Skip to main content

Advertisement

SpringerLink
Log in

Reduced fine motor competence in children with ADHD is associated with atypical microstructural organization within the superior longitudinal fasciculus

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Recent work in healthy adults suggests that white matter organization within the superior longitudinal fasciculus (SLF) may, at least partly, explain individual differences in fine motor skills. The SLF is also often implicated in the neurobiology underlying attention deficit hyperactivity disorder (ADHD) as part of the attention network connecting frontal and parietal regions. While ADHD is primarily characterized by inattention, impulsivity and/or hyperactivity, atypical fine motor control is a common comorbid feature. This study aimed to investigate the association between reduced fine motor skills in ADHD and microstructural properties within the SLF. Participants were 55 right-handed children with ADHD and 61 controls aged 9–11 years. Fine motor control was assessed using the Grooved Pegboard task. Children underwent high angular resolution diffusion MRI. Following pre-processing, constrained spherical deconvolution tractography was performed to delineate the three SLF branches bilaterally. Children with ADHD showed significantly poorer fine motor performance relative to controls in the non-dominant hand, indicated by significantly slower left handed Grooved Pegboard task performance. This slower response time for the non-dominant (left) hand was significantly associated with reduced apparent fibre density within the right SLF I, and reduced right SLF I, II and III volume. This finding was independent of spatial attention performance. These data support previous reports indicating that children with ADHD have poorer fine motor performance than controls in their non-dominant hand, and indicates that the neurobiological basis for impaired fine motor control may involve white matter properties within the contralateral SLF. This suggests that white matter properties in fronto-parietal areas may have broader implications than attention.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Australian Bureau of Statistics. (2011). Socio-economic indexes for areas (SEIFA). Australia: Canberra Retrieved from https://www.abs.gov.au/websitedbs/censushome.nsf/home/seifa.

  • Bellgrove, M. A., Barry, E., Johnson, K. A., Cox, M., Dáibhis, A., Daly, M., et al. (2008). Spatial attentional bias as a marker of genetic risk, symptom severity, and stimulant response in ADHD. Neuropsychopharmacology, 33(10), 2536.

    Article  CAS  Google Scholar 

  • Bellgrove, M. A., Hawi, Z., Kirley, A., Fitzgerald, M., Gill, M., & Robertson, I. H. (2005). Association between dopamine transporter (DAT1) genotype, left-sided inattention, and an enhanced response to methylphenidate in attention-deficit hyperactivity disorder. Neuropsychopharmacology, 30(12), 2290.

    Article  CAS  Google Scholar 

  • 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(1), 289–300.

  • Budisavljevic, S., Dell'Acqua, F., Zanatto, D., Begliomini, C., Miotto, D., Motta, R., & Castiello, U. (2016). Asymmetry and structure of the fronto-parietal networks underlie visuomotor processing in humans. Cerebral Cortex, 27(2), 1532–1544.

    Google Scholar 

  • Causby, R., Reed, L., McDonnell, M., & Hillier, S. (2014). Use of objective psychomotor tests in health professionals. Perceptual and Motor Skills, 118(3), 765–804.

    Article  Google Scholar 

  • Conners, C. K. (2008). Conners 3rd edition: Manual (Vol 14). In Multi-health systems Toronto. Ontario: Canada.

    Google Scholar 

  • De Schotten, M. T., Dell'Acqua, F., Forkel, S. J., Simmons, A., Vergani, F., Murphy, D. G., & Catani, M. (2011). A lateralized brain network for visuospatial attention. Nature Neuroscience, 14(10), 1245.

    Article  Google Scholar 

  • Dell'Acqua, F., & Tournier, J. D. (2018). Modelling white matter with spherical deconvolution: How and why? NMR in Biomedicine, e3945.

  • Dougherty, C. C., Evans, D. W., Myers, S. M., Moore, G. J., & Michael, A. M. (2016). A comparison of structural brain imaging findings in autism spectrum disorder and attention-deficit hyperactivity disorder. Neuropsychology Review, 26(1), 25–43.

    Article  Google Scholar 

  • Egeland, J., Ueland, T., & Johansen, S. (2012). Central processing energetic factors mediate impaired motor control in ADHD combined subtype but not in ADHD inattentive subtype. Journal of Learning Disabilities, 45(4), 361–370.

    Article  Google Scholar 

  • Farquharson, S., & Tournier, J.-D. (2016). High angular resolution diffusion imaging. In Diffusion Tensor Imaging (pp. 383-406): Springer.

  • Farquharson, S., Tournier, J. D., Calamante, F., Fabinyi, G., Schneider-Kolsky, M., Jackson, G. D., & Connelly, A. (2013). White matter fiber tractography: Why we need to move beyond DTI clinical article. Journal of Neurosurgery, 118(6), 1367–1377. https://doi.org/10.3171/2013.2.Jns121294.

    Article  PubMed  Google Scholar 

  • Fenollar-Cortés, J., Gallego-Martínez, A., & Fuentes, L. J. (2017). The role of inattention and hyperactivity/impulsivity in the fine motor coordination in children with ADHD. Research in Developmental Disabilities, 69, 77–84.

    Article  Google Scholar 

  • Floris, D. L., & Howells, H. (2018). Atypical structural and functional motor networks in autism. Progress in Brain Research, 238, 207–248.

    Article  Google Scholar 

  • Friedman, L. A., & Rapoport, J. L. (2015). Brain development in ADHD. Current Opinion in Neurobiology, 30, 106–111.

    Article  CAS  Google Scholar 

  • Genc, S., Malpas, C. B., Ball, G., Silk, T. J., & Seal, M. L. (2018). Age, sex, and puberty related development of the corpus callosum: A multi-technique diffusion MRI study. Brain Structure and Function, 1-13.

  • Goulardins, J. B., Marques, J. C., & De Oliveira, J. A. (2017). Attention deficit hyperactivity disorder and motor impairment: A critical review. Perceptual and Motor Skills, 124(2), 425–440.

    Article  Google Scholar 

  • Goulardins, J. B., Rigoli, D., Licari, M., Piek, J. P., Hasue, R. H., Oosterlaan, J., & Oliveira, J. A. (2015). Attention deficit hyperactivity disorder and developmental coordination disorder: Two separate disorders or do they share a common etiology. Behavioural Brain Research, 292, 484–492.

    Article  Google Scholar 

  • Horowitz, A., Barazany, D., Tavor, I., Bernstein, M., Yovel, G., & Assaf, Y. (2015). In vivo correlation between axon diameter and conduction velocity in the human brain. Brain Structure and Function, 220(3), 1777–1788.

    Article  Google Scholar 

  • Howells, H., Thiebaut de Schotten, M., Dell’Acqua, F., Beyh, A., Zappalà, G., Leslie, A., et al. (2018). Frontoparietal tracts linked to lateralized hand preference and manual specialization. Cerebral Cortex, 28(7), 2482–2494.

    Article  Google Scholar 

  • Jenkinson, M., & Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5(2), 143–156.

    Article  CAS  Google Scholar 

  • Jeurissen, B., Leemans, A., Jones, D. K., Tournier, J. D., & Sijbers, J. (2011). Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Human Brain Mapping, 32(3), 461–479.

    Article  Google Scholar 

  • Kaiser, M.-L., Schoemaker, M., Albaret, J.-M., & Geuze, R. (2015). What is the evidence of impaired motor skills and motor control among children with attention deficit hyperactivity disorder (ADHD)? Systematic review of the literature. Research in Developmental Disabilities, 36, 338–357.

    Article  Google Scholar 

  • Kamali, A., Flanders, A. E., Brody, J., Hunter, J. V., & Hasan, K. M. (2014). Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Structure and Function, 219(1), 269–281.

    Article  Google Scholar 

  • Konrad, A., Dielentheis, T. F., El Masri, D., Bayerl, M., Fehr, C., Gesierich, T., et al. (2010). Disturbed structural connectivity is related to inattention and impulsivity in adult attention deficit hyperactivity disorder. European Journal of Neuroscience, 31(5), 912–919.

    Article  Google Scholar 

  • Langevin, L. M., Macmaster, F. P., Crawford, S., Lebel, C., & Dewey, D. (2014). Common white matter microstructure alterations in pediatric motor and attention disorders. The Journal of Pediatrics, 164(5), 1157–1164 e1151. https://doi.org/10.1016/j.jpeds.2014.01.018.

    Article  PubMed  Google Scholar 

  • Lavasani, N. M., & Stagnitti, K. (2011). A study on fine motor skills of Iranian children with attention deficit/hyper activity disorder aged from 6 to 11 years. Occupational Therapy International, 18(2), 106–114.

    Article  Google Scholar 

  • Levy, F., Hay, D. A., McSTEPHEN, M., Wood, C., & Waldman, I. (1997). Attention-deficit hyperactivity disorder: A category or a continuum? Genetic analysis of a large-scale twin study. Journal of the American Academy of Child & Adolescent Psychiatry, 36(6), 737–744.

    Article  CAS  Google Scholar 

  • Makris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness Jr., V. S., & Pandya, D. N. (2004). Segmentation of subcomponents within the superior longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study. Cerebral Cortex, 15(6), 854–869.

    Article  Google Scholar 

  • McLennan, J. D. (2016). Understanding attention deficit hyperactivity disorder as a continuum. Canadian Family Physician, 62(12), 979–982.

    PubMed  PubMed Central  Google Scholar 

  • Merker, B., & Podell, K. (2011). Grooved pegboard test. In Encyclopedia of clinical neuropsychology (pp. 1176-1178): Springer.

  • Parlatini, V., Radua, J., Dell’Acqua, F., Leslie, A., Simmons, A., Murphy, D. G., et al. (2017). Functional segregation and integration within fronto-parietal networks. Neuroimage, 146, 367–375.

    Article  Google Scholar 

  • Petrovic, P., & Castellanos, F. X. (2016). Top-down dysregulation—From ADHD to emotional instability. Frontiers in Behavioral Neuroscience, 10, 70.

    Article  Google Scholar 

  • Polanczyk, G. V., Willcutt, E. G., Salum, G. A., Kieling, C., & Rohde, L. A. (2014). ADHD prevalence estimates across three decades: An updated systematic review and meta-regression analysis. International Journal of Epidemiology, 43(2), 434–442.

    Article  Google Scholar 

  • Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage, 59(3), 2142–2154.

    Article  Google Scholar 

  • Raffelt, D., Tournier, J. D., Rose, S., Ridgway, G. R., Henderson, R., Crozier, S., et al. (2012). Apparent fibre density: A novel measure for the analysis of diffusion-weighted magnetic resonance images. Neuroimage, 59(4), 3976–3994. https://doi.org/10.1016/j.neuroimage.2011.10.045.

    Article  PubMed  Google Scholar 

  • Rommelse, N. N., Altink, M. E., Oosterlaan, J., Buschgens, C. J., Buitelaar, J., De Sonneville, L. M., & Sergeant, J. A. (2007). Motor control in children with ADHD and non-affected siblings: Deficits most pronounced using the left hand. Journal of Child Psychology and Psychiatry, 48(11), 1071–1079.

    Article  Google Scholar 

  • Scharoun, S., Bryden, P., Otipkova, Z., Musalek, M., & Lejcarova, A. (2013). Motor skills in Czech children with attention-deficit/hyperactivity disorder and their neurotypical counterparts. Research in Developmental Disabilities, 34(11), 4142–4153.

    Article  CAS  Google Scholar 

  • Sciberras, E., Efron, D., Schilpzand, E. J., Anderson, V., Jongeling, B., Hazell, P., et al. (2013). The Children’s attention project: A community-based longitudinal study of children with ADHD and non-ADHD controls. BMC Psychiatry, 13(1), 18.

    Article  Google Scholar 

  • Shaffer, D., Fisher, P., Lucas, C. P., Dulcan, M. K., & Schwab-Stone, M. E. (2000). NIMH diagnostic interview schedule for children version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 39(1), 28–38.

    Article  CAS  Google Scholar 

  • Silk, T. J., Genc, S., Anderson, V., Efron, D., Hazell, P., Nicholson, J. M., et al. (2016). Developmental brain trajectories in children with ADHD and controls: A longitudinal neuroimaging study. BMC Psychiatry, 16(1), 59.

    Article  Google Scholar 

  • Smith, R. E., Tournier, J.-D., Calamante, F., & Connelly, A. (2012). Anatomically-constrained tractography: Improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage, 62(3), 1924–1938.

    Article  Google Scholar 

  • Strenge, H., Niederberger, U., & Seelhorst, U. (2002). Correlation between tests of attention and performance on grooved and Purdue pegboards in normal subjects. Perceptual and Motor Skills, 95(2), 507–514.

    Article  Google Scholar 

  • van Ewijk, H., Heslenfeld, D. J., Zwiers, M. P., Buitelaar, J. K., & Oosterlaan, J. (2012). Diffusion tensor imaging in attention deficit/hyperactivity disorder: A systematic review and meta-analysis. Neuroscience & Biobehavioral Reviews, 36(4), 1093–1106.

    Article  Google Scholar 

  • Wang, X., Pathak, S., Stefaneanu, L., Yeh, F.-C., Li, S., & Fernandez-Miranda, J. C. (2016). Subcomponents and connectivity of the superior longitudinal fasciculus in the human brain. Brain Structure and Function, 221(4), 2075–2092.

    Article  Google Scholar 

  • Weschler, D. (2011). Wechsler abbreviated scale of intelligence–second edition (WASI-II) manual. In: San Antonio, TX: Psychological Corporation.

  • Wu, Z.-M., Bralten, J., Cao, Q.-J., Hoogman, M., Zwiers, M. P., An, L., et al. (2017). White matter microstructural alterations in children with ADHD: Categorical and dimensional perspectives. Neuropsychopharmacology, 42(2), 572.

    Article  Google Scholar 

  • Wulf, G. (2007). Attention and motor skill learning: Human kinetics.

Download references

Funding sources

This project is funded by Project Grants from the Australian National Health and Medical Research Council (NHRMC) (1,065,895, 1,008,522). A/Prof Sciberras’ position is funded by an NHMRC Career Development Fellowship (1,110,688: 2016–21) and a Veski Inspiring Women’s Fellowship. A/Prof Efron is funded by a Clinician Scientist Fellowship from the Murdoch Children’s Research Institute (MCRI). MCRI is supported by the Victorian Government’s Operational Infrastructure Support Program.

Author information

Authors and Affiliations

  1. Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Victoria, Australia

    Christian Hyde, Emma Sciberras, Ian Fuelscher & Tim Silk

  2. Developmental Imaging, Clinical Sciences, Murdoch Children’s Research Institute, Melbourne, Australia

    Daryl Efron & Tim Silk

  3. Department of Paediatrics, University of Melbourne, Melbourne, Australia

    Daryl Efron & Tim Silk

Authors
  1. Christian Hyde
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emma Sciberras
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daryl Efron
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ian Fuelscher
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tim Silk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Hyde.

Ethics declarations

The authors declare that they have no conflict of interest. All procedures performed in this study were approved by, and conducted in accordance with, the ethical standards of the institutional human research ethics committee. In doing so, they were performed according to the standards of the 1964 Helsinki declaration and its later amendments or comparable standards. Informed consent was obtained from all individual participants included in this study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM1

(DOCX 68 kb)

ESM2

(DOCX 15 kb)

ESM3

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hyde, C., Sciberras, E., Efron, D. et al. Reduced fine motor competence in children with ADHD is associated with atypical microstructural organization within the superior longitudinal fasciculus. Brain Imaging and Behavior 15, 727–737 (2021). https://doi.org/10.1007/s11682-020-00280-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-020-00280-z

Keywords

Search

Navigation