Multimodal functional imaging of motor imagery using a novel paradigm

Neuroimaging studies have shown that the neural mechanisms of motor imagery (MI) overlap substantially with the mechanisms of motor execution (ME). Surprisingly, however, the role of several regions of the motor circuitry in MI remains controversial, a variability that may be due to differences in neuroimaging techniques, MI training, instruction types, or tasks used to evoke MI. The objectives of this study were twofold: (i) to design a novel task that reliably invokes MI, provides a reliable behavioral measure of MI performance, and is transferable across imaging modalities; and (ii) to measure the common and differential activations for MI and ME with functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG). We present a task in which it is difficult to give accurate responses without the use of either motor execution or motor imagery. The behavioral results demonstrate that participants performed similarly on the task when they imagined vs. executed movements and this performance did not change over time. The fMRI results show a spatial overlap of MI and ME in a number of motor and premotor areas, sensory cortices, cerebellum, inferior frontal gyrus, and ventrolateral thalamus. MI uniquely engaged bilateral occipital areas, left parahippocampus, and other temporal and frontal areas, whereas ME yielded unique activity in motor and sensory areas, cerebellum, precuneus, and putamen. The MEG results show a robust event-related beta band desynchronization in the proximity of primary motor and premotor cortices during both ME and MI. Together, these results further elucidate the neural circuitry of MI and show that our task robustly and reliably invokes motor imagery, and thus may prove useful for interrogating the functional status of the motor circuitry in patients with motor disorders.

[1]  Y. Adachi,et al.  Magnetoencephalogram systems developed at KIT , 1999, IEEE Transactions on Applied Superconductivity.

[2]  R. Poldrack,et al.  Cortical and Subcortical Contributions to Stop Signal Response Inhibition: Role of the Subthalamic Nucleus , 2006, The Journal of Neuroscience.

[3]  F J Valero-Cuevas,et al.  Fine-wire electromyographic recording during force generation. Application to index finger kinesiologic studies. , 1997, American journal of physical medicine & rehabilitation.

[4]  Volkmar Glauche,et al.  Ventral and dorsal fiber systems for imagined and executed movement , 2012, Experimental Brain Research.

[5]  M. Jeannerod,et al.  Possible involvement of primary motor cortex in mentally simulated movement: a functional magnetic resonance imaging study. , 1996, Neuroreport.

[6]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[7]  Karl J. Friston,et al.  Cortical areas and the selection of movement: a study with positron emission tomography , 1991, Experimental Brain Research.

[8]  M. Lotze,et al.  Motor imagery , 2006, Journal of Physiology-Paris.

[9]  Qing Gao,et al.  Evaluation of effective connectivity of motor areas during motor imagery and execution using conditional Granger causality , 2011, NeuroImage.

[10]  S. Murphy Imagery interventions in sport. , 1994, Medicine and science in sports and exercise.

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

[12]  M. Jeannerod,et al.  Vegetative response during imagined movement is proportional to mental effort , 1991, Behavioural Brain Research.

[13]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[14]  A. Berthoz,et al.  Mental representations of movements. Brain potentials associated with imagination of eye movements , 1999, Clinical Neurophysiology.

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

[16]  M. Hallett,et al.  Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. , 2008, Cerebral cortex.

[17]  J B Poline,et al.  Partially overlapping neural networks for real and imagined hand movements. , 2000, Cerebral cortex.

[18]  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.

[19]  E. Naito,et al.  Internally Simulated Movement Sensations during Motor Imagery Activate Cortical Motor Areas and the Cerebellum , 2002, The Journal of Neuroscience.

[20]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

[22]  A. R. McIntosh,et al.  Spatiotemporal analysis of event-related fMRI data using partial least squares , 2004, NeuroImage.

[23]  M. Jeannerod Mental imagery in the motor context , 1995, Neuropsychologia.

[24]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[25]  Karl J. Friston,et al.  Principal component analysis learning algorithms: a neurobiological analysis , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  J. Decety,et al.  Comparative analysis of actual and mental movement times in two graphic tasks , 1989, Brain and Cognition.

[27]  C. Richards,et al.  Brain activity during visual versus kinesthetic imagery: An fMRI study , 2009, Human brain mapping.

[28]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

[29]  J. Annett Motor imagery: Perception or action? , 1995, Neuropsychologia.

[30]  Leslie G. Ungerleider,et al.  Changes in limbic and prefrontal functional interactions in a working memory task for faces. , 1996, Cerebral cortex.

[31]  R. Poldrack,et al.  Common neural substrates for inhibition of spoken and manual responses. , 2008, Cerebral cortex.

[32]  M. Hallett,et al.  Functional properties of brain areas associated with motor execution and imagery. , 2003, Journal of neurophysiology.

[33]  Adam P. Morris,et al.  Executive Brake Failure following Deactivation of Human Frontal Lobe , 2006 .

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

[35]  W Lang,et al.  Electric and magnetic fields of the brain accompanying internal simulation of movement. , 1996, Brain research. Cognitive brain research.

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

[37]  C. Molinaro,et al.  Mental Imagery Combined with Physical Practice of Approach Shots for Golf Beginners , 2005, Perceptual and motor skills.

[38]  Paul E. Downing,et al.  Visuo-motor imagery of specific manual actions: A multi-variate pattern analysis fMRI study , 2012, NeuroImage.

[39]  Robert Tibshirani,et al.  The Bootstrap Method for Assessing Statistical Accuracy , 1985 .

[40]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex , 2004, Trends in Cognitive Sciences.

[41]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[42]  Bruce M. Gans PRIMARY CARE FOR PERSONS WITH DISABILITIES: Establishing a Vision for the Future , 1997 .

[43]  Blake W. Johnson,et al.  Cerebral processes during visuo-motor imagery of hands. , 2006, Psychophysiology.

[44]  V. Jousmäki,et al.  Involvement of Primary Motor Cortex in Motor Imagery: A Neuromagnetic Study , 1997, NeuroImage.

[45]  K. Amunts,et al.  Broca's region subserves imagery of motion: A combined cytoarchitectonic and fMRI study , 2000, Human brain mapping.

[46]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[47]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

[48]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[49]  Eleanor A Maguire,et al.  A New Role for the Parahippocampal Cortex in Representing Space , 2011, The Journal of Neuroscience.

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

[51]  Thomas L. Saaty,et al.  Ratio Scales Derived from Perturbations of Consistent Judgments , 1990 .

[52]  F. Bookstein,et al.  Neurobehavioral effects of prenatal alcohol: Part II. Partial least squares analysis. , 1989, Neurotoxicology and teratology.

[53]  D. F. Marks,et al.  Visual imagery differences in the recall of pictures. , 1973, British journal of psychology.

[54]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[55]  Gen Uehara,et al.  Multi-Channel SQUID Systems for Biomagnetic Measurement , 2003 .

[56]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[57]  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.

[58]  Rupert Lanzenberger,et al.  The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling , 2008, NeuroImage.

[59]  H. C. Dijkerman,et al.  Does motor imagery training improve hand function in chronic stroke patients? A pilot study , 2004, Clinical rehabilitation.

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

[61]  M. Diamond,et al.  Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[62]  A. Berthoz,et al.  Mental representations of movements. Brain potentials associated with imagination of hand movements. , 1995, Electroencephalography and clinical neurophysiology.

[63]  Manuel Rodrı́guez,et al.  Hand movement distribution in the motor cortex: the influence of a concurrent task and motor imagery , 2004, NeuroImage.

[64]  Louis Yuge,et al.  Neuromagnetic beta oscillation changes during motor imagery and motor execution of skilled movements , 2011, Neuroreport.