Prefrontal Cortex Activity in Siblings With and Without Developmental Coordination Disorder: An Exploratory Study

Click name to view affiliation

Mandy S. Plumb School of Health, Medical and Applied Sciences, Central Queensland University—Cairns Campus, Cairns, QLD, Australia

Search for other papers by Mandy S. Plumb in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-3129-7383 *
,
Megan Charity Federation University Australia, Ballarat, VIC, Australia

Search for other papers by Megan Charity in
Current site
Google Scholar
PubMed
Close
,
Kimberly Milla University of Delaware, Newark, DE, USA

Search for other papers by Kimberly Milla in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-5832-9656
,
Barry Bodt University of Delaware, Newark, DE, USA

Search for other papers by Barry Bodt in
Current site
Google Scholar
PubMed
Close
, and
Nancy Getchell Kinesiology and Applied Physiology, University of Delaware, Newark, DE, USA

Search for other papers by Nancy Getchell in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0001-9230-9838
Restricted access

Background: Previous research suggests that children with or at risk of probable developmental coordination disorder (pDCD) activate different areas of the brain when performing certain motor skills compared with typically developing (TD) children. This study used functional near-infrared spectroscopy to compare prefrontal cortex (PFC) activity in TD and pDCD during the completion of manual (three-dimensional [3D]) and computerized versions (two-dimensional) of the Tower of Hanoi (ToH) puzzle. Method: A total of 12 children (TD and pDCD; one female/11 male, x¯=10.36, SD ± 1.52 years) performed the two-dimensional and 3D conditions of the ToH disk tasks, with equivalent executive function but different motor requirements, with functional near-infrared spectroscopy to compare PFC activity. Results: Interestingly, brain oxygenation levels were more apparent in the 3D versus two-dimensional ToH. In the 3D, there were large differences between pairs of discordant sibling sets and this was located to the right medial PFC, with pDCD exhibiting less activation in this region. Conclusion: While only exploratory, we have identified potential differences in the right medial PFC region, which differs within sibling sets with different pDCD status. These results concur with previous studies and are an area that needs to be explored further with a larger cohort of TD and pDCD.

  • Collapse
  • Expand
  • Abibullaev, B., An, J., Jin, S.-H., & Moon, J.I. (2014). Classification of brain hemodynamic signals arising from visual action observation tasks for brain-computer interfaces: A functional near-infrared spectroscopy study. Measurement: Journal of the International Measurement Confederation, 49(1), 320328. https://doi.org/10.1016/j.measurement.2013.11.044

    • Search Google Scholar
    • Export Citation
  • Adams, I.L.J., Ferguson, G.D., Lust, J.M., Steenbergen, B., & Smits-Engelsman, B.C.M. (2016). Action planning and position sense in children with DCD. Human Movement Science, 46, 196208. https://doi.org/10.1016/j.humov.2016.01.006

    • Search Google Scholar
    • Export Citation
  • Adams, I.L.J., Lust, J.M., Wilson, P.H., & Steenbergen, B. (2017). Development of motor imagery and anticipatory action planning in children with DCD—A longitudinal approach. Human Movement Science, 55, 296306. https://doi.org/10.1016/j.himov.2017.08.021

    • Search Google Scholar
    • Export Citation
  • Alexander, W.H., & Brown, J.W. (2011). Medial prefrontal cortex as an action-outcome predictor. Nature Neuroscience, 14(10), Article 1338. https://doi.org/10.1038/nn.2921

    • Search Google Scholar
    • Export Citation
  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). American Psychiatric Association. https://10.1176/appi.books.9780890425596

    • Search Google Scholar
    • Export Citation
  • Ayaz, H. (2010). Functional near infrared spectroscopy based brain computer interface. (PhD Thesis). Drexel University.

  • Ayaz, H., Izzetoglu, M., Platek, S.M., Bunce, S., Izzetoglu, K., Pourrezaei, K., & Onaral, B. (2006). Registering fNIR data to brain surface image using MRI templates. International Conference of the IEEE Engineering in Medicine and Biology Society, 2006, 26712674. https://doi.org/10.1109/IEMBS.2006.260835

    • Search Google Scholar
    • Export Citation
  • Ayaz, H., Onaral, B., Izzetoglu, K., Shewokis, P.A., McKendrick, R., and Parasuraman, R. (2013). Continuous monitoring of brain dynamics with functional near infrared spectroscopy as a tool for neuroergonomic research: empirical examples and a technological development. Frontiers in Human Neuroscience, 7, 871. https://doi.org/10.3389/fnhum.2013.00871

    • Search Google Scholar
    • Export Citation
  • Ayaz, H., Shewokis, P.A., Bunce, S., Izzetoglu, K., Willems, B., and Onaral, B. (2012). Optical brain monitoring for operator training and mental workload assessment. Neuroimage, 59, 3647. https://doi.org/10.1016/j.neuroimage.2011

    • Search Google Scholar
    • Export Citation
  • Ayaz, H., Shewokis, P.A., Bunce, S.C., and Onaral, B. (2018). U.S. Patent No. 9,946,344. Washington, DC: U.S. Patent and Trademark Office.

    • Search Google Scholar
    • Export Citation
  • Ayaz, H., Shewokis, P., Curtin, A., Izzetoglu, M., Izzetoglu, K., & Onaral, B. (2011). Using MazeSuite and functional near infrared spectroscopy to study learning in spatial navigation. Journal of Visualized Experiments, 56, Article 3443. https://doi.org/10.3791/3443

    • Search Google Scholar
    • Export Citation
  • Bechara, A., & Damasio, A.R. (2005). The somatic marker hypothesis: A neural theory of economic decision. Games and Economic Behavior, 52(2), 336372. https://doi.org/10.1016/j.geb.2004.06.010

    • Search Google Scholar
    • Export Citation
  • Bhoyroo, R., Hands, B., Wilmut, K., Hyde, C., & Wigley, A. (2018). Investigating motor planning in children with DCD: Evidence from simple and complex grip selection tasks. Human Movement Science, 61, 4251. https://doi.org/10.1016/j.humov.2018.07.006

    • Search Google Scholar
    • Export Citation
  • Brown-Lum, M., & Zwicker, J.G. (2015). Brain imaging increases our undertsanding of Developmental Coordination Disorder: A review of literature and future directions. Current Developmental Disorder Reports, 2(2), 131140. https://doi.org/10.1007/s40474-015-0046-6

    • Search Google Scholar
    • Export Citation
  • Cabeza, R., & Kingstone, A. (Eds.). (2006). Handbook of functional neuroimaging of cognition. MIT Press.

  • Caçola, P., Getchell, N., Srinivasan, D., Alexandrakis, G., & Liu, H. (2018). Cortical activity in fine-motor tasks in children with Developmental Coordination Disorder: A preliminary fNIRS study. International Journal of Developmental Neuroscience, 65, 8390. http://doi.org/10.1016/j.ijdevneu.2017.11.001

    • Search Google Scholar
    • Export Citation
  • Cohen, R.G., & Rosenbaum, D.A. (2004). Where grasps are made reveals how grasps are planned: Generation and recall of motor plans. Experimental Brain Research, 157, 486495. https://doi.org/10.1007/s00221-004-1862-9

    • Search Google Scholar
    • Export Citation
  • Cope, M., & Delpy, D.T. (1988). Sytem for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination. Medical and Biological Engineering and Computing, 26, 289294. https://doi.org/10.1007/BF02447083

    • Search Google Scholar
    • Export Citation
  • Debrabant, J., Gheysen, F., Caeyenberghs, K., Vingerhoets, L.G., & Vingerhoets, G. (2013). Neural underpinnings of impaired predictive motor timing in children with Developmental Coordination Disorder. Research in Developmental Disabilities, 34(5), 14781487. https://doi.org/10.1016/j.ridd.2013.02.008

    • Search Google Scholar
    • Export Citation
  • de Castelnau, P., Albaret, J.-M., Chaix, Y., & Zanone, P.-G. (2008). A study of EEG coherenve in DCD children during motor synchronization task. Human Movement Science, 27(2), 230241. https://doi.org/10.1016/j.humov.2008.02.006

    • Search Google Scholar
    • Export Citation
  • Euston, D.R., Gruber, A.J., & McNaughton, B.L. (2012). The role of medial prefrontal cortex in memory and decision making. Neuron, 76(6), 105770. https://doi.org/10.1016/j.neuron.2012.12.002

    • Search Google Scholar
    • Export Citation
  • Ferrari, M., & Quaresima, V. (2012). A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. NeuroImage, 63(2), 921935. https://doi.org/10.1016/j.neuroimage.2012.03.049

    • Search Google Scholar
    • Export Citation
  • Fuelsher, I., Williams, J., Wilmut, K., Enticott, P.G., & Hyde, C. (2016). Modelling the maturation of grip selection planning and action representation: Insights from typical and atypical motor development. Frontiers in Psychology, 7, Article 108. https://doi.org/10.3389/fpsyg.2016.0018

    • Search Google Scholar
    • Export Citation
  • Getchell, N., & Liang, L.Y. (2018). Functional neuroimaging of prefrontal cortex activity during a problem solving versus motor task in children with and without autism. In H. Ayaz & F. Dehais (Eds.), Neuroergonomics: The brain at work and in everyday life. Elsevier Publishing. https://doi.org/10.1016/B978-0-12-811926-6.00080-4

    • Search Google Scholar
    • Export Citation
  • Haahr, M. (1998). True random service. Retrieved August 30, 2018, from https://www.random.org/integers/

  • Henderson, S.E., Sugden, D.A., & Barnett, A.L. (2007). Movement assessment battery for children – Second Edition [MABC-2]. The Psychological Coorporation.

    • Search Google Scholar
    • Export Citation
  • Hill, E.L. (2004). Executive dysfunction in autism. Trends in Cognitive Sciences, 8, 2632. https://doi.org/16.1016/j.tics.2003.11.003

    • Search Google Scholar
    • Export Citation
  • Hilton, C.L., Zhang, Y., Whilte, M.R., Klohr, C.L., & Constantino, J. (2012). Motor impairment in sibling pairs concordant and discordant for autism spectrum disorders. Autism, 16(4), 430441.

    • Search Google Scholar
    • Export Citation
  • Holroyd, C.B., Coles, M.G., & Nieuwenhuis, S. (2002). Medial prefrontal cortex and error potentials. Science, 296, 16101611.

  • Homan, R., Herman, J., & Purdy, P. (1987). Cerebral location of international 10-20 system electrode placement. Electroencephalography and Clinical Neurophysiology, 66(4), 376382. https://doi.org/10.1010/0013-4694(87)90206-9

    • Search Google Scholar
    • Export Citation
  • Hughes, C. (1996). Brief report: Planning problems in autism at the level of motor control. Journal of Autism and Developmental Disorders, 26, 99107. https://doi.org/10.1007/BF02276237

    • Search Google Scholar
    • Export Citation
  • Huhn, A.S., Sweeney, M.M., Brooner, R.K., Kidorf, M.S., Tompkins, D.A., Ayaz, H., & Dunn, K.E. (2018). Prefrontal cortex response to drug cues, craving, and current depressive symptoms are associated with treatment outcomes in methadone-maintained patients. Neuropsychopharmacology, 44(4), 826833. https://doi.org/10.1038/s41386-018-0252-0

    • Search Google Scholar
    • Export Citation
  • Hyde, C., & Wilson, P.H. (2011). Dissecting online control in Developmental Coordination Disorder: A kinematic analysis of double-step reaching. Brain and Cognition, 75(3), 232241. https://doi.org/10.1016/j.bandc.2010.12.004

    • Search Google Scholar
    • Export Citation
  • Irani, F.P., Platek, S.M., Bunce, S., Ruocco, A.C., & Chute, D. (2007). Functional Near Infrared Spectroscopy (fNIRS): An emerging neuroimaging technology with important applications for the study of brain disorders. The Clinical Neuropsychologist, 21(1), 937. https://doi.org/10.1080/13854040600910018

    • Search Google Scholar
    • Export Citation
  • Izzetoglu, M., Bunce, S.C., Izzetoglu, K., Onaral, B., & Pourrezaei, K. (2007). Functional brain imaging using near-infrared technology. IEEE Engineering in Medicine and Biology Magazine, 26(4), 3846.

    • Search Google Scholar
    • Export Citation
  • Jonides, J., Smith, E.E., Koeppe, R.A., Awh, E., Minoshima, S., & Mintun, M.A. (1993). Spatial working memory in humans as revealed by PET. Nature, 363, 623625.

    • Search Google Scholar
    • Export Citation
  • Kawato, M. (1999). Internal models for motor control and trajectory planning. Current Opinion in Neurobiology, 9, 718727. https://doi.org/10.1016/S0959-4388(99)00028-8

    • Search Google Scholar
    • Export Citation
  • Kim, H.Y., Seo, K., Jeon, H.J., Lee, U., & Lee, H. (2017). Application of functional near-infrared spectroscopy to the study of brain function in humans and animal models. Molecules and Cells, 40(8), 523532. https://doi.org/10.14348/molcells.2017

    • Search Google Scholar
    • Export Citation
  • Kuhtz-Buschbeck, J.P., Mahnkopf, C., Holzknecht, C., Siebner, H., Ulmer, S., & Jansen O. (2003). Effector-independent representations of simple and complex imagined finger movements: A combined fMRI and TMS study. The European Journal of Neuroscience, 18(12), 33753387. https://doi.org/10.1111/j.1460-9568.2003.03066.x

    • Search Google Scholar
    • Export Citation
  • Liang, L.Y., Shewokis, P., & Getchell, N. (2016). Brain activation in the prefrontal cortex during motor and cognitive tasks in adults. Journal of Behavioral and Brain Science, 6, 463474. https://doi.org/10.4236/jbbs.2016.612042

    • Search Google Scholar
    • Export Citation
  • Milla, K., Bakhshipour, E., Bodt, B., & Getchell, N. (2019). Does movement matter? Prefrontal cortex activity during 2D vs. 3D performance of the Tower of Hanoi puzzle. Frontiers in Human Neuroscience, 13, Article 156. https://doi.org/10.3389/fnhum.2019.00156

    • Search Google Scholar
    • Export Citation
  • Miller, E.K., & Cohen, J.D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24(1), 167202. https://doi.org/10.1146/annurev.neuro.24.1.167

    • Search Google Scholar
    • Export Citation
  • Mushiake, H.S., Sakamoto, K., Saito, N., Inui, T., Aihara, K., & Tanji, J. (2009). Involvement of the prefrontal cortex in problem solving. International Review of Neurobiology, 85, 111. https://doi.org/10.1016/S0074-7742(09)85001-0

    • Search Google Scholar
    • Export Citation
  • Narayanan, N.S., & Laubach, M. (2006). Top-down control of motor cortex ensembles by dorsomedial prefrontal cortex. Neuron, 52(5), 921931. https://doi.org/10.1016/j.neuron.2006.10.021

    • Search Google Scholar
    • Export Citation
  • Nolen, M., Wilson, P., Ruddock, J., & Steenbergen, B. (2014). Mild impairments of motor imagery skills in children with DCD. Research in Developmental Disorders, 35, 11521159. https://doi.org/10.1016/j.ridd.2014.01.0626

    • Search Google Scholar
    • Export Citation
  • Pardo, J.V., Fox, P.T., & Raichle, M.E. (1991) Localization of a human system for sustained attention by positron emission tomography. Nature, 349, 6164.

    • Search Google Scholar
    • Export Citation
  • Plumb, M.S., Wilson, A.D., Mulroue, A., Brockman, A., Williams, J.H.G., & Mon-Williams, M. (2008). Online corrections in children with and without DCD. Human Movement Science, 27(5), 695704. https://doi.org/10.1016/j.humov.2007.11.004

    • Search Google Scholar
    • Export Citation
  • Posner, M.I., Rothbart, M. K., Sheese, B.E., & Tang, Y. (2007). The anterior cingulate gyrus and the mechanism of self- regulation. Cognitive, Affective & Behavioral Neuroscience, 7, 391395. https://doi.org/10.3758/cabn.7.4.391

    • Search Google Scholar
    • Export Citation
  • Reddy, P., Shewokis, P.A., & Izzetoglu, K. (2022). Individual differences in skill acquisition and transfer assessed by dual task training performance and brain activity. Brain Informatics, 9, Article 9. https://doi.org/10.1186/s40708‐022‐00157‐5

    • Search Google Scholar
    • Export Citation
  • Ridderinkhof, K.R., Ullsperger, M., Crone, E.A, & Nieuwenhuis, S. (2004). The role of the medial frontal cortex in cognitive control. Science, 306, 443447.

    • Search Google Scholar
    • Export Citation
  • Rosenbaum, D.A., Marchak, F., Barnes, H.J., Vaughan, J., Slotta, J., & Jorgensen, M. (1990). Constraints for action selection: Overhand versus underhand grips. In M. Jeannerod (Ed.), Attention and performance XIII: Motor representation and control (pp. 321342). Lawrence Erlbaum Associates.

    • Search Google Scholar
    • Export Citation
  • Rosenbaum, D.A., Vaughan, J., Jorgensen, M.J., Barnes, H.J., & Stewart, E. (1993). Plans for object manipulation. In D.E. Meyer & S. Kornblum (Eds.), Attention and performance XIV—A silver jubilee: Synergies in experimental psychology, artificial intelligence and cognitive neuroscience (pp. 803820). MIT Press, Bradford Books.

    • Search Google Scholar
    • Export Citation
  • Salesforce Company. (2018). Heroku development center. https://devcenter.heroku.com/articles/heroku-dashboard

  • Scarr, S., & Grajek, S. (1982). Similarities and differences among siblings. In M.E. Lamb, B. Sutton-Smith, Brian Sutton-Smith, & Michael E. Lamb (Eds.), Sibling relationships: Their nature and significance across the lifespan (pp. 357381). Psychology Press.

    • Search Google Scholar
    • Export Citation
  • Scheres, A., Oosterlann, J., Geurts, H., Morein-Zamir, J., Meiran, N., Schut, H., Vlasved, L., & Sergeant, J. (2004). Executive functioning in boys with ADHD: Primarily an inhibition deficit? Archive of Clinical Neuropsychology, 19, 569594. https://doi.org/10.1016/j.acn.2003.08.005

    • Search Google Scholar
    • Export Citation
  • Schielzeth, H., Dingemanse, N., Nakagawa, S., Westneat, D., Allegue, H., Teplitsky, C., Réale, D., Dochtermann, N., Garamszegi, L., & Araya-Ajoy, Y. (2020). Robustness of linear mixed-effects models to violations of distributional assumptions. Methods in Ecology and Evolution, 11(9), 11411152. http://doi.org/10.1111/2041-210X.13434

    • Search Google Scholar
    • Export Citation
  • Scholkmann, F., Kleiser, S., Zimmermann, R., Mata Pavia, J., Wolf, U., & Wolf, M. (2014). A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. Neuroimage, 85(1), 627. https://doi.org/10.1016/j.neuroimage

    • Search Google Scholar
    • Export Citation
  • Shimoda, K., Moriguchi, Y., Tsuchiya, K., Katsuyama, S., & Tozato, F. (2014). Activation of the pre-frontal cortex while performing a task at preferred slow pace and metronome slow pace: A functional near-infrared spectroscopy study. Neural Plasticity, 2014, Article 269120. https://doi.org/10.1155/2014/269120

    • Search Google Scholar
    • Export Citation
  • Smits-Engelsman, B.C.M., Wilson, P.H., Westenberg, Y., & Duysens, J. (2003). Fine motor deficiencies in children with Developmental Coordination Disorder and learning disabilities: An underlying open-loop control deficit. Human Movement Science, 22(4–5), 495513. https://doi.org/10.1016/j.humov.2003.09.006

    • Search Google Scholar
    • Export Citation
  • Smyth, M., & Mason, U. (1997). Planning and execution of action in children with and without developmental coordination disorder. Journal of Child Psychology and Psychiatry, 38, 10231037. https://doi.org/10.1111/j.1469-7610.1997.tb01619.x

    • Search Google Scholar
    • Export Citation
  • Strangman, G., Culver, J.P., Thompson, J.H., & Boas, D.A. (2002). A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. NeuroImage, 17, 719731. https://doi.org/10.1006/nimg.2002.1227

    • Search Google Scholar
    • Export Citation
  • van Swieten, L.M., van Bergen, E., Williams, J.H.G., Wilson, A.D., Plumb, M.S., Kent, S.W., & Mon-Williams, M.A. (2010). A test of motor (not executive) planning in developmental coordination disorder. Journal of Experimental Psychology: Human Perception and Performance, 36, 493499. https://doi.org/10.1037/a0017177

    • Search Google Scholar
    • Export Citation
  • Welsh, M., & Huizinga, M. (2001). The development and preliminary validation of the Tower of Hanoi-Revised. Assessment, 8(2), 167176. https://doi.org/10.1177/107319110100800205

    • Search Google Scholar
    • Export Citation
  • Welsh, M., & Huizinga, M. (2005). Tower of Hanoi disk-transfer task: Influences of strategy knowledge and learning on performance. Learning and Individual Differences, 15, 28398. https://doi.org/10.1016/j.lindif.2005.05.002

    • Search Google Scholar
    • Export Citation
  • Wilcox, T., & Biondi, M. (2015). fNIRS in developmental sciences. Wiley InterdisciplinaryReviews: Cognitive Science, 6(3), 263283. https://doi.org/10.1002/wcs.143

    • Search Google Scholar
    • Export Citation
  • Wilmut, K., & Byrne, M. (2014). Grip selection for sequential movements in children and adults with and without DCD. Human Movement Science, 36, 272284. https://doi.org/10.1016/j.humov.2013.07.015

    • Search Google Scholar
    • Export Citation
  • Wilson, P.H., Smits‐Engelsman, B., Caeyenberghs, K., Steenbergen, B., Sugden, D., Clark, J., Mumford, N., & Blank, R. (2017). Cognitive and neuroimaging findings in developmental coordination disorder: New insights from a systematic review of recent research. Developmental Medicine & Child Neurology, 59(11), 11171129. https://doi.org/10.1111/dmcn.13530

    • Search Google Scholar
    • Export Citation
  • Wood, J., & Grafman, J. (2003). Human prefrontal cortex: Processing and representational perspectives. Nature Reviews Neuroscience, 4, 139147. https://doi.org/10.1038/nrn1033

    • Search Google Scholar
    • Export Citation
  • Yin, X., Xu, B., Jiang, C., Fu, Y., Wang, Z., Li, H., & Shi, G. (2015). A hybrid BCI based on EEG and fNIRS signals improves the performance of decoding motor imagery of both force and speed of hand clenching. Journal of Neural Engineering, 12(3), Article 36004. https://doi.org/10.1088/1741-2560/12/3/036004

    • Search Google Scholar
    • Export Citation
  • Zhang, H., Duan, L., Zhang, Y.J., Lu, C.M., Liu, H., & Zhu, C.Z. (2011). Test-retest assessment of independent component analysis-derived resting-state functional connectivity based on functional near-infrared spectroscopy. NeuroImage, 55, 607615. https://doi.org/10.1016/j.neuroimage.2010.12.007

    • Search Google Scholar
    • Export Citation
  • Zhang, H., Zhang, Y.-J., Lu, C.-M., Ma, S.-Y., Zang, Y.-F., & Zhu, C.-Z. (2010). Functional connectivity as revealed by independent component analysis of resting-state fNIRS measurements. NeuroImage, 51(3), 11501161. https://doi.org/10.1016/j.neuroimage.2010.02.080

    • Search Google Scholar
    • Export Citation
  • Zwicker, J.G., Missiuna, C., Harris, S.R., & Boyd, L.A. (2011). Brain activation associated with motor skill practice in children with Developmental Coordination Disorder: An fMRI study. International Society for Developmental Neuroscience, 29(2), 145152. https://doi.org/10.1016/j.ijdevneu.2010.12.002

    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 991 783 18
Full Text Views 394 180 0
PDF Downloads 94 10 0