Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia

Computer-mediated connections between human motor cortical neurons and assistive devices promise to improve or restore lost function in people with paralysis. Recently, a pilot clinical study of an intracortical neural interface system demonstrated that a tetraplegic human was able to obtain continuous two-dimensional control of a computer cursor using neural activity recorded from his motor cortex. This control, however, was not sufficiently accurate for reliable use in many common computer control tasks. Here, we studied several central design choices for such a system including the kinematic representation for cursor movement, the decoding method that translates neuronal ensemble spiking activity into a control signal and the cursor control task used during training for optimizing the parameters of the decoding method. In two tetraplegic participants, we found that controlling a cursor's velocity resulted in more accurate closed-loop control than controlling its position directly and that cursor velocity control was achieved more rapidly than position control. Control quality was further improved over conventional linear filters by using a probabilistic method, the Kalman filter, to decode human motor cortical activity. Performance assessment based on standard metrics used for the evaluation of a wide range of pointing devices demonstrated significantly improved cursor control with velocity rather than position decoding.

[1]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Miguel A. L. Nicolelis,et al.  Actions from thoughts , 2001, Nature.

[3]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

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

[5]  Miriam Zacksenhouse,et al.  Cortical Ensemble Adaptation to Represent Velocity of an Artificial Actuator Controlled by a Brain-Machine Interface , 2005, The Journal of Neuroscience.

[6]  K. Pearson Mathematical Contributions to the Theory of Evolution. III. Regression, Heredity, and Panmixia , 1896 .

[7]  A B Schwartz,et al.  Motor cortical representation of speed and direction during reaching. , 1999, Journal of neurophysiology.

[8]  Michael J. Black,et al.  Probabilistic Inference of Hand Motion from Neural Activity in Motor Cortex , 2001, NIPS.

[9]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[10]  T. Başar,et al.  A New Approach to Linear Filtering and Prediction Problems , 2001 .

[11]  H. Hotelling New Light on the Correlation Coefficient and its Transforms , 1953 .

[12]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[13]  D.M. Taylor,et al.  Information conveyed through brain-control: cursor versus robot , 2003, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[14]  Sarah A. Douglas,et al.  Testing pointing device performance and user assessment with the ISO 9241, Part 9 standard , 1999, CHI '99.

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

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

[17]  J. Kalaska,et al.  Changes in the temporal pattern of primary motor cortex activity in a directional isometric force versus limb movement task. , 1998, Journal of neurophysiology.

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

[19]  Byron M. Yu,et al.  Mixture of Trajectory Models for Neural Decoding of Goal-directed Movements a Computational Model of Craving and Obsession Decoding Visual Inputs from Multiple Neurons in the Human Temporal Lobe Encoding Contribution of Individual Retinal Ganglion Cell Responses to Velocity and Acceleration , 2008 .

[20]  Michael J. Black,et al.  Modeling and decoding motor cortical activity using a switching Kalman filter , 2004, IEEE Transactions on Biomedical Engineering.

[21]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during spiral tracing. , 1999, Journal of neurophysiology.

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

[23]  I. Scott MacKenzie,et al.  Accuracy measures for evaluating computer pointing devices , 2001, CHI.

[24]  E. Fetz,et al.  Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. , 1980, Journal of neurophysiology.

[25]  J. Chapin Using multi-neuron population recordings for neural prosthetics , 2004, Nature Neuroscience.

[26]  R. Andersen,et al.  Cognitive Control Signals for Neural Prosthetics , 2004, Science.

[27]  Michael J. Black,et al.  Multi-state decoding of point-and-click control signals from motor cortical activity in a human with tetraplegia , 2007, 2007 3rd International IEEE/EMBS Conference on Neural Engineering.

[28]  R. E. Kalman,et al.  A New Approach to Linear Filtering and Prediction Problems , 2002 .

[29]  L. Paninski,et al.  Spatiotemporal tuning of motor cortical neurons for hand position and velocity. , 2004, Journal of neurophysiology.

[30]  D R Humphrey,et al.  Predicting Measures of Motor Performance from Multiple Cortical Spike Trains , 1970, Science.

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

[32]  Wei Wu,et al.  Bayesian Population Decoding of Motor Cortical Activity Using a Kalman Filter , 2006, Neural Computation.

[33]  J. Donoghue,et al.  Primary Motor Cortex Tuning to Intended Movement Kinematics in Humans with Tetraplegia , 2008, The Journal of Neuroscience.

[34]  M A Lebedev,et al.  A comparison of optimal MIMO linear and nonlinear models for brain–machine interfaces , 2006, Journal of neural engineering.

[35]  R E Kass,et al.  Recursive bayesian decoding of motor cortical signals by particle filtering. , 2004, Journal of neurophysiology.

[36]  J. Flanagan,et al.  Task-specific internal models for kinematic transformations. , 2003, Journal of neurophysiology.

[37]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[38]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[41]  Arthur Gelb,et al.  Applied Optimal Estimation , 1974 .

[42]  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.

[43]  Michael J. Black,et al.  Closed-loop neural control of cursor motion using a Kalman filter , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[44]  Byron M. Yu,et al.  A high-performance brain–computer interface , 2006, Nature.

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

[46]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[47]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during lemniscate tracing. , 1999 .

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

[49]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. III. Positional gradients and population coding of movement direction from various movement origins , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  E. Todorov Direct cortical control of muscle activation in voluntary arm movements: a model , 2000, Nature Neuroscience.

[51]  Pamela Reinagel,et al.  Decoding visual information from a population of retinal ganglion cells. , 1997, Journal of neurophysiology.