Abstract
Neuroanatomical correlates of developmental psychopathology such as attention deficit hyperactivity and conduct disorder have been identified. The majority of studies point to lesser gray matter in psychopathology, often involving prefrontal cortices. The goal of this study was to test whether similar neural correlates exist for behavioral variance in healthy children and adolescents. A large sample (n = 106) aged 8–19 years underwent MR scanning and their parents completed the Strength and Difficulties Questionnaire. The relationships between cortical thickness and conduct problems and hyperactivity/inattention scale scores were investigated throughout the cerebrum. No associations were found between normal variance in hyperactivity/inattention and cortical thickness. Normal variance in conduct problems was associated with thinner left hemisphere prefrontal and supramarginal cortices. Relationships between conduct problems and cortical thickness interacted with age, with the greatest differences in cortical thickness seen in the younger children. These interactions were observed in the anterior cingulate, orbitofrontal, middle and superior frontal, as well as lateral and medial temporal cortices. In conclusion, the results indicate neurobiological continuity between symptoms of conduct problems within the normal range, and conduct disorder. Relationships of thinner cortices and conduct problems were primarily seen in younger children, and appeared to decrease with age, indicative of different maturational trajectories in the groups. The long-term consequences are unknown, and the results point to a need for longitudinal studies of developmental trajectories of neuroanatomical foundations of behavioral adjustment.
Similar content being viewed by others
References
Anderson SW, Damasio H, Tranel D, Damasio AR (2000) Long-term sequelae of prefrontal cortex damage acquired in early childhood. Dev Neuropsychol 18:281–296
Anderson SW, Wisnowski JL, Barrash J, Damasio H, Tranel D (2009) Consistency of neuropsychological outcome following damage to prefrontal cortex in the first years of life. J Clin Exp Neuropsychol 31:170–179
Bussing R, Grudnik J, Mason D, Wasiak M, Leonard C (2002) ADHD and conduct disorder: an MRI study in a community sample. World J Biol Psychiatry 3:216–220
Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179–194
Dale AM, Sereno MI (1993) Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5:162–176
De Brito SA, Mechelli A, Wilke M, Laurens KR, Jones AP, Barker GJ, Hodgins S, Viding E (2009) Size matters: increased grey matter in boys with conduct problems and callous-unemotional traits. Brain 132:843–852
Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980
Elliott R, Dolan RJ, Frith CD (2000) Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb Cortex 10:308–317
Fairchild G, Passamonti L, Hurford G, Hagan CC, von dem Hagen EA, van Goozen SH, Goodyer IM, Calder AJ (2011) Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. Am J Psychiatry 168:624–633
Fellows LK, Farah MJ (2005) Is anterior cingulate cortex necessary for cognitive control? Brain J Neurol 128:788–796
Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055
Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20:70–80
Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207
Fischl B, Sereno MI, Tootell RB, Dale AM (1999) High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 8:272–284
Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22
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. Proc Natl Acad Sci USA 101:8174–8179
Goodman R (1997) The strengths and difficulties questionnaire: a research note. J Child Psychol Psychiatry 38:581–586
Goodman A, Goodman R (2009) Strengths and difficulties questionnaire as a dimensional measure of child mental health. J Am Acad Child Adolesc Psychiatry 48:400–403
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
Hayasaka S, Nichols TE (2003) Validating cluster size inference: random field and permutation methods. Neuroimage 20:2343–2356
Huebner T, Vloet TD, Marx I, Konrad K, Fink GR, Herpertz SC, Herpertz-Dahlmann B (2008) Morphometric brain abnormalities in boys with conduct disorder. J Am Acad Child Adolesc Psychiatry 47:540–547
Kruesi MJ, Casanova MF, Mannheim G, Johnson-Bilder A (2004) Reduced temporal lobe volume in early onset conduct disorder. Psychiatry Res 132:1–11
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. Arch Gen Psychiatry 60:878–888
Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9:856–869
Obel C, Heiervang E, Rodriguez A, Heyerdahl S, Smedje H, Sourander A, Guethmundsson OO, Clench-Aas J, Christensen E, Heian F, Mathiesen KS, Magnusson P, Njarethvik U, Koskelainen M, Ronning JA, Stormark KM, Olsen J (2004) The strengths and difficulties questionnaire in the Nordic countries. Eur Child Adolesc Psychiatry 13(Suppl 2):II32–II39
Østby Y, Tamnes CK, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2009) Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J Neurosci 29:11772–11782
Pavuluri MN, Yang S, Kamineni K, Passarotti AM, Srinivasan G, Harral EM, Sweeney JA, Zhou XJ (2009) Diffusion tensor imaging study of white matter fiber tracts in pediatric bipolar disorder and attention-deficit/hyperactivity disorder. Biol Psychiatry 65:586–593
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
Rushworth MF, Krams M, Passingham RE (2001) The attentional role of the left parietal cortex: the distinct lateralization and localization of motor attention in the human brain. J Cogn Neurosci 13:698–710
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. Cereb Cortex 14:721–730
Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22:1060–1075
Segonne F, Grimson E, Fischl B (2005) A genetic algorithm for the topology correction of cortical surfaces. Inf Process Med Imaging 19:393–405
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. Proc Natl Acad Sci USA 104:19649–19654
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. Am J Psychiatry 168:143–151
Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, Evans A, Rapoport J, Giedd J (2006) Intellectual ability and cortical development in children and adolescents. Nature 440:676–679
Tamm L, Menon V, Reiss AL (2006) Parietal attentional system aberrations during target detection in adolescents with attention deficit hyperactivity disorder: event-related fMRI evidence. Am J Psychiatry 163:1033–1043
Tamnes CK, Østby Y, Fjell AM, Westlye LT, Due-Tønnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534–548
Tamnes CK, Østby Y, Walhovd KB, Westlye LT, Due-Tønnessen P, Fjell AM (2010) Neuroanatomical correlates of executive functions in children and adolescents: a magnetic resonance imaging (MRI) study of cortical thickness. Neuropsychologia 48:2496–2508
Wahlund K, Kristiansson M (2009) Aggression, psychopathy and brain imaging—review and future recommendations. Int J Law Psychiatry 32:266–271
Walhovd KB, Moe V, Slinning K, Due-Tonnessen P, Bjornerud A, Dale AM, van der Kouwe A, Quinn BT, Kosofsky B, Greve D, Fischl B (2007) Volumetric cerebral characteristics of children exposed to opiates and other substances in utero. Neuroimage 36:1331–1344
Walhovd KB, Westlye LT, Moe V, Slinning K, Due-Tonnessen P, Bjornerud A, van der Kouwe A, Dale AM, Fjell AM (2010) White matter characteristics and cognition in prenatally opiate- and polysubstance-exposed children: a diffusion tensor imaging study. Am J Neuroradiol 31:894–900
Wechsler D (1999) Wechsler abbreviated scale of intelligence (WASI). The Psychological Corporation, San Antonio
Rubia K (211) “Cool” inferior frontostriatal dysfunction in attention-deficit/hyperactivity disorder versus “hot” ventromedial orbitofrontal-limbic dysfunction in conduct disorder: a review. Biol Psychiatry 15:69–87
Acknowledgments
We thank all participants and their families. This work was supported by grants from the Norwegian Research Council (177404/W50 and 186092/V50 to K.B.W., 170837/V50 to Ivar Reinvang, PhD, CSHC, University of Oslo, Norway), the University of Oslo (to K.B.W.), and the Department of Psychology, University of Oslo (to A.M.F.).
Conflict of interest
The authors declare that they have no conflicts of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
787_2012_241_MOESM1_ESM.tif
Online Figure 1 Significant negative relationships between age and cortical thickness were seen bilaterally throughout most of the cortical mantle, both medially (upper panel) and laterally (lower panel) (cluster-wise p < .05, two-tailed, fully corrected for multiple comparisons across space). The results are shown as color-coded overlays and projected onto an inflated template brain. (TIFF 4209 kb)
787_2012_241_MOESM2_ESM.tif
Online Figure 2 Cortical thickness and conduct problems with IQ as a covariate in addition to age and sex Conduct problems was negatively related to cortical thickness in two clusters in the left hemisphere (cluster-wise p < .05, two-tailed, fully corrected for multiple comparisons across space). Sex and age were included as covariates. No relationships were seen in the opposite direction. The results are shown as color-coded overlays and projected onto an inflated template brain. (TIFF 4482 kb)
787_2012_241_MOESM3_ESM.tif
Online Figure 3 Age – conduct problems interactions on cortical thickness with IQ as a covariate in addition to age and sex Significant interactions between age and conduct problems were seen in three clusters in the left and two clusters in the right hemisphere (cluster-wise p < .05, two-tailed, fully corrected for multiple comparisons across space). All interactions were positive, meaning that thickness and conduct problems were more closely related in the younger than the older children. No relationships were seen in the opposite direction. The results are shown as color-coded overlays and projected onto an inflated template brain. (TIFF 4015 kb)
Rights and permissions
About this article
Cite this article
Walhovd, K.B., Tamnes, C.K., Østby, Y. et al. Normal variation in behavioral adjustment relates to regional differences in cortical thickness in children. Eur Child Adolesc Psychiatry 21, 133–140 (2012). https://doi.org/10.1007/s00787-012-0241-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00787-012-0241-5