Movement Kinematics Dynamically Modulates the Rolandic ~ 20-Hz Rhythm During Goal-Directed Executed and Observed Hand Actions

  • B. Marty
  • M. Bourguignon
  • V. Jousmäki
  • V. Wens
  • S. Goldman
  • X. De Tiège
Original Paper

Abstract

This study investigates whether movement kinematics modulates similarly the rolandic α and β rhythm amplitude during executed and observed goal-directed hand movements. It also assesses if this modulation relates to the corticokinematic coherence (CKC), which is the coupling observed between cortical activity and movement kinematics during such motor actions. Magnetoencephalography (MEG) signals were recorded from 11 right-handed healthy subjects while they performed or observed an actor performing the same repetitive hand pinching action. Subjects’ and actor’s forefinger movements were monitored with an accelerometer. Coherence was computed between acceleration signals and the amplitude of α (8–12 Hz) or β (15–25 Hz) oscillations. The coherence was also evaluated between source-projected MEG signals and their β amplitude. Coherence was mainly observed between acceleration and the amplitude of β oscillations at movement frequency within bilateral primary sensorimotor (SM1) cortex with no difference between executed and observed movements. Cross-correlation between the amplitude of β oscillations at the SM1 cortex and movement acceleration was maximal when acceleration was delayed by ~ 100 ms, both during movement execution and observation. Coherence between source-projected MEG signals and their β amplitude during movement observation and execution was not significantly different from that during rest. This study shows that observing others’ actions engages in the viewer’s brain similar dynamic modulations of SM1 cortex β rhythm as during action execution. Results support the view that different neural mechanisms might account for this modulation and CKC. These two kinematic-related phenomena might help humans to understand how observed motor actions are actually performed.

Keywords

Magnetoencephalography MEG Coherence mu rhythm Primary sensory motor cortex Mirror neurons system Corticokinematic coherence CKC 

Notes

Acknowledgements

Xavier De Tiège is Postdoctorate Clinical Master Specialist at the Fonds de la Recherche Scientifique (FRS-FNRS, Brussels, Belgium). This work was supported by the program Attract of Innoviris (Grant 2015-BB2B-10 to Mathieu Bourguignon), the Spanish Ministry of Economy and Competitiveness (Grant PSI2016-77175-P to Mathieu Bourguignon), the Marie Skłodowska-Curie Action of the European Commission (grant #743562 to Mathieu Bourguignon), a Brains Back to Brussels grant to Veikko Jousmäki from the Institut d’Encouragement de la Recherche Scientifique et de l’Innovation de Bruxelles (Brussels, Belgium), European Research Council (Advanced Grant #232946 to Riitta Hari), the Fonds de la Recherche Scientifique (FRS-FNRS, Belgium, Research Credits: J009713), and the Academy of Finland (grants #131483 and #263800). The MEG project at the ULB-Hôpital Erasme (Brussels, Belgium) is financially supported by the Fonds Erasme. We thank Helge Kainulainen and Ronny Schreiber at the Brain Research Unit (Aalto University, Finland) for technical support. We also thank Professor Stéphane Swillens at the Université libre de Bruxelles (ULB) and Professor Riitta Hari (Aalto University) for their support and advices. Finally Brice Marty specially thanks Doctor Stéphanie Grégoire (Mc Gill University) for their support.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Avanzini P, Fabbri-Destro M, Dalla Volta R, Daprati E, Rizzolatti G, Cantalupo G (2012) The dynamics of sensorimotor cortical oscillations during the observation of hand movements: an EEG study. PLoS ONE 7:e37534CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bauer M, Oostenveld R, Peeters M, Fries P (2006) Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26:490–501CrossRefPubMedGoogle Scholar
  3. Bortel R, Sovka P (2007) Approximation of statistical distribution of magnitude squared coherence estimated with segment overlapping. Signal Process 87:1100–1117CrossRefGoogle Scholar
  4. Bourguignon M, De Tiège X, de Beeck MO, Pirotte B, Van Bogaert P, Goldman S, Hari R, Jousmäki V (2011) Functional motor-cortex mapping using corticokinematic coherence. Neuroimage 55:1475–1479CrossRefPubMedGoogle Scholar
  5. Bourguignon M, De Tiège X, de Beeck MO, Van Bogaert P, Goldman S, Jousmaki V, Hari R (2013) Primary motor cortex and cerebellum are coupled with the kinematics of observed hand movements. Neuroimage 66:500–507CrossRefPubMedGoogle Scholar
  6. Bourguignon M, Jousmäki V, Op de Beeck M, Van Bogaert P, Goldman S, De Tiège X (2012) Neuronal network coherent with hand kinematics during fast repetitive hand movements. Neuroimage 59(2):1684–1691CrossRefPubMedGoogle Scholar
  7. Bourguignon M, Piitulainen H, De Tiege X, Jousmaki V, Hari R (2015) Corticokinematic coherence mainly reflects movement-induced proprioceptive feedback. Neuroimage 106:382–390CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brinkman L, Stolk A, Dijkerman HC, de Lange FP, Toni I (2014) Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions. J Neurosci 34:14783–14792CrossRefPubMedPubMedCentralGoogle Scholar
  9. Caetano G, Jousmaki V, Hari R (2007) Actor’s and observer’s primary motor cortices stabilize similarly after seen or heard motor actions. Proc Natl Acad Sci USA 104:9058–9062CrossRefPubMedPubMedCentralGoogle Scholar
  10. Carrette E, De Tiege X, Op De Beeck M, De Herdt V, Meurs A, Legros B, Raedt R, Deblaere K, Van Roost D, Bourguignon M, Goldman S, Boon P, Van Bogaert P, Vonck K (2011) Magnetoencephalography in epilepsy patients carrying a vagus nerve stimulator. Epilepsy Res 93:44–52CrossRefPubMedGoogle Scholar
  11. Cassim F, Monaca C, Szurhaj W, Bourriez JL, Defebvre L, Derambure P, Guieu JD (2001) Does post-movement beta synchronization reflect an idling motor cortex? Neuroreport 12:3859–3863CrossRefPubMedGoogle Scholar
  12. Cheyne D, Gaetz W, Garnero L, Lachaux JP, Ducorps A, Schwartz D, Varela FJ (2003) Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. Brain Res Cogn Brain Res 17:599–611CrossRefPubMedGoogle Scholar
  13. De Tiege X, de Beeck MO, Funke M, Legros B, Parkkonen L, Goldman S, Van Bogaert P (2008) Recording epileptic activity with MEG in a light-weight magnetic shieldGoogle Scholar
  14. Faes L, Pinna GD, Porta A, Maestri R, Nollo G (2004) Surrogate data analysis for assessing the significance of the coherence function. IEEE Trans Biomed Eng 51:1156–1166CrossRefPubMedGoogle Scholar
  15. Gastaut H (1952) Electrocorticographic study of the reactivity of rolandic rhythm. Rev Neurol (Paris) 87:176–182Google Scholar
  16. Halliday DM, Rosenberg JR, Amjad AM, Breeze P, Conway BA, Farmer SF (1995) A framework for the analysis of mixed time series/point process data—theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. Prog Biophys Mol Biol 64:237–278CrossRefPubMedGoogle Scholar
  17. Hari R, Forss N, Avikainen S, Kirveskari E, Salenius S, Rizzolatti G (1998) Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc Natl Acad Sci USA 95:15061–15065CrossRefPubMedPubMedCentralGoogle Scholar
  18. Houweling S, Beek PJ, Daffertshofer A (2010) Spectral changes of interhemispheric crosstalk during movement instabilities. Cereb Cortex 20:2605–2613CrossRefPubMedGoogle Scholar
  19. Jarvelainen J, Schurmann M, Hari R (2004) Activation of the human primary motor cortex during observation of tool use. Neuroimage 23:187–192CrossRefPubMedGoogle Scholar
  20. Jerbi K, Lachaux JP, N’Diaye K, Pantazis D, Leahy RM, Garnero L, Baillet S (2007) Coherent neural representation of hand speed in humans revealed by MEG imaging. Proc Natl Acad Sci USA 104:7676–7681CrossRefPubMedPubMedCentralGoogle Scholar
  21. Keysers C, Kaas JH, Gazzola V (2010) Somatosensation in social perception. Nat Rev Neurosci 11(6):417–428CrossRefPubMedGoogle Scholar
  22. Kilner JM, Frith CD (2007) A possible role for primary motor cortex during action observation. Proc Natl Acad Sci USA 104:8683–8684CrossRefPubMedPubMedCentralGoogle Scholar
  23. Kilner JM, Marchant JL, Frith CD (2009) Relationship between activity in human primary motor cortex during action observation and the mirror neuron system. PLoS ONE 4:e4925CrossRefPubMedPubMedCentralGoogle Scholar
  24. Lippi G, Fontana R, Avanzini P, Aloe R, Ippolito L, Sandei F, Favaloro EJ (2012) Influence of mechanical trauma of blood and hemolysis on PFA-100 testing. Blood Coagul Fibrinolysis 23:82–86CrossRefPubMedGoogle Scholar
  25. Marty B, Bourguignon M, Jousmaki V, Wens V, Op de Beeck M, Van Bogaert P, Goldman S, Hari R, De Tiege X (2015a) Cortical kinematic processing of executed and observed goal-directed hand actions. Neuroimage 119:221–228CrossRefPubMedGoogle Scholar
  26. Marty B, Bourguignon M, Op de Beeck M, Wens V, Goldman S, Van Bogaert P, Jousmaki V, De Tiege X (2015b) Effect of movement rate on corticokinematic coherence. Neurophysiol Clin 45:469–474CrossRefGoogle Scholar
  27. Nagamine T, Kajola M, Salmelin R, Shibasaki H, Hari R (1996) Movement-related slow cortical magnetic fields and changes of spontaneous MEG- and EEG-brain rhythms. Electroencephalogr Clin Neurophysiol 99:274–286CrossRefPubMedGoogle Scholar
  28. Neuper C, Wortz M, Pfurtscheller G (2006) ERD/ERS patterns reflecting sensorimotor activation and deactivation. Prog Brain Res 159:211–222CrossRefPubMedGoogle Scholar
  29. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25CrossRefPubMedGoogle Scholar
  30. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  31. Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110:1842–1857CrossRefPubMedGoogle Scholar
  32. Pfurtscheller G, Stancak A Jr, Neuper C (1996) Post-movement beta synchronization. A correlate of an idling motor area? Electroencephalogr Clin Neurophysiol 98:281–293CrossRefPubMedGoogle Scholar
  33. Piitulainen H, Bourguignon M, De Tiege X, Hari R, Jousmaki V (2013a) Coherence between magnetoencephalography and hand-action-related acceleration, force, pressure, and electromyogram. Neuroimage 72:83–90CrossRefPubMedGoogle Scholar
  34. Piitulainen H, Bourguignon M, De Tiège X, Hari R, Jousmäki V (2013b) Corticokinematic coherence during active and passive finger movements. Neuroscience 238:361–370CrossRefGoogle Scholar
  35. Press C, Cook J, Blakemore SJ, Kilner J (2011) Dynamic modulation of human motor activity when observing actions. J Neurosci 31:2792–2800CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192CrossRefPubMedGoogle Scholar
  37. Rizzolatti G, Sinigaglia C (2010) The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 11:264–274CrossRefPubMedGoogle Scholar
  38. Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53:1–31CrossRefPubMedGoogle Scholar
  39. Salenius S, Schnitzler A, Salmelin R, Jousmaki V, Hari R (1997) Modulation of human cortical rolandic rhythms during natural sensorimotor tasks. Neuroimage 5:221–228CrossRefPubMedGoogle Scholar
  40. Salmelin R, Hari R (1994a) Characterization of spontaneous MEG rhythms in healthy adults. Electroencephalogr Clin Neurophysiol 91:237–248CrossRefPubMedGoogle Scholar
  41. Salmelin R, Hari R (1994b) Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement. Neuroscience 60:537–550CrossRefPubMedGoogle Scholar
  42. Schalk G, Kubanek J, Miller KJ, Anderson NR, Leuthardt EC, Ojemann JG, Limbrick D, Moran D, Gerhardt LA, Wolpaw JR (2007) Decoding two-dimensional movement trajectories using electrocorticographic signals in humans. J Neural Eng 4:264–275CrossRefPubMedGoogle Scholar
  43. Schnitzler A, Salenius S, Salmelin R, Jousmaki V, Hari R (1997) Involvement of primary motor cortex in motor imagery: a neuromagnetic study. Neuroimage 6:201–208CrossRefPubMedGoogle Scholar
  44. Seeber M, Scherer R, Muller-Putz GR (2016) EEG oscillations are modulated in different behavior-related networks during rhythmic finger movements. J Neurosci 36:11671–11681CrossRefPubMedGoogle Scholar
  45. Taulu S, Simola J, Kajola M (2005) Applications of the signal space separation method. IEEE Trans Signal Process 53:3359–3372CrossRefGoogle Scholar
  46. 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 44:867–880CrossRefPubMedGoogle Scholar
  47. Vigneswaran G, Philipp R, Lemon RN, Kraskov A (2013) M1 corticospinal mirror neurons and their role in movement suppression during action observation. Curr Biol 23:236–243CrossRefPubMedPubMedCentralGoogle Scholar
  48. Yuan H, Perdoni C, He B (2010) Relationship between speed and EEG activity during imagined and executed hand movements. J Neural Eng 7:26001CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zhou G, Bourguignon M, Parkkonen L, Hari R (2016) Neural signatures of hand kinematics in leaders vs. followers: A dual-MEG study. Neuroimage 125:731–738CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • B. Marty
    • 1
  • M. Bourguignon
    • 1
    • 2
    • 3
    • 4
  • V. Jousmäki
    • 1
    • 3
  • V. Wens
    • 1
    • 5
  • S. Goldman
    • 1
    • 5
  • X. De Tiège
    • 1
    • 5
  1. 1.Laboratoire de Cartographie fonctionnelle du Cerveau, UNI – ULB Neuroscience InstituteUniversité libre de Bruxelles (ULB)BrusselsBelgium
  2. 2.Laboratoire Cognition Langage et Développement, UNI – ULB Neuroscience InstituteUniversité libre de Bruxelles (ULB)BrusselsBelgium
  3. 3.Department of Neuroscience and Biomedical Engineering and Aalto NeuroImagingAalto University School of ScienceEspooFinland
  4. 4.BCBL, Basque Center on Cognition, Brain and LanguageSan SebastianSpain
  5. 5.Department of Functional Neuroimaging, Service of Nuclear Medicine, CUB Hôpital ErasmeUniversité libre de Bruxelles (ULB)BrusselsBelgium

Personalised recommendations