Action observation facilitates motor cortical activity in patients with stroke and hemiplegia

Motor imagery (MI) is a mental practice that reproduces the visual- and/or kinesthetic-modality brain activations accompanying movement. It is a useful rehabilitation technique as the affected motor cortex can be stimulated in patients with stroke and hemiplegia. However, most patients with stroke have difficulty with MI owing to advanced age and/or higher-cognitive dysfunction, thus impairing their ability to internally simulate the action. We therefore investigated whether action observation (AO), an alternative form of motor stimulation that works via the mirror-neuron system, could facilitate motor cortical activity in such patients. Combined AO and physical training of the observed actions has been reported to have a positive impact on motor deficits after stroke. Eleven patients with stroke and hemiplegia affecting the hand performed MI and AO with verbal and video instructions under 19 channels of electroencephalogram (EEG) recording. The event-related desynchronization (ERD) was measured as an electroencephalographic marker of motor cortical activity. The ERD power in the AO condition (30.0±5.0%) was significantly higher than that in the MI condition (12.2±3.9%). These results suggest that AO could be a good option for patients with stroke who have difficulty using MI to effectively stimulate and reestablish cortical-peripheral motor pathways.

[1]  Luigi Cattaneo,et al.  Representation of Goal and Movements without Overt Motor Behavior in the Human Motor Cortex: A Transcranial Magnetic Stimulation Study , 2009, The Journal of Neuroscience.

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

[3]  S. Small,et al.  Functions of the Mirror Neuron System: Implications for Neurorehabilitation , 2006, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[4]  W. Zijlstra,et al.  The role of motor imagery in learning a totally novel movement , 2003, Experimental Brain Research.

[5]  Hidenao Fukuyama,et al.  Action observation with kinesthetic illusion can produce human motor plasticity , 2015, The European journal of neuroscience.

[6]  P. Duncan,et al.  Measurement of Motor Recovery After Stroke: Outcome Assessment and Sample Size Requirements , 1992, Stroke.

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

[8]  M. Schoenfeld,et al.  Action Imagery Combined With Action Observation Activates More Corticomotor Regions Than Action Observation Alone , 2012, Journal of neurologic physical therapy : JNPT.

[9]  L. Fogassi,et al.  Monkey gaze behaviour during action observation and its relationship to mirror neuron activity , 2013, The European journal of neuroscience.

[10]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[11]  G. Rizzolatti,et al.  Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. , 2014, Physiological reviews.

[12]  Joseph E LeDoux,et al.  Parallels between cerebellum- and amygdala-dependent conditioning , 2002, Nature Reviews Neuroscience.

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

[14]  T. Elbert,et al.  New treatments in neurorehabiliation founded on basic research , 2002, Nature Reviews Neuroscience.

[15]  G. Fink,et al.  Connectivity-based approaches in stroke and recovery of function , 2014, The Lancet Neurology.

[16]  G. Pfurtscheller,et al.  Foot and hand area mu rhythms. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[17]  F. D. Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991 .

[18]  John P. John,et al.  Assessing Neurocognition via Gamified Experimental Logic: A Novel Approach to Simultaneous Acquisition of Multiple ERPs , 2016, Front. Neurosci..

[19]  Arne D. Ekstrom,et al.  Single-Neuron Responses in Humans during Execution and Observation of Actions , 2010, Current Biology.

[20]  T. Itil,et al.  Digital computer analyzed sleep and resting EEG during haloperidol treatment. , 1970, The American journal of psychiatry.

[21]  E. Naito,et al.  Body representations in the human brain revealed by kinesthetic illusions and their essential contributions to motor control and corporeal awareness , 2016, Neuroscience Research.

[22]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[23]  F. Pazzaglia,et al.  The generation and maintenance of visual mental images: Evidence from image type and aging , 2007, Brain and Cognition.

[24]  L. Fournier,et al.  Mirror neuron activation as a function of explicit learning: changes in mu‐event‐related power after learning novel responses to ideomotor compatible, partially compatible, and non‐compatible stimuli , 2016, The European journal of neuroscience.

[25]  Ethan R. Buch,et al.  Think to Move: a Neuromagnetic Brain-Computer Interface (BCI) System for Chronic Stroke , 2008, Stroke.

[26]  Byounghee Lee,et al.  Differences in Brain Waves of Normal Persons and Stroke Patients during Action Observation and Motor Imagery , 2014, Journal of physical therapy science.

[27]  R Langton-Hewer,et al.  The hemiplegic arm after stroke: measurement and recovery. , 1983, Journal of neurology, neurosurgery, and psychiatry.

[28]  J. Steurer,et al.  Journal of Neuroengineering and Rehabilitation Efficacy of Motor Imagery in Post-stroke Rehabilitation: a Systematic Review , 2022 .

[29]  Effie Chew,et al.  Is Motor‐Imagery Brain‐Computer Interface Feasible in Stroke Rehabilitation? , 2014, PM & R : the journal of injury, function, and rehabilitation.

[30]  Shlomo Bentin,et al.  Mirror-neuron system recruitment by action observation: Effects of focal brain damage on mu suppression , 2014, NeuroImage.

[31]  S. Tipper From observation to action simulation: The role of attention, eye-gaze, emotion, and body state , 2010, Quarterly journal of experimental psychology.

[32]  L. Buxbaum,et al.  The Role of the Dynamic Body Schema in Praxis: Evidence from Primary Progressive Apraxia , 2000, Brain and Cognition.

[33]  Differences in Learning Facilitatory Effect of Motor Imagery and Action Observation of Golf Putting , 2009 .

[34]  M. Brass,et al.  Inhibition of imitative behaviour and social cognition , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[35]  J. Ushiba,et al.  Event-related desynchronization reflects downregulation of intracortical inhibition in human primary motor cortex. , 2013, Journal of neurophysiology.

[36]  M. Hommel,et al.  Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. , 2005, Brain : a journal of neurology.

[37]  J. H. van der Lee,et al.  Exercise therapy for arm function in stroke patients: a systematic review of randomized controlled trials , 2001, Clinical rehabilitation.

[38]  Shlomo Bentin,et al.  Dysfunction of the Human Mirror Neuron System in Ideomotor Apraxia: Evidence from Mu Suppression , 2016, Journal of Cognitive Neuroscience.

[39]  KyeongMi Kim,et al.  Action observation for upper limb function after stroke: evidence-based review of randomized controlled trials , 2015, Journal of physical therapy science.

[40]  P M Rossini,et al.  Neuroimaging experimental studies on brain plasticity in recovery from stroke. , 2007, Europa medicophysica.

[41]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[42]  S. Small,et al.  Fine modulation in network activation during motor execution and motor imagery. , 2004, Cerebral cortex.

[43]  Craig Hall,et al.  The MIQ-RS: A Suitable Option for Examining Movement Imagery Ability , 2007, Evidence-based complementary and alternative medicine : eCAM.

[44]  J. Berger AIDS and stroke risk , 2004, The Lancet Neurology.

[45]  C. Neuper,et al.  Relationship Between Electrical Brain Responses to Motor Imagery and Motor Impairment in Stroke , 2012, Stroke.