Abstract
Abnormalities in the white matter microstructure of the attentional system have been implicated in the aetiology of attention deficit hyperactivity disorder (ADHD). Diffusion tensor imaging (DTI) is a promising magnetic resonance imaging (MRI) technology that has increasingly been used in studies of white matter microstructure in the brain. The main objective of this work was to perform an exploratory analysis of white matter tracts in a sample of children with ADHD versus typically developing children (TDC). For this purpose, 13 drug-naive children with ADHD of both genders underwent MRI using DTI acquisition methodology and tract-based spatial statistics. The results were compared to those of a sample of 14 age- and gender-matched TDC. Lower fractional anisotropy was observed in the splenium of the corpus callosum, right superior longitudinal fasciculus, bilateral retrolenticular part of the internal capsule, bilateral inferior fronto-occipital fasciculus, left external capsule and posterior thalamic radiation (including right optic radiation). We conclude that white matter tracts in attentional and motor control systems exhibited signs of abnormal microstructure in this sample of drug-naive children with ADHD.
Similar content being viewed by others
References
Amador N, Fried I (2004) Single-neuron activity in the human supplementary motor area underlying preparation for action. J Neurosurg 100:250–259
American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th edition (DSM-IV). American Psychiatric Association, Washington, DC
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edition (DSM-V). American Psychiatric Association, Washington, DC
Arnsten AF (2006) Fundamentals of attention-deficit/hyperactivity disorder: circuits and pathways. J Clin Psychiatry 67(Suppl 8):7–12
Ashtari M, Kumra S, Bhaskar S et al (2005) Attention-deficit/hyperactivity disorder: a preliminary diffusion tensor imaging study. Biol Psychiatry 57:448–455
Ashtari M, Cervellione KL, Hasan KM et al (2007) White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study. Neuroimage 35:501–510
Banich MT (2003) Interaction between the hemispheres and its implications for the processing capacity of the brain. In: Davidson RJ, Hugdahl K (eds) The asymmetrical brain. MIT Press, Cambridge, pp 261–302
Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94
Barnea-Goraly N, Menon V, Eckert M et al (2005) White matter development during childhood and adolescence: a crosssectional diffusion tensor imaging study. Cereb Cortex 15:1848–1854
Bava Boucquey V, Goldenberg D, Thayer RE, Ward M, Jacobus J et al (2011) Sex differences in adolescent white matter architecture. Brain Res 1375:41–48
Bloom JS, Hynd GW (2005) The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol Rev 15:59–71
Brasil HH, Bordin IA (2010) Convergent validity of K-SADS-PL by comparison with CBCL in a Portuguese speaking outpatient population. BMC Psychiatry 10:83
Bush G (2010) Attention-deficit/hyperactivity disorder and attention networks. Neuropsychopharmacology 35:278–300
Caille S, Sauerwein HC, Schiavetto A et al (2005) Sensory and motor interhemispheric integration after section of different portions of the anterior corpus callosum in nonepileptic patients. Neurosurgery 57:50–59
Cao Q, Sun L, Gong G et al (2010) The macrostructural and microstructural abnormalities of corpus callosum in children with attention deficit/hyperactivity disorder: a combined morphometric and diffusion tensor MRI study. Brain Res 1310:172–180
Casey BJ, Trainor R, Giedd J et al (1997) The role of the anterior cingulated in automatic and controlled processes, a developmental neuroanatomical study. Dev Psychobiol 30:61–69
Castellanos FX, Tannock R (2002) Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nat Rev Neurosci 3:617–628
Chambers WJ, Puig-Antich J, Hirsch M et al (1985) The assessment of affective disorders in children and adolescents by semi-structured interview: test-retest reliability of the Schedule for Affective Disorders and Schizophrenia for School-Age Children, Present Episode version. Arch Gen Psychiatry 42:696–702
Conturo TE, Lori NF, Cull TS et al (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96:10422–10427
Davenport ND, Karatekin C, White T, Lim KO (2010) Differential fractional anisotropy abnormalities in adolescents with ADHD or schizophrenia. Psychiatry Res 181(3):193–198
De Luis-García R, Cabús-Piñol G, Imaz-Roncero C, Argibay-Quiñones D, Barrio-Arranz G, Aja-Fernández S, Alberola-López C (2015) Attention deficit/hyperactivity disorder and medication with stimulants in young children: a DTI study. Prog Neuropsychopharmacol Biol Psychiatry 57:176–184
El-Sayed E, Larsson JO, Persson HE et al (2003) ‘‘Maturational lag’’ hypothesis of attention deficit hyperactivity disorder: an update. Acta Paediatr 92:776–784
Faraone SV, Biederman J, Mennin D, Gershon J, Tsuang MT (1996) A prospective four-year follow-up study of children at risk for ADHD: psychiatric, neuropsychological, and psychosocial outcome. J Am Acad Child Adolesc Psychiatry 35:1449–1459
Galvan A, Hare TA, Davidson M et al (2005) The role of ventral frontostriatal circuitry in reward-based learning in humans. J Neurosci 25:8650–8656
Geffen GM, Jones DL, Geffen LB (1994) Interhemispheric control of manual motor activity. Behav Brain Res 64:131–140
Gillberg C, Gillberg IC, Rasmussen P et al (2004) Co-existing disorders in ADHD-implications for diagnosis and intervention. Eur Child Adolesc Psychiatry 13(Suppl 1):180–192
Greene RW, Biederman J, Faraone SV, Ouellette CA, Penn C, Griffin SM (1996) Toward a new psychometric definition of social disability in children with attention-deficit hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 35:571–578
Haber SN, Brucker JL (2009) Cognitive and limbic circuits that are affected by deep brain stimulation. Front Biosci 14:1823–1834
Hamilton LS, Levitt JG, O’Neill J et al (2008) Reduced white matter integrity in attention-deficit hyperactivity disorder. NeuroReport 19:1705–1708
Herting MM, Maxwell EC, Irvine C, Nagel BJ (2012) The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb Cortex 22:1979–1992
Hoptman MJ, Davidson RJ (1994) How and why do the two cerebral hemispheres interact? Psychol Bull 116:195–219
Innocenti GM, Bressoud R (2003) Callosal axons and their development. In: Iacoboni M, Zaidel E (eds) The parallel brain: The cognitive neuroscience of the corpus callosum. MIT Press, Cambridge, pp 11–26
Kadesjo B, Gillberg C (1999) Developmental coordination disorder in Swedish 7-year-old children. J Am Acad Child Adolesc Psychiany 38:820–828
King JB, Yurgelun-Todd D, Stoeckel A, Di Muzio JM, Lopez-Larson MP (2015) Sex differences in white matter integrity in youths with attention-deficit/hyperactivity disorder: a pilot study. Front Neurosci 9:232
Klingberg T, Vaidya CJ, Gabrieli JD et al (1999) Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. NeuroReport 10:2817–2821
Knight RT, Scabini D, Woods DL (1989) Prefrontal cortex gating of auditory transmission in humans. Brain Res 504:338–342
Konrad K, Eickhoff SB (2010) Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder. Hum Brain Mapp 31(6):904–916
Le Bihan D (2003) Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4:469–480
Mathalon DH, Whitfield SL, Ford JM (2003) Anatomy of an error: ERP and fMRI. Biol Psychol 64:119–141
Mazaheri A, Nieuwenhuis IL, van Dijk H, Jensen O (2009) Prestimulus alpha and mu activity predicts failure to inhibit motor responses. Hum Brain Mapp 30(6):1791–1800
Midorikawa A, Kawamura M, Takaya R (2006) A disconnection syndrome due to agenesis of the corpus callosum: disturbance of unilateral synchronization. Cortex 42:356–365
Mori S, Zhang J (2006) Principles of diffusion tensor primer imaging and its applications to basic neuroscience research. Neuron 51:527–539
Mori S, Wakana S, Nagae-Poetscher LM, Van Zijl PC (2005) MRI atlas of human white matter. Elsevier, Amsterdan
Moseley ME, Kucharczyk J, Asgari HS et al (1991) Anisotropy in diffusion weighted MRI. Magn Reson Med 19:321–326
Mostofsky SH, Cooper KL, Kates WR et al (2002) Smaller prefrontal and premotor volumes in boys with attention-deficit/hyperactivity disorder. Biol Psychiatry 52:785–794
Pavuluri MN, Yang S, Kamineni K et al (2009) Diffusion tensor imaging study of white matter fiber tracts in pediatric bipolar disorder and attention-deficit/hyperactivity disorder. Biol Psychiatry 65:586–593
Querne L, Berquin P, Vernier-Hauvette MP et al (2008) Dysfunction of the attentional brain network in children with developmental coordination disorder: a fMRI study. Brain Res 1244:89–102
Sergeant JA, Pick JP, Oosterlaan J (2006) ADHD and DCD: a relationship in need of research. Hum Mov Sci 25:76–89
Serrien DJ, Nirkko AC, Wiesendanger M (2001) Role of the corpus callosum in bimanual coordination: a comparison of patients with congenital and acquired callosal damage. Eur J Neurosci 14:1897–1905
Silk T, Vance A, Rinehart N et al (2009a) White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Hum Brain Mapp 30:2757–2765
Silk TJ, Vance A, Rinehart N et al (2009b) Structural development of the basal ganglia in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Psychiatry Res 172:220–225
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(S1):208–219
Smith SM, Jenkinson M, Johansen-Berg H et al (2006) Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505
Suzuki Y, Matsuzawa H, Kwee IL et al (2003) Absolute eigenvalue diffusion tensor analysis for human brain maturation. NMR Biomed 16:257–260
Tamm L, Barnea-Goraly N, Reiss AL (2012) Diffusion tensor imaging reveals white matter abnormalities in attention-deficit/hyperactivity disorder. Psychiatry Res 202(2):150–154
Van Ewijk H, Heslenfeld DJ, Zwiers MP, Buitelaar JK, Oosterlann J (2012) Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neurosci Biobehav Rev 36(4):1093–1106
Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36(3):630–644
Wang Y, Adamson C, Yuan W, Altaye M, Rajagopal A, Byars AW et al (2012) Sex differences in white matter development during adolescence: a DTI study. Brain Res 1478:1–15
Wann J (2007) Current approaches to intervention in children with developmental coordination disorder. Dev Med Child Neurol 49:405
Watemberg N, Waiserberg N, Zuk L, Lerman-Sagie T (2007) Developmental coordination disorder in children with attention-deficit–hyperactivity disorder and physical therapy intervention. Dev Med Child Neurol 49:920–925
Wechsler D (1991) WISC-III/manual. The Psychological Corporation, New York
Weyandt L, Swentosky A, Gudmundsdottir BG (2013) Neuroimaging and ADHD: fMRI, PET, DTI findings, and methodological limitations. Dev Neuropsyschol 38(4):211–225
Woolrich MW, Jbabdi S, Patenaude B et al (2009) Bayesian analysis of neuroimaging data in FSL. Neuroimage 45:S173–S186
Zametkin AJ, Liebenauer LL, Fitzgerald GA et al (1993) Brain metabolism in teenagers with attention-deficit hyperactivity disorder. Arch Gen Psychiatry 50:333–340
Zwicker JG, Missiuna C, Boyd LA (2009) Neural correlates of developmental coordination disorder: a review of hypotheses. J Child Neurol 24:1273–1281
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pastura, G., Doering, T., Gasparetto, E.L. et al. Exploratory analysis of diffusion tensor imaging in children with attention deficit hyperactivity disorder: evidence of abnormal white matter structure. ADHD Atten Def Hyp Disord 8, 65–71 (2016). https://doi.org/10.1007/s12402-015-0185-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12402-015-0185-y