Differential Representation of Arm Movement Direction in Relation to Cortical Anatomy and Function

Information about arm movement direction in neuronal activity of the cerebral cortex can be used for movement control mediated by a brain-machine interface (BMI). Here we provide a topographic analysis of the information related to arm movement direction that can be extracted from single trials of electrocorticographic (ECoG) signals recorded from the human frontal and parietal cortex based on a precise assignment of ECoG recording channels to the subjects' individual cortical anatomy and function. To this aim, each electrode contact was identified on structural MRI scans acquired while the electrodes were implanted and was thus related to the brain anatomy of each patient. Cortical function was assessed by direct cortical electrical stimulation. We show that activity from the primary motor cortex, in particular from the region showing hand and arm motor responses upon electrical stimulation, carries most directional information. The premotor, posterior parietal and lateral prefrontal cortex contributed gradually less, but still significant information. This gradient was observed for decoding from movement-related potentials, and from spectral amplitude modulations in low frequencies and in the high gamma band. Our findings thus demonstrate a close topographic correlation between cortical functional anatomy and direction-related information in humans that might be used for brain-machine interfacing.

[1]  H. Kornhuber,et al.  [CHANGES IN THE BRAIN POTENTIAL IN VOLUNTARY MOVEMENTS AND PASSIVE MOVEMENTS IN MAN: READINESS POTENTIAL AND REAFFERENT POTENTIALS]. , 1965, Pflugers Archiv fur die gesamte Physiologie des Menschen und der Tiere.

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

[3]  H. Steinmetz,et al.  Craniocerebral topography within the international 10-20 system. , 1989, Electroencephalography and clinical neurophysiology.

[4]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[5]  R P Lesser,et al.  Functional significance of the mu rhythm of human cortex: an electrophysiologic study with subdural electrodes. , 1993, Electroencephalography and clinical neurophysiology.

[6]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

[7]  O Levrier,et al.  Location of hand function in the sensorimotor cortex: MR and functional correlation. , 1994, AJNR. American journal of neuroradiology.

[8]  T J Ebner,et al.  8-12 Hz rhythmic oscillations in human motor cortex during two-dimensional arm movements: evidence for representation of kinematic parameters. , 1994, Electroencephalography and clinical neurophysiology.

[9]  G Pfurtscheller,et al.  EEG-based brain computer interface (BCI). Search for optimal electrode positions and frequency components. , 1995, Medical progress through technology.

[10]  A. Walden,et al.  Spectral analysis for physical applications : multitaper and conventional univariate techniques , 1996 .

[11]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[12]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[13]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[14]  B. Feige,et al.  The Role of Higher-Order Motor Areas in Voluntary Movement as Revealed by High-Resolution EEG and fMRI , 1999, NeuroImage.

[15]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[16]  A P Batista,et al.  Reach plans in eye-centered coordinates. , 1999, Science.

[17]  Miguel A. L. Nicolelis,et al.  Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex , 1999, Nature Neuroscience.

[18]  H. Flor,et al.  A spelling device for the paralysed , 1999, Nature.

[19]  F. Aokia,et al.  Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks , 1999 .

[20]  S P Levine,et al.  A direct brain interface based on event-related potentials. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[21]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[22]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[23]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[24]  Dawn M. Taylor,et al.  Direct Cortical Control of 3D Neuroprosthetic Devices , 2002, Science.

[25]  Nicholas G. Hatsopoulos,et al.  Brain-machine interface: Instant neural control of a movement signal , 2002, Nature.

[26]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[27]  J. Spreer,et al.  Visualization of subdural strip and grid electrodes using curvilinear reformatting of 3D MR imaging data sets. , 2002, AJNR. American journal of neuroradiology.

[28]  S. Meagher Instant neural control of a movement signal , 2002 .

[29]  S. P. Levine,et al.  Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement , 2003, Clinical Neurophysiology.

[30]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[31]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[32]  R. Andersen,et al.  Neural prosthetic control signals from plan activity , 2003, Neuroreport.

[33]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

[34]  T. Vilis,et al.  Gaze-Centered Updating of Visual Space in Human Parietal Cortex , 2003, The Journal of Neuroscience.

[35]  C. Mehring,et al.  Inference of hand movements from local field potentials in monkey motor cortex , 2003, Nature Neuroscience.

[36]  C. Mehring,et al.  Comparing information about arm movement direction in single channels of local and epicortical field potentials from monkey and human motor cortex , 2004, Journal of Physiology-Paris.

[37]  Nicholas Hatsopoulos,et al.  Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. , 2004, Journal of neurophysiology.

[38]  José del R. Millán,et al.  Noninvasive brain-actuated control of a mobile robot by human EEG , 2004, IEEE Transactions on Biomedical Engineering.

[39]  Mayer Aladjem,et al.  Regularized discriminant analysis for face recognition , 2004, Pattern Recognit..

[40]  Tonio Ball,et al.  Towards an implantable brain-machine interface based on epicortical field potentials , 2004 .

[41]  Jonathan R Wolpaw,et al.  Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Gerwin Schalk,et al.  A brain–computer interface using electrocorticographic signals in humans , 2004, Journal of neural engineering.

[43]  J. Tanji,et al.  Functional specialization in dorsal and ventral premotor areas. , 2004, Progress in brain research.

[44]  H. Kornhuber,et al.  Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale , 1965, Pflüger's Archiv für die gesamte Physiologie des Menschen und der Tiere.

[45]  R. Andersen,et al.  Selecting the signals for a brain–machine interface , 2004, Current Opinion in Neurobiology.

[46]  A. Schwartz,et al.  Differential Representation of Perception and Action in the Frontal Cortex , 2004, Science.

[47]  Leonardo Fogassi,et al.  Motor functions of the parietal lobe , 2005, Current Opinion in Neurobiology.

[48]  Adam N Mamelak,et al.  Spatial selectivity in human ventrolateral prefrontal cortex , 2005, Nature Neuroscience.

[49]  C. Mehring,et al.  Encoding of Movement Direction in Different Frequency Ranges of Motor Cortical Local Field Potentials , 2005, The Journal of Neuroscience.

[50]  David M. Santucci,et al.  Frontal and parietal cortical ensembles predict single‐trial muscle activity during reaching movements in primates , 2005, The European journal of neuroscience.

[51]  Arnaud Delorme,et al.  High-Frequency γ-Band Activity in the Basal Temporal Cortex during Picture-Naming and Lexical-Decision Tasks , 2005, The Journal of Neuroscience.

[52]  D. Kovalev,et al.  Rapid and fully automated visualization of subdural electrodes in the presurgical evaluation of epilepsy patients. , 2005, AJNR. American journal of neuroradiology.

[53]  C. Crainiceanu,et al.  Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. , 2005, Brain : a journal of neurology.

[54]  A. Engel,et al.  Invasive recordings from the human brain: clinical insights and beyond , 2005, Nature Reviews Neuroscience.

[55]  Philippe Kahane,et al.  High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex , 2005, NeuroImage.

[56]  M. Hallett,et al.  What is the Bereitschaftspotential? , 2006, Clinical Neurophysiology.

[57]  Rajesh P. N. Rao,et al.  Electrocorticography-based brain computer Interface-the seattle experience , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[58]  G. Schalk,et al.  ECoG factors underlying multimodal control of a brain-computer interface , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[60]  R. Andersen,et al.  Dorsal Premotor Neurons Encode the Relative Position of the Hand, Eye, and Goal during Reach Planning , 2006, Neuron.

[61]  R. Andersen,et al.  Target Selection Signals for Arm Reaching in the Posterior Parietal Cortex , 2007, The Journal of Neuroscience.

[62]  Tutis Vilis,et al.  Human parietal "reach region" primarily encodes intrinsic visual direction, not extrinsic movement direction, in a visual motor dissociation task. , 2007, Cerebral cortex.

[63]  J. Wolpaw,et al.  Decoding two-dimensional movement trajectories using electrocorticographic signals in humans , 2007, Journal of neural engineering.

[64]  Dennis C. Tkach,et al.  Congruent Activity during Action and Action Observation in Motor Cortex , 2007, The Journal of Neuroscience.

[65]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[66]  Eran Stark,et al.  Predicting Movement from Multiunit Activity , 2007, The Journal of Neuroscience.

[67]  K. Sekihara,et al.  Spatial Localization of Cortical Time-Frequency Dynamics , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[68]  Robert T. Knight,et al.  Five-dimensional neuroimaging: Localization of the time–frequency dynamics of cortical activity , 2008, NeuroImage.

[69]  Paul Ferrari,et al.  Self-paced movements induce high-frequency gamma oscillations in primary motor cortex , 2008, NeuroImage.

[70]  Rajesh P. N. Rao,et al.  Beyond the Gamma Band: The Role of High-Frequency Features in Movement Classification , 2008, IEEE Transactions on Biomedical Engineering.

[71]  C. McIntyre,et al.  Chronic subdural electrodes in the management of epilepsy , 2008, Clinical Neurophysiology.

[72]  Andreas Schulze-Bonhage,et al.  Prediction of arm movement trajectories from ECoG-recordings in humans , 2008, Journal of Neuroscience Methods.

[73]  J. A. Wilson,et al.  Two-dimensional movement control using electrocorticographic signals in humans , 2008, Journal of neural engineering.

[74]  Dean J Krusienski,et al.  Emulation of computer mouse control with a noninvasive brain–computer interface , 2008, Journal of neural engineering.

[75]  E. Fetz,et al.  Direct control of paralyzed muscles by cortical neurons , 2008, Nature.

[76]  C. Braun,et al.  Hand Movement Direction Decoded from MEG and EEG , 2008, The Journal of Neuroscience.

[77]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[78]  Paolo Maria Rossini,et al.  High-gamma band activity of primary hand cortical areas: A sensorimotor feedback efficiency index , 2008, NeuroImage.

[79]  Gerwin Schalk,et al.  Unique Cortical Physiology Associated With Ipsilateral Hand Movements and Neuroprosthetic Implications , 2008, Stroke.

[80]  Andreas Schulze-Bonhage,et al.  Movement related activity in the high gamma range of the human EEG , 2008, NeuroImage.

[81]  Rajesh P. N. Rao,et al.  Generalized Features for Electrocorticographic BCIs , 2008, IEEE Transactions on Biomedical Engineering.

[82]  Andrew S. Whitford,et al.  Cortical control of a prosthetic arm for self-feeding , 2008, Nature.

[83]  Andreas Schulze-Bonhage,et al.  Signal quality of simultaneously recorded invasive and non-invasive EEG , 2009, NeuroImage.

[84]  W. A. Sarnacki,et al.  Electroencephalographic (EEG) control of three-dimensional movement , 2010, Journal of neural engineering.