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Cortical thickness and inattention/hyperactivity symptoms in young children: a population-based study

Published online by Cambridge University Press:  14 July 2014

S. E. Mous ,
R. L. Muetzel ,
H. El Marroun ,
T. J. C. Polderman ,
A. van der Lugt ,
V. W. Jaddoe ,
A. Hofman ,
F. C. Verhulst ,
H. Tiemeier  and
D. Posthuma
...Show all authors
S. E. Mous
Affiliation:
The Generation R Study Group, Erasmus Medical Center, Rotterdam, The Netherlands Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands
R. L. Muetzel
Affiliation:
The Generation R Study Group, Erasmus Medical Center, Rotterdam, The Netherlands Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands
H. El Marroun
Affiliation:
The Generation R Study Group, Erasmus Medical Center, Rotterdam, The Netherlands Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands
T. J. C. Polderman
Affiliation:
Complex Trait Genetics, Department of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), Neuroscience Campus Amsterdam (NCA), VU University, Amsterdam, The Netherlands
A. van der Lugt
Affiliation:
Department of Radiology, Erasmus Medical Center, Rotterdam, The Netherlands
V. W. Jaddoe
Affiliation:
The Generation R Study Group, Erasmus Medical Center, Rotterdam, The Netherlands Department of Epidemiology, Erasmus Medical Center, Rotterdam, The Netherlands Department of Pediatrics, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands
A. Hofman
Affiliation:
Department of Epidemiology, Erasmus Medical Center, Rotterdam, The Netherlands
F. C. Verhulst
Affiliation:
Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands
H. Tiemeier
Affiliation:
Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands Department of Epidemiology, Erasmus Medical Center, Rotterdam, The Netherlands
D. Posthuma
Affiliation:
Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands Center for Neurogenomics and Cognitive Research, VU University, Amsterdam, The Netherlands Department of Clinical Genetics, Section Medical Genomics, VU MC, Amsterdam, The Netherlands
T. White*
Affiliation:
Department of Child and Adolescent Psychiatry/Psychology, Erasmus Medical Center – Sophia Children's Hospital, Rotterdam, The Netherlands Department of Radiology, Erasmus Medical Center, Rotterdam, The Netherlands
*
* Address for correspondence: T. White, M.D., Ph.D., Erasmus MC-Sophia, Department of Child and Adolescent Psychiatry/Psychology, Room KP-2869, PO Box 2060, 3000 CB Rotterdam, The Netherlands. (Email: t.white@erasmusmc.nl)
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Abstract

Background.

While many neuroimaging studies have investigated the neurobiological basis of attention deficit hyperactivity disorder (ADHD), few have studied the neurobiology of attention problems in the general population. The ability to pay attention falls along a continuum within the population, with children with ADHD at one extreme of the spectrum and, therefore, a dimensional perspective of evaluating attention problems has an added value to the existing literature. Our goal was to investigate the relationship between cortical thickness and inattention and hyperactivity symptoms in a large population of young children.

Method.

This study is embedded within the Generation R Study and includes 6- to 8-year-old children (n = 444) with parent-reported attention and hyperactivity measures and high-resolution structural imaging data. We investigated the relationship between cortical thickness across the entire brain and the Child Behavior Checklist Attention Deficit Hyperactivity Problems score.

Results.

We found that greater attention problems and hyperactivity were associated with a thinner right and left postcentral gyrus. When correcting for potential confounding factors and multiple testing, these associations remained significant.

Conclusions.

In a large, population-based sample we showed that young (6- to 8-year-old) children who show more attention problems and hyperactivity have a thinner cortex in the region of the right and left postcentral gyrus. The postcentral gyrus, being the primary somatosensory cortex, reaches its peak growth early in development. Therefore, the thinner cortex in this region may reflect either a deviation in cortical maturation or a failure to reach the same peak cortical thickness compared with children without attention or hyperactivity problems.

Keywords

Attention problemsbrain imagingchildrencortical thicknessepidemiologypopulation-based studies
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 15 , November 2014 , pp. 3203 - 3213
Copyright
Copyright © Cambridge University Press 2014 

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References

Achenbach, TM, Rescorla, LA (2000). Manual for the ASEBA Preschool Forms and Profiles. University of Vermont, Research Center for Children, Youth, and Families: Burlington, VT.Google Scholar
Biederman, J, Monuteaux, MC, Greene, RW, Braaten, E, Doyle, AE, Faraone, SV (2001). Long-term stability of the Child Behavior Checklist in a clinical sample of youth with attention deficit hyperactivity disorder. Journal of Clinical Child and Adolescent Psychology 30, 492–502.Google Scholar
Cascio, CJ (2010). Somatosensory processing in neurodevelopmental disorders. Journal of Neurodevelopmental Disorders 2, 62–69.Google Scholar
Chklovskii, DB, Mel, BW, Svoboda, K (2004). Cortical rewiring and information storage. Nature 431, 782–788.CrossRefGoogle ScholarPubMed
Dale, AM, Fischl, B, Sereno, MI (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage 9, 179–194.Google Scholar
Derauf, C, Kekatpure, M, Neyzi, N, Lester, B, Kosofsky, B (2009). Neuroimaging of children following prenatal drug exposure. Seminars in Cell and Developmental Biology 20, 441–454.Google Scholar
Dockstader, C, Gaetz, W, Cheyne, D, Tannock, R (2009). Abnormal neural reactivity to unpredictable sensory events in attention-deficit/hyperactivity disorder. Biological Psychiatry 66, 376–383.Google Scholar
Ducharme, S, Hudziak, JJ, Botteron, KN, Albaugh, MD, Nguyen, TV, Karama, S, Evans, AC; Brain Development Cooperative G (2012). Decreased regional cortical thickness and thinning rate are associated with inattention symptoms in healthy children. Journal of the American Academy of Child and Adolescent Psychiatry 51, 18–27.e2.Google Scholar
Durston, S (2003). A review of the biological bases of ADHD: what have we learned from imaging studies? Mental Retardation and Developmental Disabilities Research Reviews 9, 184–195.Google Scholar
Fischl, B, Dale, AM (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences USA 97, 11050–11055.Google Scholar
Ghosh, SS, Kakunoori, S, Augustinack, J, Nieto-Castanon, A, Kovelman, I, Gaab, N, Christodoulou, JA, Triantafyllou, C, Gabrieli, JD, Fischl, B (2010). Evaluating the validity of volume-based and surface-based brain image registration for developmental cognitive neuroscience studies in children 4 to 11 years of age. NeuroImage 53, 85–93.Google Scholar
Gogtay, N, Giedd, JN, Lusk, L, Hayashi, KM, Greenstein, D, Vaituzis, AC, Nugent, TF 3rd, Herman, DH, Clasen, LS, Toga, AW, Rapoport, JL, Thompson, PM (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences USA 101, 8174–8179.Google Scholar
Hagler, DJ Jr, Saygin, AP, Sereno, MI (2006). Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. NeuroImage 33, 1093–1103.Google Scholar
Han, X, Jovicich, J, Salat, D, van der Kouwe, A, Quinn, B, Czanner, S, Busa, E, Pacheco, J, Albert, M, Killiany, R, Maguire, P, Rosas, D, Makris, N, Dale, A, Dickerson, B, Fischl, B (2006). Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. NeuroImage 32, 180–194.CrossRefGoogle ScholarPubMed
Hensch, TK (2004). Critical period regulation. Annual Review of Neuroscience 27, 549–579.Google Scholar
Hudziak, JJ, Achenbach, TM, Althoff, RR, Pine, DS (2007). A dimensional approach to developmental psychopathology. International Journal of Methods in Psychiatric Research 16 (Suppl. 1), S16–S23.Google Scholar
Huttenlocher, PR, Dabholkar, AS (1997). Regional differences in synaptogenesis in human cerebral cortex. Journal of Comparative Neurology 387, 167–178.Google Scholar
Insel, T, Cuthbert, B, Garvey, M, Heinssen, R, Pine, DS, Quinn, K, Sanislow, C, Wang, P (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. American Journal of Psychiatry 167, 748–751.Google Scholar
Jaddoe, VW, van Duijn, CM, Franco, OH, van der Heijden, AJ, van Iizendoorn, MH, de Jongste, JC, van der Lugt, A, Mackenbach, JP, Moll, HA, Raat, H, Rivadeneira, F, Steegers, EA, Tiemeier, H, Uitterlinden, AG, Verhulst, FC, Hofman, A (2012). The Generation R Study: design and cohort update 2012. European Journal of Epidemiology 27, 739–756.Google Scholar
Jovicich, J, Czanner, S, Greve, D, Haley, E, van der Kouwe, A, Gollub, R, Kennedy, D, Schmitt, F, Brown, G, Macfall, J, Fischl, B, Dale, A (2006). Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. NeuroImage 30, 436–443.Google Scholar
Juuhl-Langseth, M, Rimol, LM, Rasmussen, IA Jr, Thormodsen, R, Holmen, A, Emblem, KE, Due-Tonnessen, P, Rund, BR, Agartz, I (2012). Comprehensive segmentation of subcortical brain volumes in early onset schizophrenia reveals limited structural abnormalities. Psychiatry Research 203, 14–23.CrossRefGoogle ScholarPubMed
Karatekin, C, White, T, Bingham, C (2010). Shared and nonshared symptoms in youth-onset psychosis and ADHD. Journal of Attention Disorders 14, 121–131.Google Scholar
Kuperberg, GR, Broome, MR, McGuire, PK, David, AS, Eddy, M, Ozawa, F, Goff, D, West, WC, Williams, SC, van der Kouwe, AJ, Salat, DH, Dale, AM, Fischl, B (2003). Regionally localized thinning of the cerebral cortex in schizophrenia. Archives of General Psychiatry 60, 878–888.Google Scholar
Lubke, GH, Hudziak, JJ, Derks, EM, van Bijsterveldt, TC, Boomsma, DI (2009). Maternal ratings of attention problems in ADHD: evidence for the existence of a continuum. Journal of the American Academy of Child and Adolescent Psychiatry 48, 1085–1093.Google Scholar
Makris, N, Biederman, J, Valera, EM, Bush, G, Kaiser, J, Kennedy, DN, Caviness, VS, Faraone, SV, Seidman, LJ (2007). Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. Cerebral Cortex 17, 1364–1375.Google Scholar
McConaughy, SH, Stanger, C, Achenbach, TM (1992). Three-year course of behavioral/emotional problems in a national sample of 4- to 16-year-olds: I. Agreement among informants. Journal of the American Academy of Child and Adolescent Psychiatry 31, 932–940.Google Scholar
Muratori, F, Salvadori, F, D'Arcangelo, G, Viglione, V, Picchi, L (2005). Childhood psychopathological antecedents in early onset schizophrenia. European Psychiatry 20, 309–314.Google Scholar
Narr, KL, Woods, RP, Lin, J, Kim, J, Phillips, OR, Del'Homme, M, Caplan, R, Toga, AW, McCracken, JT, Levitt, JG (2009). Widespread cortical thinning is a robust anatomical marker for attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry 48, 1014–1022.Google Scholar
Nii, Y, Uematsu, S, Lesser, RP, Gordon, B (1996). Does the central sulcus divide motor and sensory functions? Cortical mapping of human hand areas as revealed by electrical stimulation through subdural grid electrodes. Neurology 46, 360–367.CrossRefGoogle ScholarPubMed
O'Donnell, S, Noseworthy, MD, Levine, B, Dennis, M (2005). Cortical thickness of the frontopolar area in typically developing children and adolescents. NeuroImage 24, 948–954.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Parush, S, Sohmer, H, Steinberg, A, Kaitz, M (2007). Somatosensory function in boys with ADHD and tactile defensiveness. Physiology and Behavior 90, 553–558.CrossRefGoogle ScholarPubMed
Penfield, W, Boldrey, E (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60, 389–443.Google Scholar
Polderman, TJ, Derks, EM, Hudziak, JJ, Verhulst, FC, Posthuma, D, Boomsma, DI (2007). Across the continuum of attention skills: a twin study of the SWAN ADHD rating scale. Journal of Child Psychology and Psychiatry 48, 1080–1087.Google Scholar
Reuter, M, Schmansky, NJ, Rosas, HD, Fischl, B (2012). Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 61, 1402–1418.Google Scholar
Rosas, HD, Liu, AK, Hersch, S, Glessner, M, Ferrante, RJ, Salat, DH, van der Kouwe, A, Jenkins, BG, Dale, AM, Fischl, B (2002). Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology 58, 695–701.Google Scholar
Salat, DH, Buckner, RL, Snyder, AZ, Greve, DN, Desikan, RS, Busa, E, Morris, JC, Dale, AM, Fischl, B (2004). Thinning of the cerebral cortex in aging. Cerebral Cortex 14, 721–730.Google Scholar
Shaw, P, Eckstrand, K, Sharp, W, Blumenthal, J, Lerch, JP, Greenstein, D, Clasen, L, Evans, A, Giedd, J, Rapoport, JL (2007). Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proceedings of the National Academy of Sciences USA 104, 19649–19654.Google Scholar
Shaw, P, Gilliam, M, Liverpool, M, Weddle, C, Malek, M, Sharp, W, Greenstein, D, Evans, A, Rapoport, J, Giedd, J (2011). Cortical development in typically developing children with symptoms of hyperactivity and impulsivity: support for a dimensional view of attention deficit hyperactivity disorder. American Journal of Psychiatry 168, 143–151.Google Scholar
Shaw, P, Lerch, J, Greenstein, D, Sharp, W, Clasen, L, Evans, A, Giedd, J, Castellanos, FX, Rapoport, J (2006). Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Archives of General Psychiatry 63, 540–549.Google Scholar
Stanger, C, MacDonald, VV, McConaughy, SH, Achenbach, TM (1996). Predictors of cross-informant syndromes among children and youths referred for mental health services. Journal of Abnormal Child Psychology 24, 597–614.Google Scholar
Statistics Netherlands (2004a). Allochtonen in Nederland 2004 (Foreigners in the Netherlands 2004). Centraal Bureau voor de Statistiek: Voorburg/Heerlen.Google Scholar
Statistics Netherlands (2004b). Standaard Onderwijsindeling 2003 (Standard Classification of Education 2003). Centraal Bureau voor de Statistiek: Voorburg/Heerlen.Google Scholar
Sur, M, Rubenstein, JL (2005). Patterning and plasticity of the cerebral cortex. Science 310, 805–810.Google Scholar
Swaab-Barneveld, H, de Sonneville, L, Cohen-Kettenis, P, Gielen, A, Buitelaar, J, Van Engeland, H (2000). Visual sustained attention in a child psychiatric population. Journal of the American Academy of Child and Adolescent Psychiatry 39, 651–659.Google Scholar
Tellegen, PJ, Winkel, M, Wijnberg-Williams, B, Laros, JA (2005). Snijders-Oomen Niet-Verbale Intelligentietest: SON-R 2.5–7. Boom Testuitgevers: Amsterdam.Google Scholar
Tiemeier, H, Velders, FP, Szekely, E, Roza, SJ, Dieleman, G, Jaddoe, VW, Uitterlinden, AG, White, TJ, Bakermans-Kranenburg, MJ, Hofman, A, Van Ijzendoorn, MH, Hudziak, JJ, Verhulst, FC (2012). The Generation R Study: a review of design, findings to date, and a study of the 5-HTTLPR by environmental interaction from fetal life onward. Journal of the American Academy of Child and Adolescent Psychiatry 51, 1119–1135.e7.CrossRefGoogle Scholar
van Rijn, S, de Sonneville, L, Lahuis, B, Pieterse, J, van Engeland, H, Swaab, H (2012). Executive function in MCDD and PDD-NOS: a study of inhibitory control, attention regulation and behavioral adaptivity. Journal of Autism and Developmental Disorders 43, 1356–1366.Google Scholar
Verhulst, FC, van der Ende, J (1992). Six-year stability of parent-reported problem behavior in an epidemiological sample. Journal of Abnormal Child Psychology 20, 595–610.Google Scholar
Walhovd, KB, Tamnes, CK, Ostby, Y, Due-Tønnessen, P, Fjell, AM (2012). Normal variation in behavioral adjustment relates to regional differences in cortical thickness in children. European Child and Adolescent Psychiatry. Published online 1 February 2012 . doi:10.1007/s00787-012-0241-5.Google Scholar
Webb, EA, O'Reilly, MA, Clayden, JD, Seunarine, KK, Chong, WK, Dale, N, Salt, A, Clark, CA, Dattani, MT (2012). Effect of growth hormone deficiency on brain structure, motor function and cognition. Brain 135, 216–227.CrossRefGoogle ScholarPubMed
White, T, El Marroun, H, Nijs, I, Schmidt, M, van der Lugt, A, Wielopolki, PA, Jaddoe, VW, Hofman, A, Krestin, GP, Tiemeier, H, Verhulst, FC (2013). Pediatric population-based neuroimaging and the Generation R Study: the intersection of developmental neuroscience and epidemiology. European Journal of Epidemiology 28, 99–111.Google Scholar
Wolosin, SM, Richardson, ME, Hennessey, JG, Denckla, MB, Mostofsky, SH (2009). Abnormal cerebral cortex structure in children with ADHD. Human Brain Mapping 30, 175–184.Google Scholar
Yang, Y, Roussotte, F, Kan, E, Sulik, KK, Mattson, SN, Riley, EP, Jones, KL, Adnams, CM, May, PA, O'Connor, MJ, Narr, KL, Sowell, ER (2012). Abnormal cortical thickness alterations in fetal alcohol spectrum disorders and their relationships with facial dysmorphology. Cerebral Cortex 22, 1170–1179.Google Scholar