Skip to main content
Log in

High Gamma Oscillations of Sensorimotor Cortex During Unilateral Movement in the Developing Brain: a MEG Study

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Recent studies in adults have found consistent contralateral high gamma activities in the sensorimotor cortex during unilateral finger movement. However, no study has reported on this same phenomenon in children. We hypothesized that contralateral high gamma activities also exist in children during unilateral finger movement. Sixty normal children (6–17 years old) were studied with a 275-channel MEG system combined with synthetic aperture magnetometry (SAM). Sixty participants displayed consistently contralateral event-related synchronization (C-ERS) within high gamma band (65–150 Hz) in the primary motor cortices (M1) of both hemispheres. Interestingly, nineteen younger children displayed ipsilateral event-related synchronization (I-ERS) within the high gamma band (65–150 Hz) just during their left finger movement. Both I-ERS and C-ERS were localized in M1. The incidence of I-ERS showed a significant decrease with age. Males had significantly higher odds of having ipsilateral activity compared to females. Noteworthy, high gamma C-ERS appeared consistently, while high gamma I-ERS changed with age. The asymmetrical patterns of neuromagnetic activities in the children’s brain might represent the maturational lateralization and/or specialization of motor function. In conclusion, the present results have demonstrated that contralateral high-gamma neuromagnetic activities are potential biomarkers for the accurate localization of the primary motor cortex in children. In addition, the interesting finding of the ipsilateral high-gamma neuromagnetic activities opens a new window for us to understand the developmental changes of the hemispherical functional lateralization in the motor system.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aramaki Y, Honda M, Sadato N (2006) Suppression of the non-dominant motor cortex during bimanual symmetric finger movement: a functional magnetic resonance imaging study. Neuroscience 141:2147–2153

    Article  CAS  PubMed  Google Scholar 

  • Armatas CA, Summers JJ (2001) The influence of task characteristics on the intermanual asymmetry of motor overflow. J Clin Exp Neuropsychol 23:557–567

    Article  CAS  PubMed  Google Scholar 

  • Armatas CA, Summers JJ, Bradshaw JL (1994) Mirror movements in normal adult subjects. J Clin Exp Neuropsychol 16:405–413

    Article  CAS  PubMed  Google Scholar 

  • Armatas CA, Summers JJ, Bradshaw JL (1996) Handedness and performance variability as factors influencing mirror movement occurrence. J Clin Exp Neuropsychol 18:823–835

    Article  CAS  PubMed  Google Scholar 

  • Cernacek J (1961) Contralateral motor irradiation–cerebral dominance. Its changes in hemiparesis. Arch Neurol 4:165–172

    CAS  PubMed  Google Scholar 

  • Chen R, Gerloff C, Hallett M, Cohen LG (1997) Involvement of the ipsilateral motor cortex in finger movements of different complexities. Ann Neurol 41:247–254

    Article  CAS  PubMed  Google Scholar 

  • Cheyne D, Bakhtazad L, Gaetz W (2006) Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event-related beamforming approach. Hum Brain Mapp 27:213–229

    Article  PubMed  Google Scholar 

  • Cheyne D, Bells S, Ferrari P, Gaetz W, Bostan AC (2008) Self-paced movements induce high-frequency gamma oscillations in primary motor cortex. Neuroimage 42:332–342

    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(Pt 12):2301–2315

    Article  PubMed  Google Scholar 

  • Crone NE, Hao L, Hart J Jr, Boatman D, Lesser RP, Irizarry R, Gordon B (2001) Electrocorticographic gamma activity during word production in spoken and sign language. Neurology 57:2045–2053

    CAS  PubMed  Google Scholar 

  • Crone NE, Sinai A, Korzeniewska A (2006) High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res 159:275–295

    Article  PubMed  Google Scholar 

  • Dalal SS, Guggisberg AG, Edwards E, Sekihara K, Findlay AM, Canolty RT, Berger MS, Knight RT, Barbaro NM, Kirsch HE, Nagarajan SS (2008) Five-dimensional neuroimaging: localization of the time-frequency dynamics of cortical activity. Neuroimage 40:1686–1700

    Article  PubMed  Google Scholar 

  • Davies PL, Rose JD (2000) Motor skills of typically developing adolescents: awkwardness or improvement? Phys Occup Ther Pediatr 20:19–42

    CAS  PubMed  Google Scholar 

  • Denckla MB (1973) Development of speed in repetitive and successive finger-movements in normal children. Dev Med Child Neurol 15:635–645

    Article  CAS  PubMed  Google Scholar 

  • Denckla MB (1974) Development of motor co-ordination in normal children. Dev Med Child Neurol 16:729–741

    Article  CAS  PubMed  Google Scholar 

  • Dorfberger S, di-Japha E, Karni A (2009) Sex differences in motor performance and motor learning in children and adolescents: an increasing male advantage in motor learning and consolidation phase gains. Behav Brain Res 198:165–171

    Article  PubMed  Google Scholar 

  • Haaland KY, Harrington DL (1994) Limb-sequencing deficits after left but not right hemisphere damage. Brain Cogn 24:104–122

    Article  CAS  PubMed  Google Scholar 

  • Hayashi MJ, Saito DN, Aramaki Y, Asai T, Fujibayashi Y, Sadato N (2008) Hemispheric asymmetry of frequency-dependent suppression in the ipsilateral primary motor cortex during finger movement: a functional magnetic resonance imaging study. Cereb Cortex 18:2932–2940

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kaiser J, Lutzenberger W (2003) Induced gamma-band activity and human brain function. Neuroscientist 9:475–484

    Article  PubMed  Google Scholar 

  • Kaiser J, Lutzenberger W (2005) Human gamma-band activity: a window to cognitive processing. Neuroreport 16:207–211

    Article  PubMed  Google Scholar 

  • Kuhtz-Buschbeck JP, Sundholm LK, Eliasson AC, Forssberg H (2000) Quantitative assessment of mirror movements in children and adolescents with hemiplegic cerebral palsy. Dev Med Child Neurol 42:728–736

    Article  CAS  PubMed  Google Scholar 

  • Largo RH, Fischer JE, Rousson V (2003) Neuromotor development from kindergarten age to adolescence: developmental course and variability. Swiss Med Wkly 133:193–199

    CAS  PubMed  Google Scholar 

  • Larson JC, Mostofsky SH, Goldberg MC, Cutting LE, Denckla MB, Mahone EM (2007) Effects of gender and age on motor exam in typically developing children. Dev Neuropsychol 32:543–562

    PubMed  Google Scholar 

  • Liederman J, Foley LM (1987) A modified finger lift test reveals an asymmetry of motor overflow in adults. J Clin Exp Neuropsychol 9:498–510

    Article  CAS  PubMed  Google Scholar 

  • Lotze M, Sauseng P, Staudt M (2009) Functional relevance of ipsilateral motor activation in congenital hemiparesis as tested by fMRI-navigated TMS. Exp Neurol 217:440–443

    Article  CAS  PubMed  Google Scholar 

  • Mayston MJ, Harrison LM, Stephens JA (1999) A neurophysiological study of mirror movements in adults and children. Ann Neurol 45:583–594

    Article  CAS  PubMed  Google Scholar 

  • McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303–1311

    Article  CAS  PubMed  Google Scholar 

  • Muller K, Kass-Iliyya F, Reitz M (1997) Ontogeny of ipsilateral corticospinal projections: a developmental study with transcranial magnetic stimulation. Ann Neurol 42:705–711

    Article  CAS  PubMed  Google Scholar 

  • Nass R (1985) Mirror movement asymmetries in congenital hemiparesis: the inhibition hypothesis revisited. Neurology 35:1059–1062

    CAS  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Pfurtscheller G (2003) Induced oscillations in the alpha band: functional meaning. Epilepsia 44(Suppl 12):2–8

    Article  PubMed  Google Scholar 

  • Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857

    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 Neurophysiol 114:1226–1236

    Article  CAS  PubMed  Google Scholar 

  • Pfurtscheller G, Neuper C, Brunner C, da Silva FL (2005) Beta rebound after different types of motor imagery in man. Neurosci Lett 378:156–159

    Article  CAS  PubMed  Google Scholar 

  • Robinson SD, Vrba J (1999) Functional neuroimaging by synthetic aperture magnetometer (SAM). In: Yoshimoto T, Kotani M, Kuriki S (eds) Recent advances in biomagnetism. Tohoku University Press, Sendai, p 302

    Google Scholar 

  • Ruff RM, Parker SB (1993) Gender- and age-specific changes in motor speed and eye-hand coordination in adults: normative values for the Finger Tapping and Grooved Pegboard Tests. Percept Mot Skills 76:1219–1230

    CAS  PubMed  Google Scholar 

  • Salmelin R, Hamalainen M, Kajola M, Hari R (1995) Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage 2:237–243

    Article  CAS  PubMed  Google Scholar 

  • Steinstraeter O, Teismann IK, Wollbrink A, Suntrup S, Stoeckigt K, Dziewas R, Pantev C (2009) Local sphere-based co-registration for SAM group analysis in subjects without individual MRI. Exp Brain Res 193:387–396

    Article  CAS  PubMed  Google Scholar 

  • Szurhaj W, Bourriez JL, Kahane P, Chauvel P, Mauguiere F, Derambure P (2005) Intracerebral study of gamma rhythm reactivity in the sensorimotor cortex. Eur J Neurosci 21:1223–1235

    Article  PubMed  Google Scholar 

  • Uttner I, Kraft E, Nowak DA, Muller F, Philipp J, Zierdt A, Hermsdorfer J (2007) Mirror movements and the role of handedness: isometric grip forces changes. Mot Control 11:16–28

    Google Scholar 

  • Weeks RA, Honda M, Catalan MJ, Hallett M (2001) Comparison of auditory, somatosensory, and visually instructed and internally generated finger movements: a PET study. Neuroimage 14:219–230

    Article  CAS  PubMed  Google Scholar 

  • Wilke M, Staudt M, Juenger H, Grodd W, Braun C, Krageloh-Mann I (2009) Somatosensory system in two types of motor reorganization in congenital hemiparesis: topography and function. Hum Brain Mapp 30:776–788

    Article  PubMed  Google Scholar 

  • Xiang J, Wilson D, Otsubo H, Ishii R, Chuang S (2001) Neuromagnetic spectral distribution of implicit processing of words. Neuroreport 12:3923–3927

    Article  CAS  PubMed  Google Scholar 

  • Xiang J, Holowka S, Sharma R, Hunjan A, Otsubo H, Chuang S (2003) Volumetric localization of somatosensory cortex in children using synthetic aperture magnetometry. Pediatr Radiol 33:321–327

    PubMed  Google Scholar 

  • Xiang J, Liu Y, Wang Y, Kotecha R, Kirtman EG, Chen Y, Huo X, Fujiwara H, Hemasilpin N, DeGrauw T, Rose D (2009) Neuromagnetic correlates of developmental changes in endogenous high-frequency brain oscillations in children: a wavelet-based beamformer study. Brain Res 1274:28–39

    Article  CAS  PubMed  Google Scholar 

  • Ziemann U, Hallett M (2001) Hemispheric asymmetry of ipsilateral motor cortex activation during unimanual motor tasks: further evidence for motor dominance. Clin Neurophysiol 112:107–113

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by a Trustee Grant to Dr. Jing Xiang from Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaolin Huo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huo, X., Wang, Y., Kotecha, R. et al. High Gamma Oscillations of Sensorimotor Cortex During Unilateral Movement in the Developing Brain: a MEG Study. Brain Topogr 23, 375–384 (2011). https://doi.org/10.1007/s10548-010-0151-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-010-0151-0

Keywords

Navigation