPubMed
Kessler, R, Adler, L, Barkley, R, Biederman, J, Conners, CK, Demler, O, Faraone, S, Greenhill, L, Howes, M, Secnik, K, Spencer, T, Ustun, B, Walters, E, Zaslavsky, A (2006). The prevalence and correlates of adult ADHD in the United States: results from the National Comorbidity Survey Replication. American Journal of Psychiatry 163, 716–723.CrossRefGoogle ScholarPubMed
Klingberg, T, Fernell, E, Olesen, PJ, Johnson, M, Gustafsson, P, Dahlström, K, Gillberg, C, Forssberg, H, Westerberg, H (2005). Computerized training of working memory in children with ADHD – a randomized, controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry 44, 177–186.CrossRefGoogle ScholarPubMed
Kreppner, JM, O'Connor, TG, Rutter, M, English & Romanian Adoptees (ERA) Study Team (2001). Can inattention/overactivity be an institutional deprivation syndrome? Journal of Abnormal Child Psychology 29, 513–528.CrossRefGoogle ScholarPubMed
Lemery-Chalfant, K, Schreiber, JE, Schmidt, NL, Van Hulle, CA, Essex, MJ, Goldsmith, HH (2007). Assessing internalizing, externalizing, and attention problems in young children: validation of the MacArthur HBQ. Journal of the American Academy of Child & Adolescent Psychiatry 46, 1315–1323.CrossRefGoogle ScholarPubMed
Loman, MM, Johnson, AE, Westerlund, A, Pollak, SD, Nelson, CA, Gunnar, MR (2013). The effect of early deprivation on executive attention in middle childhood. Journal of Child Psychology and Psychiatry 54, 37–45.CrossRefGoogle ScholarPubMed
Luciana, M, Nelson, CA (2002). Assessment of neuropsychological function in children through the Cambridge Neuropsychological Testing Automated Battery (CANTAB): normative performance in 4 to 12 year-olds. Developmental Neuropsychology 22, 595–624.CrossRefGoogle Scholar
MacKinnon, DP, Lockwood, CM, Hoffman, JM, West, SG, Sheets, V (2002). A comparison of methods to test mediation and other intervening variable effects. Psychological Methods 7, 83–104.CrossRefGoogle ScholarPubMed
Martel, M, Nikolas, M, Nigg, JT (2007). Executive function in adolescents with ADHD. Journal of the American Academy of Child and Adolescent Psychiatry 46, 1437–1444.CrossRefGoogle ScholarPubMed
Martinussen, R, Hayden, J, Hogg-Johnson, S, Tannock, R (2005) A meta-analysis of working memory impairments in children with ADHD. Journal of the American Academy of Child and Adolescent Psychiatry 44, 377–384.CrossRefGoogle Scholar
McDermott, JM, Troller-Renfree, S, Vanderwert, R, Nelson, CA, Zeanah, CH, Fox, NA (2013). Psychosocial deprivation, executive functions and the emergence of socio-emotional behavior problems. Frontiers in Human Neuroscience 7, 167.CrossRefGoogle ScholarPubMed
McLaughlin, KA, Fox, NA, Zeanah, CH, Sheridan, MA, Marshall, P, Nelson, CA (2010 a). Delayed maturation in brain electrical activity partially explains the association between early environmental deprivation and symptoms of attention-deficit/hyperactivity disorder. Biological Psychiatry 68, 329–336.CrossRefGoogle ScholarPubMed
McLaughlin, KA, Green, JG, Gruber, MJ, Sampson, NA, Zaslavsky, AM, Kessler, RC (2010 b). Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: associations with persistence of DSM-IV disorders. Archives of General Psychiatry 67, 124–132.CrossRefGoogle ScholarPubMed
McLaughlin, KA, Sheridan, MA, Winter, W, Fox, NA, Zeanah, CH, Nelson, CA (2014). Widespread reductions in cortical thickness following severe early-life deprivation: a neurodevelopmental pathway to attention-deficit/hyperactivity disorder. Biological Psychiatry 76, 629–638.CrossRefGoogle ScholarPubMed
Merz, EC, McCall, RB (2011). Parent ratings of executive functioning in children adopted from psychosocially depriving institutions. Journal of Child Psychology and Psychiatry 52, 537–546.CrossRefGoogle ScholarPubMed
Merz, EC, McCall, RB, Groza, V (2013). Parent-reported executive functioning in post-institutionalized children: a follow-up study. Journal of Clinical Child & Adolescent Psychology 42, 726–733.CrossRefGoogle Scholar
Nelson, CA, Fox, NA, Zeanah, CH (2014). Romania's Abandoned Children: Deprivation, Brain Development, and the Struggle for Recovery. Harvard University Press: Cambridge, MA.CrossRefGoogle Scholar
Niendam, TA, Laird, AR, Ray, KL, Dean, YM, Glahn, DC, Carter, CS (2012). Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective and Behavioral Neuroscience 12, 241–268.CrossRefGoogle ScholarPubMed
Nigg, JT (2001). Is ADHD a disinhibitory disorder? Psychological Bulletin 127, 571–598.CrossRefGoogle ScholarPubMed
Nigg, JT, Nikolas, M, Friderici, K, Leeyoung, P, Zucker, RA (2007). Genotype and neuropsychological response inhibition as resilience promoters for ADHD, ODD, and CD under conditions of psychosocial adversity. Development and Psychopathology 19, 767–786.CrossRefGoogle ScholarPubMed
Pears, KC, Fisher, PA, Bruce, J, Kim, HK, Yoerger, K (2010). Early elementary school adjustment of maltreated children in foster care: the role of inhibitory control and caregiver involvement. Child Development 81, 1550–1564.CrossRefGoogle Scholar
Pollak, SD, Nelson, CA, Schlaak, MF, Roeber, BJ, Wewerka, SS, Wiik, KL, Frenn, KA, Loman, MM, Gunnar, MR (2010). Neurodevelopmental effects of early deprivation in postinstitutionalized children. Child Development 81, 224–236.CrossRefGoogle ScholarPubMed
Preacher, KJ, Hayes, AF (2008). Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behavior Research Methods 40, 879–891.CrossRefGoogle ScholarPubMed
Rutter, M, Kreppner, JM, O'Connor, TG, The English Romanian Adoptees (ERA) Study Team (2001). Specificity and heterogeneity in children's responses to profound institutional privation. British Journal of Psychiatry 17, 97–103.CrossRefGoogle Scholar
Rutter, M, Sonuga-Barke, E, Beckett, C, Castle, J, Kreppner, J, Kumsta, R, Schlotz, W, Stevens, S, Bell, C, Gunnar, M (2010). Deprivation-specific psychological patterns: effects of institutional deprivation. Monographs of the Society for Research in Child Development 75, 1–242.CrossRefGoogle Scholar
Schoemaker, K, Bunte, T, Wiebe, SA, Espy, KA, Dekovic, M, Matthys, W (2012). Executive function deficits in preschool children with ADHD and DBD. Journal of Child Psychology and Psychiatry 53, 111–119.CrossRefGoogle ScholarPubMed
Sergeant, J (2000). The cognitive-energetic model: an empirical approach to attention-deficit hyperactivity disorder. Neuroscience and Biobehavioral Reviews 24, 7–12.CrossRefGoogle Scholar
Shallice, T (1982). Specific impairments in planning. Philosophical Transactions of the Royal Society of London 298, 199–209.Google ScholarPubMed
Slopen, N, McLaughlin, KA, Fox, NA, Zeanah, CH, Nelson, CA (2012). Alterations in neural processing and psychopathology in children raised in institutions. Archives of General Psychiatry 69, 1022–1030.CrossRefGoogle ScholarPubMed
Sonuga-Barke, E, Dalen, L, Daley, D, Remington, B (2002). Are planning, working memory, and inhibition associated with individual differences in preschool ADHD symptoms? Developmental Neuropsychology 21, 255–272.CrossRefGoogle ScholarPubMed
Spencer, TJ, Biederman, J, Mick, E (2007). Attention-deficit/hyperactivity disorder: diagnosis, lifespan, comorbidities, and neurobiology. Journal of Pediatric Psychology 32, 631–642.CrossRefGoogle ScholarPubMed
Stevens, SE, Sonuga-Barke, E, Kreppner, JM, Beckett, C, Castle, J, Colvert, E, Groothues, C, Hawkins, A, Rutter, M (2008). Inattention/overactivity following early severe institutional deprivation: presentation and associations in early adolescence. Journal of Abnormal Child Psychology 36, 385–398.CrossRefGoogle ScholarPubMed
Taylor, E, Rogers, JW (2005). Practitioner review: early adversity and developmental disorders. Journal of Child Psychology and Psychiatry 46, 451–467.CrossRefGoogle ScholarPubMed
UNICEF (2010). At Home or in a Home? Formal care and adoption of children in Eastern Europe and Central Asia. UNICEF Geneva, Swizerland.Google Scholar
Wiik, KL, Loman, MM, Van Ryzin, MJ, Armstrong, JM, Essex, MJ, Pollak, SD, Gunnar, MR (2011). Behavioral and emotional symptoms of post-institutionalized children in middle childhood. Journal of Child Psychology and Psychiatry 52, 56–63.CrossRefGoogle ScholarPubMed
Willcutt, EG, Doyle, AE, Nigg, JT, Faraone, SV, Pennington, BF (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biological Psychiatry 57, 1336–1346.CrossRefGoogle ScholarPubMed
Zeanah, CH, Egger, HL, Smyke, AT, Nelson, CA, Fox, NA, Marshall, PJ, Guthrie, D (2009). Institutional rearing and psychiatric disorders in Romanian preschool children. American Journal of Psychiatry 166, 777–785.CrossRefGoogle ScholarPubMed
Zeanah, CH, Fox, NA, Nelson, CA (2012). The Bucharest Early Intervention Project: case study in the ethics of mental health research. Journal of Nervous and Mental Disease 200, 243–247.CrossRefGoogle ScholarPubMed
Zeanah, CH, Nelson, CA, Fox, NA, Smyke, AT, Marshall, P, Parker, S, Koga, S (2003). Designing research to study the effects of institutionalization on brain and behavioral development: the Bucharest Early Intervention Project. Developmental Psychopathology 15, 885–907.CrossRefGoogle Scholar