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Developmental Trajectory of Beta Cortical Oscillatory Activity During a Knee Motor Task

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Abstract

There is currently a void in the scientific literature on the cortical beta oscillatory activity that is associated with the production of leg motor actions. In addition, we have limited data on how these cortical oscillations may progressively change as a function of development. This study began to fill this vast knowledge gap by using high-density magnetoencephalography to quantify the beta cortical oscillatory activity over a cross-section of typically developing children as they performed an isometric knee target matching task. Advanced beamforming methods were used to identify the spatiotemporal changes in beta oscillatory activity during the motor planning and motor action time frames. Our results showed that a widespread beta event-related desynchronization (ERD) was present across the pre/postcentral gyri, supplementary motor area, and the parietal cortices during the motor planning stage. The strength of this beta ERD sharply diminished across this fronto-parietal network as the children initiated the isometric force needed to match the target. Rank order correlations indicated that the older children were more likely to initiate their force production sooner, took less time to match the targets, and tended to have a weaker beta ERD during the motor planning stage. Lastly, we determined that there was a relationship between the child’s age and the strength of the beta ERD within the parietal cortices during isometric force production. Altogether our results suggest that there are notable maturational changes during childhood and adolescence in beta cortical oscillatory activity that are associated with the planning and execution of leg motor actions.

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References

  • Alegre M, Labarga A, Gurtubay IG, Iriarte J, Malanda A, Artieda J (2002) Beta electroencephalograph changes during passive movements: sensory afferences contribute to beta event-related desynchronization in humans. Neurosci Lett 331(1):29–32

    Article  CAS  PubMed  Google Scholar 

  • Alegre M, Gurtubay IG, Labarga A, Iriarte J, Malanda A, Artieda J (2003) Alpha and beta oscillatory changes during stimulus-induced movement paradigms: effect of stimulus predictability. Neuroreport 14(3):381–385

    Article  PubMed  Google Scholar 

  • Barry RL, Williams JM, Klassen LM, Gallivan JP, Culham JC, Menon RS (2010) Evaluation of preproscessing steps to compensate for magnetic field distortions due to body movements in BOLD fMRI. Magn Reson Imaging 28:235–244

    Article  PubMed  Google Scholar 

  • Beurze SM, de Lange FP, Toni I, Medendrop WP (2007) Integration of target and effector information in the human brain during reach planning. J Neurophys 97:188–199

    Article  CAS  Google Scholar 

  • Bueti D, Walsh V, Frith C, Rees G (2008) Different brain circuits underlie motor and perceptual representations of temporal intervals. J Cogn Neurosci 20(2):204–214

    Article  PubMed  Google Scholar 

  • Buneo CA, Anderson RA (2006) The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements. Neuropsychologia 44:2594–2606

    Article  PubMed  Google Scholar 

  • Cassim F, Szurhaj W, Sediri H, Devos D, Bourriez JL, Poirot I, Derambure P, Defebvre L, Guieu JD (2000) Brief and sustained movements: differences in event-related (de)synchronization (ERD/ERS) patterns. Clin Neurophys 111:2032–2039

    Article  CAS  Google Scholar 

  • Ciccarelli O, Toosy AT, Marsden JF, Wheeler-Kinshott CM, Sahyoun C, Matthews PM, Miller DH, Thompson AJ (2005) Identifying brain regions for integrative sensorimotor processing with ankle movements. Exp Brain Res 166:31–42

    Article  CAS  PubMed  Google Scholar 

  • Contreras-Vidal JL, Bo J, Boudreau JP, Clark JE (2005) Development of visuomotor representations for hand movement in young children. Exp Brain Res 162(2):155–164

    Article  PubMed  Google Scholar 

  • Crone NE, Miglioretti DL, Gordon B, Lesser RP (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121:2301–2315

    Article  PubMed  Google Scholar 

  • Davies BL, Gehringer JE, Kurz MJ (2015) Age-related differences in the motor planning of a lower leg target matching task. Hum Mov Sci 44:299–306

    Article  PubMed  Google Scholar 

  • De Almeida PMD, Vieira AICMD, Canario NIS, Castelo-Branco M, Caldas ALD (2015) Brain activity during lower-limb movement with manual facilitation: an fMRI study. Neurol Res Int 701452:1–14

    Article  Google Scholar 

  • Della-Maggiore V, Malfait N, Ostry DJ, Paus T (2004) Stimulation of the posterior parietal cortex interferes with arm trajectory adjustments during the learning of new dynamics. J Neurosci 24(44):9971–9976

    Article  CAS  PubMed  Google Scholar 

  • Dobkin BH, Firestine A, West M, Saremi K, Woods R (2004) Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. NeuroImage 23:370–381

    Article  PubMed  PubMed Central  Google Scholar 

  • Ernst MD (2004) Permutation methods: a basis for exact inference. Stat Sci 19(4):676–685

    Article  Google Scholar 

  • Gaetz W, MacDonald M, Cheyne D, Snead OC (2010) Neuromagnetic imaging of movement-related cortical oscillations in children and adults: age predicts post-movement beta rebound. NeuroImage 51:792–807

    Article  CAS  PubMed  Google Scholar 

  • Gaetz W, Edgar JC, Wang DJ, Roberts TP (2011) Relating MEG measured motor cortical oscillation to resting γ-aminobutyric acid (GABA) concentration. NeuroImage 55(2):616–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallivan JP, McLean DA, Valyear KF, Pettypiece CE, Culham J (2011) Decoding action intentions from preparatory brain activity in human parieto-frontal networks. J Neurosci 31(26):9599–9610

    Article  CAS  PubMed  Google Scholar 

  • Gallivan JP, McLean DA, Flanagan JR, Culham JC (2013) Where one hand meets the other: limb-specific and action-dependent movement plans decoded from preparatory signals in single human frontoparietal brain areas. J Neurosci 33(5):1991–2008

    Article  CAS  PubMed  Google Scholar 

  • Grent-’t-Jong T, Oostenveld R, Jensen O, Medendorp WP, Praamstra P (2014) Competitive interactions in sensorimotor cortex: oscillations express separation between alternative movement targets. J Neurophys 112(2):224–232

    Article  Google Scholar 

  • Gross J, Kujala J, Hamalainen M, Timmermann L, Schnitzler A, Salmelin R (2001) Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Nat Acad Sci 98:694–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall SD, Standford IM, Yamawaki N, McAllister N, Ronnqvist KC, WoodHall GL, Furlong PL (2011) The role of GABAergic modulation in motor function related neuronal network activity. NeuroImage 56:1506–1510

    Article  CAS  PubMed  Google Scholar 

  • Heinrichs-Graham E, Wilson TW (2015a) Spatiotemporal oscillatory dynamics during the encoding and maintenance of a visual working memory task. Cortex 69:121–130

    Article  PubMed  PubMed Central  Google Scholar 

  • Heinrichs-Graham E, Wilson TW (2015b) Coding complexity in the human motor circuit. Hum Brain Mapp 36(12):5155–5167

    Article  PubMed  Google Scholar 

  • Heinrichs-Graham E, Wilson TW, Santamaria PM, Heithoff SK, Torres-Russotto D, Hutter-Saunders JA, Estes KA, Meza JL, Mosley RL, Gendelman HE (2014) Neuromagnetic evidence of abnormal movement-related beta desynchronization in Parkinson’s disease. Cereb Cortex 24(10):2669–2678

    Article  PubMed  Google Scholar 

  • Heinrichs-Graham E, Arpin DJ, Wilson TW (2016) Cue-related temporal factors modulate movement-related beta oscillatory activity in the human motor circuit. J Cogn Neurosci 11:1–13

    Google Scholar 

  • Hillebrand A, Singh KD, Holliday IE, Furlong PL, Barnes GR (2005) A new approach to neuroimaging with magnetoencephalography. Hum Brain Mapp 25:199–211

    Article  PubMed  Google Scholar 

  • Johannsen P, Christensen LOD, Sinkjaer T, Nielsen JB (2001) Cerebral functional anatomy of voluntary contractions of ankle muscles in man. J Physiol 535:397–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurkiewicz MT, Gaetz WC, Bostan AC, Cheyne D (2006) Post-movement beta rebound is generated in the motor cortex: evidence from neuromagnetic recordings. NeuroImage 32:1281–1289

    Article  PubMed  Google Scholar 

  • Kaiser J, Birbaumer N, Lutzenberger W (2001) Event-related beta desynchroniztion indicates timing of response selection in a delayed-response paradigm in humans. Neurosci Lett 312:149–152

    Article  CAS  PubMed  Google Scholar 

  • Kapreli E, Athanasopoulos S, Papathanasiou M, van Hecke P, Strimpakos N, Gouliamos A, Peeters R, Sunaert S (2006) Lateralization of brain activity during lower limb joint movement. An fMRI study. NeuroImage 32:1709–1721

    Article  PubMed  Google Scholar 

  • Kilner J, Bott L, Posada A (2005) Modulations in the degree of synchronization during ongoing oscillatory activity in the human brain. Eur J Neurosci 21:2547–2554

    Article  PubMed  Google Scholar 

  • Kurz MJ, Becker KM, Heinrichs-Graham E, Wilson TW (2014a) Neurophysiological abnormalities in the sensorimotor cortices during the motor planning and movement execution stages of children with cerebral palsy. Dev Med Child Neurol 56(11):1072–1077

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurz MJ, Heinrichs-Graham E, Arpin DJ, Becker KM, Wilson TW (2014b) Aberrant synchrony in the somatosensory cortices predicts motor performance errors in children with cerebral palsy. J Neurophysiol 111(3):573–579

    Article  PubMed  Google Scholar 

  • Kurz MJ, Becker KM, Heinrichs-Graham E, Wilson TW (2015a) Children with cerebral palsy have uncharacterisitc somatosensory cortical oscillations after mechanoreceptor stimulation. Neuroscience 305:67–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurz MJ, Heinrichs-Graham E, Becker KM, Wilson TW (2015b) The magnitude of somatosensory cortical activity is related to the mobilty and strength impairments seen in children with cerebral palsy. J Neurophysiol 113:3143–3150

    Article  PubMed  PubMed Central  Google Scholar 

  • Luft AR, Smith GV, Forrester L, Whitall J, Macko RF, Hauser TK, Goldberg AP, Hanley DF (2002) Comparing brain activation associated with isolated upper and lower limb movement across corresponding joints. Hum Brain Mapp 17:131–140

    Article  PubMed  Google Scholar 

  • MacIntosh BJ, Mraz R, Baker N, Staines WR, Graham SJ (2004) Optimizing the experimental design for ankle dorsiflexion fMRI. NeuroImage 22:1619–1627

    Article  PubMed  Google Scholar 

  • Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164(1):177–190

    Article  PubMed  Google Scholar 

  • Miller KJ, Leuthardt EC, Schalk G, Rao RPN, Anderson NR, Moran DW, Miller JW, Ojemann JG (2007) Spectral changes in cortical surface potentials during motor movement. J Neurosci 27(9):2424–2432

    Article  CAS  PubMed  Google Scholar 

  • Muthukumaraswamy SD, Myers JFM, Wilson SJ, Nutt DJ, Lingford-Hughes A (2013) The effect of elevated endogenous GABA levels on movement related network oscillations. NeuroImage 66:36–41

    Article  CAS  PubMed  Google Scholar 

  • Neuper C, Pfurtscheller G (1996) Post-movement synchronization of beta rhythms in the EEG over the cortical foot area in man. Neurosci Lett 216:17–20

    Article  CAS  PubMed  Google Scholar 

  • Neuper C, Pfurtscheller G (2001) Evidence for distinct beta resonance frequencies in human EEG related to specific sensorimotor cortical areas. Clin Neurophys 112:2084–2097

    Article  CAS  Google Scholar 

  • Pfurtscheller G, Berghold A (1989) Patterns of cortical activation during planning of voluntary movement. Electroencephalogr Clin Neurophysiol 72(3):250–258

    Article  CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Graimann B, Huggins JE, Levine SP, Schuh LA (2003) Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophys 114:1226–1236

    Article  CAS  Google Scholar 

  • Proskovec AL, Heinrichs-Graham E, Wilson TW (2016) Aging modulates the oscillatory dynamics underlying successful working memory encoding and maintenance. Hum Brain Mapp 37:2348–2361

    Article  PubMed  Google Scholar 

  • Sahyoun C, Floyer-Lea A, Johansen-Berg H, Matthews PM (2004) Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. NeuroImage 21:568–575

    Article  CAS  PubMed  Google Scholar 

  • Scantlebury M, Cunningham T, Dockstader C, Laughlin S, Gaetz W, Rockel C, Dickson J, Mabbott D (2014) Relations between white matter maturation and reaction time in childhood. J Int Neuropsychol Soc 20:99–112

    Article  PubMed  Google Scholar 

  • Seto E, Sela G, McIlroy WE, Black SE, Staines WR, Bronskill MJ, McIntosh AR, Graham SJ (2001) Quantifying head motion associated with motor tasks used in fMRI. NeuroImage 14:284–297

    Article  CAS  PubMed  Google Scholar 

  • Shadmehr R (2004) Generalization as a behavioral window to the neural mechanisms of learning internal models. Hum Mov Sci 23:543–568

    Article  PubMed  PubMed Central  Google Scholar 

  • Talairach G, Tournoux P (1998) Co-planar stereotaxic atlas of the human brain. Thieme, New York

    Google Scholar 

  • Taulu S, Simola J (2006) Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Phys Med Biol 51(7):1759–1768

    Article  CAS  PubMed  Google Scholar 

  • Tzagarakis C, Ince NF, Leuthold AC, Pellizzer GP (2010) Beta-band activity during motor planning reflects response uncertainty. J Neurosci 30(4):11270–11277

    Article  CAS  PubMed  Google Scholar 

  • Tzagarakis C, West S, Pellizzer G (2015) Brain oscillatory activity during motor preparation: effect of directional uncertainty on beta, but not alpha, frequency band. Front Neurosci 9(1–13):2015

    Google Scholar 

  • Valyear KF, Frey SH (2015) Human posterior parietal cortex mediates hand-specific planning. NeuroImage 114:226–238

    Article  PubMed  PubMed Central  Google Scholar 

  • van Veen BD, van Drongelen W, Yuchtman M, Suzuki A (1997) Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans Biomed Eng 44:867–880

    Article  PubMed  Google Scholar 

  • Wheaton LA, Carpenter M, Mizelle JC, Forrester L (2008) Preparatory band specific premotor cortical activity differentiates upper and lower extremity movement. Exp Brain Res 184:121–126

    Article  PubMed  Google Scholar 

  • Wilson TW, Slason E, Asherin R, Kronberg E, Teale PD, Reite ML, Rojas DC (2010) An extended motor network generates beta and gamma oscillatory perturbations during development. Brain Cogn 73(2):75–84

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson TW, Slason E, Asherin R, Kronberg E, Teale PD, Reite ML, Rojas DC (2011) Abnormal gamma and beta MEG activity during finger movements in early-onset psychosis. Dev Neuropsychol 36(5):596–613

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson TW, Heinrichs-Graham E, Becker KM (2014) Circadian modulation of motor- related beta oscillatory responses. NeuroImage 102:531–539

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson TW, Heinrichs-Graham E, Becker KM, Aloi J, Robertson KR, Sandkovsky U, White ML, O’Neill J, Knott NL, Fox HS, Swindells S (2015) Multimodal neuroimaging evidence of alterations in cortical structure and function in HIV-infected older adults. Hum Brain Mapp 36(3):897–910

    Article  PubMed  Google Scholar 

  • Wilson TW, Heinrichs-Graham E, Proskovec AL, McDermott TJ (2016) Neuroimaging with magnetoencephalography: a dynamic view of brain pathophysiology. Transl Res. doi:10.1016/j.trsl.2016.01.007

    Google Scholar 

  • Wolpert DM (2007) Probabilistic models in human sensorimotor control. Hum Move Sci 26:511–524

    Article  Google Scholar 

  • Yan JH, Thomas JR, Stelmach GE, Thomas KT (2000) Developmental features of rapid aiming arm movements across the lifespan. J Motor Behav 32(2):121–140

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by Grants from the National Institutes of Health (5R21-HD077532, 1R01-HD086245) and the National Science Foundation (NSF 1539067).

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Correspondence to Max J. Kurz.

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Kurz, M.J., Proskovec, A.L., Gehringer, J.E. et al. Developmental Trajectory of Beta Cortical Oscillatory Activity During a Knee Motor Task. Brain Topogr 29, 824–833 (2016). https://doi.org/10.1007/s10548-016-0500-8

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  • DOI: https://doi.org/10.1007/s10548-016-0500-8

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