Combined and Singular Effects of Action Observation and Motor Imagery Paradigms on Resting-State Sensorimotor Rhythms

In the present study, 30 right-handed participants randomly performed one of three motor neurorehabilitation paradigms: action observation (AO), motor imagery (MI) and combined action observation and motor imagery (AO+MI) of the right arm and hand movement. Resting state electroencephalography (EEG) was acquired for 5 min before and immediately after the motor paradigms session. EEG was recorded from 10 sites over sensorimotor areas, and the average power was calculated for left (FC3, C3, C1, C5, CP3) and right (FC4, C4, C2, C6, CP4) regions in the spectral bands: delta, theta, alpha, mu, low and high beta. Our main finding demonstrates that delta, theta and mu activity decreased significantly on the contralateral regions during MI, while low beta increased significantly. Except for the mu band, the same changes were observed on the ipsilateral side, where delta and theta decreased significantly, while low beta became significantly higher. No relevant effects were observed for AO or combined AO and MI. These findings demonstrate a rapid effect of MI on cortical modulation in sensorimotor areas which is revealed by changes in resting state oscillatory activity and suggest an interesting interplay between MI and AO. The presented findings may be relevant for choosing a proper protocol for clinical motor neurorehabilitation approaches.

[1]  S. Small,et al.  Action observation has a positive impact on rehabilitation of motor deficits after stroke , 2007, NeuroImage.

[2]  M. Jeannerod Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[3]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[4]  G. Pfurtscheller,et al.  Event-related cortical desynchronization detected by power measurements of scalp EEG. , 1977, Electroencephalography and clinical neurophysiology.

[5]  J. Baron,et al.  Motor Imagery: A Backdoor to the Motor System After Stroke? , 2006, Stroke.

[6]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[7]  M. Jeannerod TO ACT OR NOT TO ACT : PERSPECTIVES ON THE REPRESENTATION OF ACTIONS , 1999 .

[8]  Marco Schieppati,et al.  Imagined and actual arm movements have similar durations when performed under different conditions of direction and mass , 2002, Experimental Brain Research.

[9]  C. Hall,et al.  Further validation and development of the movement imagery questionnaire. , 2012, Journal of sport & exercise psychology.

[10]  Maurizio Corbetta,et al.  Neurological Principles and Rehabilitation of Action Disorders , 2011, Neurorehabilitation and neural repair.

[11]  Karl J. Friston,et al.  Hemodynamic correlates of EEG: A heuristic , 2005, NeuroImage.

[12]  Paul S. Holmes,et al.  Motor Imagery during Action Observation: A Brief Review of Evidence, Theory and Future Research Opportunities , 2016, Front. Neurosci..

[13]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

[14]  S. Swinnen,et al.  Neural correlates of action: Comparing meta-analyses of imagery, observation, and execution , 2018, Neuroscience & Biobehavioral Reviews.

[15]  C. Richards,et al.  Potential role of mental practice using motor imagery in neurologic rehabilitation. , 2001, Archives of physical medicine and rehabilitation.

[16]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[17]  Anthony Singhal,et al.  Theta oscillations reflect a putative neural mechanism for human sensorimotor integration. , 2012, Journal of neurophysiology.

[18]  Sebastiaan Overeem,et al.  Corticospinal Beta-Band Synchronization Entails Rhythmic Gain Modulation , 2010, The Journal of Neuroscience.

[19]  P Baraldi,et al.  Ipsilateral involvement of primary motor cortex during motor imagery , 2000, The European journal of neuroscience.

[20]  Kristen L. Macuga,et al.  Neural representations involved in observed, imagined, and imitated actions are dissociable and hierarchically organized , 2012, NeuroImage.

[21]  D. Poeppel,et al.  Health, USA Reviewed by: , 2010 .

[22]  P. Welch The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[23]  R. Oostenveld,et al.  Frontal theta EEG activity correlates negatively with the default mode network in resting state. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[24]  A. Sirigu,et al.  The Mental Representation of Hand Movements After Parietal Cortex Damage , 1996, Science.

[25]  Diane M. Ste-Marie,et al.  Observation interventions for motor skill learning and performance: an applied model for the use of observation , 2012 .

[26]  C. Schuster,et al.  Best practice for motor imagery: a systematic literature review on motor imagery training elements in five different disciplines , 2011, BMC medicine.

[27]  C. Hall,et al.  Measuring movement imagery abilities: A revision of the Movement Imagery Questionnaire. , 1997 .

[28]  Claire Calmels,et al.  A Neuroscientific Review of Imagery and Observation Use in Sport , 2008, Journal of motor behavior.

[29]  J. Decety,et al.  Neural mechanisms subserving the perception of human actions , 1999, Trends in Cognitive Sciences.

[30]  M. Erb,et al.  Activation of Cortical and Cerebellar Motor Areas during Executed and Imagined Hand Movements: An fMRI Study , 1999, Journal of Cognitive Neuroscience.

[31]  Maurizio Corbetta,et al.  Neurological Principles and Rehabilitation of Action Disorders , 2011, Neurorehabilitation and neural repair.

[32]  Aymeric Guillot,et al.  Multiple roles of motor imagery during action observation , 2013, Front. Hum. Neurosci..

[33]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[34]  B. Givens,et al.  Theta reset produces optimal conditions for long‐term potentiation , 2004, Hippocampus.

[35]  J. Baron,et al.  Does motor imagery share neural networks with executed movement: a multivariate fMRI analysis , 2013, Front. Hum. Neurosci..

[36]  G. Buccino Action observation treatment: a novel tool in neurorehabilitation , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  R. Enoka Neuromechanical Basis of Kinesiology, 2nd Edition , 1995 .

[38]  M. Kahana,et al.  Theta returns , 2001, Current Opinion in Neurobiology.

[39]  Clemens Brunner,et al.  Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks , 2006, NeuroImage.