Enhanced Activation of Motor Execution Networks Using Action Observation Combined with Imagination of Lower Limb Movements

The combination of first-person observation and motor imagery, i.e. first-person observation of limbs with online motor imagination, is commonly used in interactive 3D computer gaming and in some movie scenes. These scenarios are designed to induce a cognitive process in which a subject imagines himself/herself acting as the agent in the displayed movement situation. Despite the ubiquity of this type of interaction and its therapeutic potential, its relationship to passive observation and imitation during observation has not been directly studied using an interactive paradigm. In the present study we show activation resulting from observation, coupled with online imagination and with online imitation of a goal-directed lower limb movement using functional MRI (fMRI) in a mixed block/event-related design. Healthy volunteers viewed a video (first-person perspective) of a foot kicking a ball. They were instructed to observe-only the action (O), observe and simultaneously imagine performing the action (O-MI), or imitate the action (O-IMIT). We found that when O-MI was compared to O, activation was enhanced in the ventralpremotor cortex bilaterally, left inferior parietal lobule and left insula. The O-MI and O-IMIT conditions shared many activation foci in motor relevant areas as confirmed by conjunction analysis. These results show that (i) combining observation with motor imagery (O-MI) enhances activation compared to observation-only (O) in the relevant foot motor network and in regions responsible for attention, for control of goal-directed movements and for the awareness of causing an action, and (ii) it is possible to extensively activate the motor execution network using O-MI, even in the absence of overt movement. Our results may have implications for the development of novel virtual reality interactions for neurorehabilitation interventions and other applications involving training of motor tasks.

[1]  D. Kiper,et al.  Virtual Reality–Augmented Neurorehabilitation Improves Motor Function and Reduces Neuropathic Pain in Patients With Incomplete Spinal Cord Injury , 2013, Neurorehabilitation and neural repair.

[2]  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.

[3]  Martin Bilodeau,et al.  Attentional Demands Associated With Postural Control Depend on Task Difficulty and Visual Condition , 2012, Journal of motor behavior.

[4]  André J. Szameitat,et al.  Cortical activation during executed, imagined, observed, and passive wrist movements in healthy volunteers and stroke patients , 2012, NeuroImage.

[5]  R. Hardwick,et al.  Transcranial magnetic stimulation reveals modulation of corticospinal excitability when observing actions with the intention to imitate , 2012, The European journal of neuroscience.

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

[7]  Guy A Orban,et al.  Acting alters visual processing: flexible recruitment of visual areas by one's own actions. , 2012, Cerebral cortex.

[8]  Corey J. Bohil,et al.  Virtual reality in neuroscience research and therapy , 2011, Nature Reviews Neuroscience.

[9]  Sergei V. Adamovich,et al.  Mechanisms of neural reorganization in chronic stroke subjects after virtual reality training , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[10]  Kynan Eng,et al.  Virtual reality rehabilitation system for neuropathic pain and motor dysfunction in spinal cord injury patients , 2011, 2011 International Conference on Virtual Rehabilitation.

[11]  Robert Riener,et al.  fMRI assessment of upper extremity related brain activation with an MRI-compatible manipulandum , 2011, International Journal of Computer Assisted Radiology and Surgery.

[12]  O. Blanke,et al.  Multisensory Mechanisms in Temporo-Parietal Cortex Support Self-Location and First-Person Perspective , 2011, Neuron.

[13]  S. Chandrasekharan,et al.  Activity of human motor system during action observation is modulated by object presence , 2011, Experimental Brain Research.

[14]  M. Hepp-Reymond,et al.  Movement Observation Activates Lower Limb Motor Networks in Chronic Complete Paraplegia , 2011, Neurorehabilitation and neural repair.

[15]  G. Rizzolatti,et al.  View-Based Encoding of Actions in Mirror Neurons of Area F5 in Macaque Premotor Cortex , 2011, Current Biology.

[16]  G. Orban,et al.  Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. , 2010, Journal of neurophysiology.

[17]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[18]  P. Siddall,et al.  Brain circuitry underlying pain in response to imagined movement in people with spinal cord injury , 2010, PAIN®.

[19]  Bin He,et al.  Negative covariation between task-related responses in alpha/beta-band activity and BOLD in human sensorimotor cortex: An EEG and fMRI study of motor imagery and movements , 2010, NeuroImage.

[20]  M. Filippi,et al.  FMRI correlates of execution and observation of foot movements in left-handers , 2010, Journal of the Neurological Sciences.

[21]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[22]  F. Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

[23]  J. Baron,et al.  Motor imagery after stroke: Relating outcome to motor network connectivity , 2009, Annals of neurology.

[24]  Marie S. Burrage,et al.  Two Forms of Spatial Imagery , 2009, Psychological science.

[25]  G. Orban,et al.  Human Functional Magnetic Resonance Imaging Reveals Separation and Integration of Shape and Motion Cues in Biological Motion Processing , 2009, The Journal of Neuroscience.

[26]  Jong-Hwan Lee,et al.  Automated classification of fMRI data employing trial-based imagery tasks , 2009, Medical Image Anal..

[27]  K. Zentgraf,et al.  Cognitive motor processes: The role of motor imagery in the study of motor representations , 2009, Brain Research Reviews.

[28]  T. A. Carpenter,et al.  Motor Imagery After Subcortical Stroke: A Functional Magnetic Resonance Imaging Study , 2009, Stroke.

[29]  Jiunjie Wang,et al.  The cortical modulation from the external cues during gait observation and imagination , 2008, Neuroscience Letters.

[30]  Jean-Claude Baron,et al.  Motor Imagery to Enhance Recovery After Subcortical Stroke: Who Might Benefit, Daily Dose, and Potential Effects , 2008, Neurorehabilitation and neural repair.

[31]  Marcel Brass,et al.  Through the looking glass: counter‐mirror activation following incompatible sensorimotor learning , 2008, The European journal of neuroscience.

[32]  G. Pfurtscheller,et al.  Brain motor system function in a patient with complete spinal cord injury following extensive brain–computer interface training , 2008, Experimental Brain Research.

[33]  Kazumi Iseki,et al.  Neural mechanisms involved in mental imagery and observation of gait , 2008, NeuroImage.

[34]  Emily S. Cross,et al.  Sensitivity of the action observation network to physical and observational learning. , 2008, Cerebral cortex.

[35]  P. S. Jones,et al.  Mapping the involvement of BA 4a and 4p during Motor Imagery , 2008, NeuroImage.

[36]  S. Cramer,et al.  Cortical activation during executed, imagined, and observed foot movements , 2008, Neuroreport.

[37]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[38]  Paul E. Summers,et al.  Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements , 2008, NeuroImage.

[39]  Steven C. Cramer,et al.  Effects of motor imagery training after chronic, complete spinal cord injury , 2007, Experimental Brain Research.

[40]  G. Rizzolatti,et al.  Congruent Embodied Representations for Visually Presented Actions and Linguistic Phrases Describing Actions , 2006, Current Biology.

[41]  O. Blanke,et al.  Neural Basis of Embodiment: Distinct Contributions of Temporoparietal Junction and Extrastriate Body Area , 2006, The Journal of Neuroscience.

[42]  Emily S. Cross,et al.  Building a motor simulation de novo: Observation of dance by dancers , 2006, NeuroImage.

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

[44]  T. Kimberley,et al.  Neural Substrates for Motor Imagery in Severe Hemiparesis , 2006, Neurorehabilitation and neural repair.

[45]  JamesW. Lewis Cortical Networks Related to Human Use of Tools , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[46]  Andrew N. Meltzoff,et al.  Neural circuits involved in imitation and perspective-taking , 2006, NeuroImage.

[47]  Georg Northoff,et al.  Self-referential processing in our brain—A meta-analysis of imaging studies on the self , 2006, NeuroImage.

[48]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[49]  A. Meltzoff,et al.  An fMRI study of imitation: action representation and body schema , 2005, Neuropsychologia.

[50]  S. Cramer,et al.  Brain motor system function after chronic, complete spinal cord injury. , 2005, Brain : a journal of neurology.

[51]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[52]  D Yves von Cramon,et al.  Motion Class Dependency in Observers' Motor Areas Revealed by Functional Magnetic Resonance Imaging , 2005, The Journal of Neuroscience.

[53]  P. Brugger,et al.  What disconnection tells about motor imagery: evidence from paraplegic patients. , 2005, Cerebral cortex.

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

[55]  Roger P. Woods,et al.  Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation , 2004, NeuroImage.

[56]  Jean-Baptiste Poline,et al.  Motor execution and imagination networks in post-stroke dystonia , 2004, Neuroreport.

[57]  Jens Frahm,et al.  Erratum to “Is the human primary motor cortex involved in motor imagery?” [Cognitive Brain Research 19 (2004) 138–144] , 2004 .

[58]  Aina Puce,et al.  Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex , 2004, NeuroImage.

[59]  P. Dechent,et al.  Is the human primary motor cortex involved in motor imagery? , 2004, Brain research. Cognitive brain research.

[60]  H Johansen-Berg,et al.  Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements , 2004, NeuroImage.

[61]  O. Blanke,et al.  Out-of-body experience and autoscopy of neurological origin. , 2004, Brain : a journal of neurology.

[62]  Isabelle Berry,et al.  Cortical Areas Involved in Virtual Movement of Phantom Limbs: Comparison with Normal Subjects , 2003, Neurosurgery.

[63]  Stefan Geyer,et al.  Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. , 2003, Journal of neurophysiology.

[64]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[65]  J. Hart,et al.  Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. , 2003, Brain research. Cognitive brain research.

[66]  Christoph Stippich,et al.  Somatotopic mapping of the human primary sensorimotor cortex during motor imagery and motor execution by functional magnetic resonance imaging , 2002, Neuroscience Letters.

[67]  O. Blanke,et al.  Neuropsychology: Stimulating illusory own-body perceptions , 2002, Nature.

[68]  Alan C. Evans,et al.  Motor Learning Produces Parallel Dynamic Functional Changes during the Execution and Imagination of Sequential Foot Movements , 2002, NeuroImage.

[69]  C. Frith,et al.  Experiencing Oneself vs Another Person as Being the Cause of an Action: The Neural Correlates of the Experience of Agency , 2002, NeuroImage.

[70]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

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

[73]  S Iwaki,et al.  Neural substrates involved in imitating finger configurations: an fMRI study , 2001, Neuroreport.

[74]  R. Turner,et al.  Characterization and Correction of Interpolation Effects in the Realignment of fMRI Time Series , 2000, NeuroImage.

[75]  Alan C. Evans,et al.  Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space , 1999, NeuroImage.

[76]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[77]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[78]  E. Tunik,et al.  Sensorimotor training in virtual reality: a review. , 2009, NeuroRehabilitation.

[79]  Anne R. Isaac,et al.  An instrument for assessing imagery of movement: The Vividness of Movement Imagery Questionnaire (VMIQ). , 1986 .

[80]  ã Federation of European Neuroscience Societies SHORT COMMUNICATION , 2022 .