Long-Term Asynchronous Decoding of Arm Motion Using Electrocorticographic Signals in Monkeys

Brain–machine interfaces (BMIs) employ the electrical activity generated by cortical neurons directly for controlling external devices and have been conceived as a means for restoring human cognitive or sensory-motor functions. The dominant approach in BMI research has been to decode motor variables based on single-unit activity (SUA). Unfortunately, this approach suffers from poor long-term stability and daily recalibration is normally required to maintain reliable performance. A possible alternative is BMIs based on electrocorticograms (ECoGs), which measure population activity and may provide more durable and stable recording. However, the level of long-term stability that ECoG-based decoding can offer remains unclear. Here we propose a novel ECoG-based decoding paradigm and show that we have successfully decoded hand positions and arm joint angles during an asynchronous food-reaching task in monkeys when explicit cues prompting the onset of movement were not required. Performance using our ECoG-based decoder was comparable to existing SUA-based systems while evincing far superior stability and durability. In addition, the same decoder could be used for months without any drift in accuracy or recalibration. These results were achieved by incorporating the spatio-spectro-temporal integration of activity across multiple cortical areas to compensate for the lower fidelity of ECoG signals. These results show the feasibility of high-performance, chronic and versatile ECoG-based neuroprosthetic devices for real-life applications. This new method provides a stable platform for investigating cortical correlates for understanding motor control, sensory perception, and high-level cognitive processes.

[1]  T. Yuen,et al.  Evaluation of electrode array material for neural prostheses. , 1979, Neurosurgery.

[2]  John P. Donoghue,et al.  Connecting cortex to machines: recent advances in brain interfaces , 2002, Nature Neuroscience.

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

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

[5]  J. Schall,et al.  Neural selection and control of visually guided eye movements. , 1999, Annual review of neuroscience.

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

[7]  Dennis A. Turner,et al.  The development of brain-machine interface neuroprosthetic devices , 2011, Neurotherapeutics.

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

[9]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces: past, present and future , 2006, Trends in Neurosciences.

[10]  Dylan F. Cooke,et al.  The Cortical Control of Movement Revisited , 2002, Neuron.

[11]  Jose C. Principe,et al.  Extraction and localization of mesoscopic motor control signals for human ECoG neuroprosthetics , 2008, Journal of Neuroscience Methods.

[12]  S. Scott,et al.  Cortical control of reaching movements , 1997, Current Opinion in Neurobiology.

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

[14]  G. Loeb,et al.  Histological reaction to various conductive and dielectric films chronically implanted in the subdural space. , 1977, Journal of biomedical materials research.

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

[16]  D. Szarowski,et al.  Brain responses to micro-machined silicon devices , 2003, Brain Research.

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

[18]  Karen L. Smith,et al.  Effects of insertion conditions on tissue strain and vascular damage during neuroprosthetic device insertion , 2006, Journal of neural engineering.

[19]  M. Laubach,et al.  Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task , 2000, Nature.

[20]  F. Mussa-Ivaldi,et al.  Brain–machine interfaces: computational demands and clinical needs meet basic neuroscience , 2003, Trends in Neurosciences.

[21]  Justin C. Williams,et al.  Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex , 2004, IEEE Transactions on Biomedical Engineering.

[22]  M. Nicolelis,et al.  Decoding of temporal intervals from cortical ensemble activity. , 2008, Journal of neurophysiology.

[23]  S. Wold,et al.  The Collinearity Problem in Linear Regression. The Partial Least Squares (PLS) Approach to Generalized Inverses , 1984 .

[24]  David M. Allen,et al.  The Relationship Between Variable Selection and Data Agumentation and a Method for Prediction , 1974 .

[25]  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.

[26]  J. Weiland,et al.  Visual and electrical evoked response recorded from subdural electrodes implanted above the visual cortex in normal dogs under two methods of anesthesia , 2003, Journal of Neuroscience Methods.

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

[28]  T. Yuen,et al.  Tissue response to potential neuroprosthetic materials implanted subdurally. , 1987, Biomaterials.

[29]  C. Mehring,et al.  Differential Representation of Arm Movement Direction in Relation to Cortical Anatomy and Function , 2008 .

[30]  Daniel W Moran,et al.  Computational model of a primate arm: from hand position to joint angles, joint torques and muscle forces , 2006, Journal of neural engineering.

[31]  Daryl R Kipke,et al.  Advanced Neurotechnologies for Chronic Neural Interfaces: New Horizons and Clinical Opportunities , 2008, The Journal of Neuroscience.

[32]  S. Wise,et al.  Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Robert Chen,et al.  Identification of arm movements using correlation of electrocorticographic spectral components and kinematic recordings , 2007, Journal of neural engineering.

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

[35]  J F Soechting,et al.  Moving in three-dimensional space: frames of reference, vectors, and coordinate systems. , 1992, Annual review of neuroscience.

[36]  W. Pilcher,et al.  Complications of epilepsy surgery. , 1993, Neurosurgery clinics of North America.

[37]  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.

[38]  Stanislav Herwik,et al.  Brain-computer interfaces: an overview of the hardware to record neural signals from the cortex. , 2009, Progress in brain research.

[39]  Nicholas G Hatsopoulos,et al.  The science of neural interface systems. , 2009, Annual review of neuroscience.

[40]  S. Scott,et al.  Changes in motor cortex activity during reaching movements with similar hand paths but different arm postures. , 1995, Journal of neurophysiology.

[41]  W. Freeman,et al.  Spatial spectra of scalp EEG and EMG from awake humans , 2003, Clinical Neurophysiology.

[42]  J. Wolpaw,et al.  Decoding flexion of individual fingers using electrocorticographic signals in humans , 2009, Journal of neural engineering.

[43]  M. Graziano,et al.  Complex Movements Evoked by Microstimulation of Precentral Cortex , 2002, Neuron.

[44]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces to restore motor function and probe neural circuits , 2003, Nature Reviews Neuroscience.

[45]  S. Farmer,et al.  Rhythmicity, synchronization and binding in human and primate motor systems , 1998, The Journal of physiology.

[46]  John P. Cunningham,et al.  Single-Neuron Stability during Repeated Reaching in Macaque Premotor Cortex , 2007, The Journal of Neuroscience.

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

[48]  Andrew B. Schwartz,et al.  Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics , 2006, Neuron.

[49]  J. F. Soechting,et al.  Moving effortlessly in three dimensions: does Donders' law apply to arm movement? , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  B. Kowalski,et al.  Partial least-squares regression: a tutorial , 1986 .