A functional magnetic resonance imaging study of visuomotor processing in a virtual reality‐based paradigm: Rehabilitation Gaming System

The Rehabilitation Gaming System (RGS) has been designed as a flexible, virtual‐reality (VR)‐based device for rehabilitation of neurological patients. Recently, training of visuomotor processing with the RGS was shown to effectively improve arm function in acute and chronic stroke patients. It is assumed that the VR‐based training protocol related to RGS creates conditions that aid recovery by virtue of the human mirror neuron system. Here, we provide evidence for this assumption by identifying the brain areas involved in controlling the catching of approaching colored balls in the virtual environment of the RGS. We used functional magnetic resonance imaging of 18 right‐handed healthy subjects (24 ± 3 years) in both active and imagination conditions. We observed that the imagery of target catching was related to activation of frontal, parietal, temporal, cingulate and cerebellar regions. We interpret these activations in relation to object processing, attention, mirror mechanisms, and motor intention. Active catching followed an anticipatory mode, and resulted in significantly less activity in the motor control areas. Our results provide preliminary support for the hypothesis underlying RGS that this novel neurorehabilitation approach engages human mirror mechanisms that can be employed for visuomotor training.

[1]  C. Winstein,et al.  The Mirror Neuron System: A Neural Substrate for Methods in Stroke Rehabilitation , 2010, Neurorehabilitation and neural repair.

[2]  R. Seitz How imaging will guide rehabilitation , 2010, Current opinion in neurology.

[3]  P. Langhorne,et al.  Stroke rehabilitation , 2011, The Lancet.

[4]  R. Seitz,et al.  Learning of Sequential Finger Movements in Man: A Combined Kinematic and Positron Emission Tomography (PET) Study , 1992, The European journal of neuroscience.

[5]  Gereon R. Fink,et al.  Mirror Neuron and Theory of Mind Mechanisms Involved in Face-to-Face Interactions: A Functional Magnetic Resonance Imaging Approach to Empathy , 2007, Journal of Cognitive Neuroscience.

[6]  G. Fink,et al.  Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches , 2011, Brain : a journal of neurology.

[7]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.

[8]  F Chollet,et al.  Neural Substrate for the Effects of Passive Training on Sensorimotor Cortical Representation: A Study with Functional Magnetic Resonance Imaging in Healthy Subjects , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[9]  E. Rolls,et al.  Value, Pleasure and Choice in the Ventral Prefrontal Cortex , 2022 .

[10]  Soojin Park,et al.  Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception , 2009, NeuroImage.

[11]  Paul F. M. J. Verschure,et al.  Neuroscience, virtual reality and neurorehabilitation: Brain repair as a validation of brain theory , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[12]  M. Chopp,et al.  Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation , 2012, The Lancet Neurology.

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

[14]  J. Mazziotta,et al.  Mirror neuron system: basic findings and clinical applications , 2007, Annals of neurology.

[15]  Steven C Cramer,et al.  Cortical Plasticity Following Motor Skill Learning During Mental Practice in Stroke , 2009, Neurorehabilitation and neural repair.

[16]  Justin T. Maxwell,et al.  From novice to no know-how: A longitudinal study of implicit motor learning , 2000, Journal of sports sciences.

[17]  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.

[18]  Rüdiger J. Seitz,et al.  Relationship Between Interhemispheric Inhibition and Motor Cortex Excitability in Subacute Stroke Patients , 2008, Neurorehabilitation and neural repair.

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

[20]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

[21]  R. Seitz,et al.  Diversity of the inferior frontal gyrus—A meta-analysis of neuroimaging studies , 2011, Behavioural Brain Research.

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

[23]  Paul F. M. J. Verschure,et al.  Distributed Adaptive Control: A theory of the Mind, Brain, Body Nexus , 2012, BICA 2012.

[24]  P. Verschure,et al.  Virtual reality based rehabilitation speeds up functional recovery of the upper extremities after stroke: a randomized controlled pilot study in the acute phase of stroke using the rehabilitation gaming system. , 2011, Restorative neurology and neuroscience.

[25]  G. Wittenberg,et al.  Dynamic Course of Intracortical TMS Paired-Pulse Responses During Recovery of Motor Function After Stroke , 2007, Neurorehabilitation and neural repair.

[26]  O. Leidner,et al.  Best Conventional Therapy Versus Modular Impairment-Oriented Training for Arm Paresis After Stroke: A Single-Blind, Multicenter Randomized Controlled Trial , 2009, Neurorehabilitation and neural repair.

[27]  Gary F. Egan,et al.  Evolution of Brain Activation with Good and Poor Motor Recovery after Stroke , 2006, Neurorehabilitation and neural repair.

[28]  G. Kwakkel,et al.  Intensity of leg and arm training after primary middle-cerebral-artery stroke: a randomised trial , 1999, The Lancet.

[29]  H. Hummelsheim,et al.  Influence of physiotherapeutic facilitation techniques on motor evoked potentials in centrally paretic hand extensor muscles. , 1995, Electroencephalography and clinical neurophysiology.

[30]  P. Celnik,et al.  Stroke Rehabilitation. , 2015, Physical medicine and rehabilitation clinics of North America.

[31]  M Massucci,et al.  Cardiorespiratory comorbidity: a new challenge for physical and rehabilitation medicine specialist. , 2012, European journal of physical and rehabilitation medicine.

[32]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[33]  R. J. Seitz,et al.  Conscious and Subconscious Sensorimotor Synchronization—Prefrontal Cortex and the Influence of Awareness , 2002, NeuroImage.

[34]  E. Rolls,et al.  From affective value to decision‐making in the prefrontal cortex , 2008, The European journal of neuroscience.

[35]  Leonardo G. Cohen,et al.  Recovery of function in humans: Cortical stimulation and pharmacological treatments after stroke , 2010, Neurobiology of Disease.

[36]  M. Franceschini,et al.  Action observation and mirror neuron network: a tool for motor stroke rehabilitation. , 2012, European journal of physical and rehabilitation medicine.

[37]  Debraj Mukherjee,et al.  Epidemiology and the global burden of stroke. , 2011, World neurosurgery.

[38]  Volker Hömberg,et al.  Remote changes in cortical excitability after stroke. , 2003, Brain : a journal of neurology.

[39]  Antonio Frisoli,et al.  The Combined Impact of Virtual Reality Neurorehabilitation and Its Interfaces on Upper Extremity Functional Recovery in Patients With Chronic Stroke , 2012, Stroke.

[40]  M. Casini,et al.  Effect of Mental Imagery on the Development of Skilled Motor Actions , 2007, Perceptual and motor skills.

[41]  G. Rizzolatti,et al.  Mirror neurons and their clinical relevance , 2009, Nature Clinical Practice Neurology.

[42]  P. Verschure,et al.  Neurorehabilitation using the virtual reality based Rehabilitation Gaming System: methodology, design, psychometrics, usability and validation , 2010, Journal of NeuroEngineering and Rehabilitation.

[43]  R. Seitz,et al.  Role of neuroimaging in promoting long‐term recovery from ischemic stroke , 2010, Journal of magnetic resonance imaging : JMRI.

[44]  R. Seitz,et al.  Mental practice improves hand function after hemiparetic stroke. , 2007, Restorative neurology and neuroscience.

[45]  M. Iacoboni,et al.  The mirror neuron system and the consequences of its dysfunction , 2006, Nature Reviews Neuroscience.

[46]  Ron Borowsky,et al.  Modularity and Intersection of “What”, “Where” and “How” Processing of Visual Stimuli: A New Method of fMRI Localization , 2005, Brain Topography.

[47]  Jing Luo,et al.  Sport expert's motor imagery: Functional imaging of professional motor skills and simple motor skills , 2010, Brain Research.

[48]  Eduardo Martínez-Vila,et al.  The Cost of Stroke , 2003, Cerebrovascular Diseases.

[49]  C. Espinosa-Garcia,et al.  Neuroprotective effects of progesterone and allopregnanolone on long-term cognitive outcome after global cerebral ischemia. , 2011, Restorative neurology and neuroscience.

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

[51]  Paul F. M. J. Verschure,et al.  Environmentally mediated synergy between perception and behaviour in mobile robots , 2003, Nature.

[52]  C. Frith,et al.  “Hey John”: Signals Conveying Communicative Intention toward the Self Activate Brain Regions Associated with “Mentalizing,” Regardless of Modality , 2003, The Journal of Neuroscience.

[53]  Steven C. Cramer Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery , 2008, Annals of neurology.