Experimental Brain Research

, Volume 236, Issue 4, pp 1067–1075 | Cite as

Corticospinal excitability is modulated by distinct movement patterns during action observation

Research Article

Abstract

It is well established that excitability of the primary motor cortex increases during action observation. However, the modulation of motor cortex excitability during observation of different actions, with distinct movement patterns, is not fully understood. The aim of the current study was to examine time-dependent changes in corticospinal excitability during observation of two actions with different levels of complexity. We developed videos of two distinct actions (a point and a reach-and-grasp), that were matched in video length, action onset, and onset of kinematics. Single-pulse transcranial magnetic stimulation was used to investigate time-dependent changes in primary motor cortex excitability during observation of the two actions. Motor evoked potentials (MEP) were recorded from two intrinsic hand muscles, namely first dorsal interosseous (FDI) and abductor digiti minimi. Results showed no difference in MEP amplitude during observation of a static hand compared to observation of the actions. When comparing the point to the grasp action, there were two key findings showing time-dependent changes in motor cortex excitability: first, greater MEP amplitude in FDI during observation of the point than the grasp action at an early time-point (index finger extension) and second, greater MEP amplitude in FDI during observation of the grasp than the point action at a later time-point (hand opening to form a grasp). These results show that excitability of the primary motor cortex is differentially modulated during observation of a point and grasp action, suggesting that the action observation network is engaged in a time-dependent manner during action observation.

Keywords

Action observation Transcranial magnetic stimulation Motor evoked potential Action complexity Primary motor cortex Kinematics 

Notes

Acknowledgements

AMV is supported by a National Health and Medical Research Council Early Career Fellowship (GNT1088295).

References

  1. Alaerts K, Heremans E, Swinnen SP, Wenderoth N (2009) How are observed actions mapped to the observer’s motor system? Influ Posture Perspect Neuropsychol 47:415–422.  https://doi.org/10.1016/j.neuropsychologia.2008.09.012 Google Scholar
  2. Borroni P, Baldissera F (2008) Activation of motor pathways during observation and execution of hand movements. Soc Neurosci 3:276–288.  https://doi.org/10.1080/17470910701515269 CrossRefPubMedGoogle Scholar
  3. Brasil-Neto JP, Cohen LG, Panizza M, Nilsson J, Roth BJ (1992) Optimal focal transcranial magnetic activation of the human motor cortex: effects of coil orientation, shape of the induced current pulse, and stimulus intensity. J Clin Neurophysiol 9:132–136.  https://doi.org/10.1097/00004691-199201000-00014 CrossRefPubMedGoogle Scholar
  4. Burgess J, Arnold S, Fitzgibbon B, Fitzgerald P, Enticott P (2013) A transcranial magnetic stimulation study of the effect of visual orientation on the putative human mirror neuron system. Front Hum Neurosci.  https://doi.org/10.3389/fnhum.2013.00679 Google Scholar
  5. Cavallo A, Heyes C, Becchio C, Bird G, Catmur C (2014) Timecourse of mirror and counter-mirror effects measured with transcranial magnetic stimulation. Soc Cogn Affect Neurosci 9:1082–1088.  https://doi.org/10.1093/scan/nst085 CrossRefPubMedGoogle Scholar
  6. Chong TTJ, Cunnington R, Williams MA, Kanwisher N, Mattingley JB (2008) fMRI adaptation reveals mirror neurons in human inferior parietal cortex. Curr Biol 18:1576–1580.  https://doi.org/10.1016/j.cub.2008.08.068 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cuypers K, Thijs H, Meesen RLJ (2014) Optimization of the transcranial magnetic stimulation protocol by defining a reliable estimate for corticospinal excitability. PLoS One 9:7.  https://doi.org/10.1371/journal.pone.0086380 CrossRefGoogle Scholar
  8. Dancause N et al (2006) Topographically divergent and convergent connectivity between premotor and primary motor cortex. Cereb Cortex 16:1057–1068.  https://doi.org/10.1093/cercor/bhj049 CrossRefPubMedGoogle Scholar
  9. di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G (1992) Understanding motor events: a neurophysiological study. Exp Brain Res 91:176–180.  https://doi.org/10.1007/BF00230027 CrossRefPubMedGoogle Scholar
  10. Dum RP, Strick PL (2002) Motor areas in the frontal lobe of the primate. Physiol Behav 77:677–682Google Scholar
  11. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73:2608–2611CrossRefPubMedGoogle Scholar
  12. Filimon F, Nelson JD, Hagler DJ, Sereno MI (2007) Human cortical representations for reaching: mirror neurons for execution, observation, and imagery. NeuroImage 37:1315–1328.  https://doi.org/10.1016/j.neuroimage.2007.06.008 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G (2005) Parietal lobe: from action organization to intention understanding. Science 308:662–667.  https://doi.org/10.1126/science.1106138 CrossRefPubMedGoogle Scholar
  14. Gangitano M, Mottaghy FM, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. NeuroReport 12:1489–1492CrossRefPubMedGoogle Scholar
  15. Gangitano M, Mottaghy FM, Pascual-Leone A (2004) Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur J Neurosci 20:2193–2202.  https://doi.org/10.1111/j.1460-9568.2004.03655.x CrossRefPubMedGoogle Scholar
  16. Gatti R, Rocca MA, Fumagalli S, Cattrysse E, Kerckhofs E, Falini A, Filippi M (2016) The effect of action observation/execution on mirror neuron system recruitment: an fMRI study in healthy individuals. Brain Imaging Behav.  https://doi.org/10.1007/s11682-016-9536-3 Google Scholar
  17. Goldsworthy MR, Hordacre B, Ridding MC (2016) Minimum number of trials required for within- and between-session reliability of TMS measures of corticospinal excitability. Neuroscience 320:205–209.  https://doi.org/10.1016/j.neuroscience.2016.02.012 CrossRefPubMedGoogle Scholar
  18. Hardwick RM, McAllister CJ, Holmes PS, Edwards MG (2012) Transcranial magnetic stimulation reveals modulation of corticospinal excitability when observing actions with the intention to imitate. Eur J Neurosci 35:1475–1480.  https://doi.org/10.1111/j.1460-9568.2012.08046.x CrossRefPubMedGoogle Scholar
  19. Hetu S, Taschereau-Dumouchel V, Meziane HB, Jackson PL, Mercier C (2016) Behavioral and TMS markers of action observation might reflect distinct neuronal processes. Front Hum Neurosci 10:458CrossRefPubMedPubMedCentralGoogle Scholar
  20. Krings T, Naujokat C, Graf V. Keyserlingk D (1998) Representation of cortical motor function as revealed by stereotactic transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol Electromyogr Mot Control 109:85–93.  https://doi.org/10.1016/S0924-980X(97)00078-7 CrossRefGoogle Scholar
  21. Lago A et al (2010) Ventral premotor to primary motor cortical interactions during noxious and naturalistic action observation. Neuropsychologia 48:1802–1806.  https://doi.org/10.1016/j.neuropsychologia.2010.02.030 CrossRefPubMedGoogle Scholar
  22. Lepage J-F, Tremblay S, Theoret H (2010) Early non-specific modulation of corticospinal excitability during action observation. Eur J Neurosci 31:931–937.  https://doi.org/10.1111/j.1460-9568.2010.07121.x CrossRefPubMedGoogle Scholar
  23. Loporto M, McAllister CJ, Edwards MG, Wright DJ, Holmes PS (2012) Prior action execution has no effect on corticospinal facilitation during action observation. Behav Brain Res 231:124–129.  https://doi.org/10.1016/j.bbr.2012.03.009 CrossRefPubMedGoogle Scholar
  24. Maeda F, Kleiner-Fisman G, Pascual-Leone A (2002) Motor facilitation while observing hand actions: specificity of the effect and role of observer’s orientation. J Neurophysiol 87:1329–1335.  https://doi.org/10.1152/jn.00773.2000 CrossRefPubMedGoogle Scholar
  25. Magill RA, Anderson D (2011) Motor learning and control: concepts and applications, 11th edn. McGraw Hill, New YorkGoogle Scholar
  26. Melgari JM, Pasqualetti P, Pauri F, Rossini PM (2008) Muscles in “Concert”: Study of primary motor cortex upper limb functional topography. PLoS One.  https://doi.org/10.1371/journal.pone.0003069 PubMedPubMedCentralGoogle Scholar
  27. Muakkassa KF, Strick PL (1979) Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’areas. Brain Res 177:176–182CrossRefPubMedGoogle Scholar
  28. Naish KR, Obhi SS (2015) Timing and specificity of early changes in motor excitability during movement observation. Exp Brain Res 233:1867–1874.  https://doi.org/10.1007/s00221-015-4258-0 CrossRefPubMedGoogle Scholar
  29. Naish KR, Houston-Price C, Bremner AJ, Holmes NP (2014) Effects of action observation on corticospinal excitability: Muscle specificity, direction, and timing of the mirror response. Neuropsychologia 64:331–348.  https://doi.org/10.1016/j.neuropsychologia.2014.09.034 CrossRefPubMedGoogle Scholar
  30. Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192.  https://doi.org/10.1146/annurev.neuro.27.070203.144230 CrossRefPubMedGoogle Scholar
  31. Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nat Rev Neurosci 2:661–670.  https://doi.org/10.1038/35090060 CrossRefPubMedGoogle Scholar
  32. Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice research. Clin Neurophysiol 120:2008–2039.  https://doi.org/10.1016/j.clinph.2009.08.016 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Rossini PM et al (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Rep IFCN Comm Electroencephalogr Clin Neurophysiol 91:79–92.  https://doi.org/10.1016/0013-4694(94)90029-9 CrossRefGoogle Scholar
  34. Rossini PM et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126:1071–1107.  https://doi.org/10.1016/j.clinph.2015.02.001 CrossRefPubMedGoogle Scholar
  35. Tabachnick BG, Fidell LS (2007) Experimental designs using ANOVA. Thomson/Brooks/Cole, GroveGoogle Scholar
  36. Taschereau-Dumouchel V et al (2016) BDNF Val(66)Met polymorphism influences visuomotor associative learning and the sensitivity to action observation. Sci Rep 6:10.  https://doi.org/10.1038/srep34907 CrossRefGoogle Scholar
  37. Turella L, Wurm M, Tucciarelli R, Lingnau A (2013) Expertise in action observation: recent neuroimaging findings and future perspectives. Front Hum Neurosci.  https://doi.org/10.3389/fnhum.2013.00637 PubMedPubMedCentralGoogle Scholar
  38. Wassermann EM, McShane LM, Hallett M, Cohen LG (1992) Noninvasive mapping of muscle representations in human motor cortex. Electroencephalogr Clin Neurophysiol Evoked Potentials Sect 85:1–8CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Psychology and Exercise ScienceMurdoch UniversityMurdochAustralia

Personalised recommendations