Cortical Ensemble Adaptation to Represent Velocity of an Artificial Actuator Controlled by a Brain-Machine Interface

Monkeys can learn to directly control the movements of an artificial actuator by using a brain-machine interface (BMI) driven by the activity of a sample of cortical neurons. Eventually, they can do so without moving their limbs. Neuronal adaptations underlying the transition from control of the limb to control of the actuator are poorly understood. Here, we show that rapid modifications in neuronal representation of velocity of the hand and actuator occur in multiple cortical areas during the operation of a BMI. Initially, monkeys controlled the actuator by moving a hand-held pole. During this period, the BMI was trained to predict the actuator velocity. As the monkeys started using their cortical activity to control the actuator, the activity of individual neurons and neuronal populations became less representative of the animal's hand movements while representing the movements of the actuator. As a result of this adaptation, the animals could eventually stop moving their hands yet continue to control the actuator. These results show that, during BMI control, cortical ensembles represent behaviorally significant motor parameters, even if these are not associated with movements of the animal's own limb.

[1]  P. Matthews,et al.  Changing brain networks for visuomotor control with increased movement automaticity. , 2004, Journal of neurophysiology.

[2]  E. Fetz,et al.  Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. , 1996, Journal of neurophysiology.

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

[4]  S. Wise,et al.  Insights into seeing and grasping: distinguishing the neural correlates of perception and action. , 2002, Behavioral and cognitive neuroscience reviews.

[5]  G. E. Alexander,et al.  Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. , 1997, Journal of neurophysiology.

[6]  M. Tanaka,et al.  Coding of modified body schema during tool use by macaque postcentral neurones. , 1996, Neuroreport.

[7]  Jun Tanji,et al.  Effects of image motion in the dorsal premotor cortex during planning of an arm movement. , 2002, Journal of neurophysiology.

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

[9]  S. Wise,et al.  Oscillations in the premotor cortex: single-unit activity from awake, behaving monkeys , 2000, Experimental Brain Research.

[10]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[11]  A. Georgopoulos,et al.  The motor cortex and the coding of force. , 1992, Science.

[12]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

[14]  S. Scott Optimal feedback control and the neural basis of volitional motor control , 2004, Nature Reviews Neuroscience.

[15]  C. Spence,et al.  Multisensory integration and the body schema: close to hand and within reach , 2003, Current Biology.

[16]  Mark Hallett,et al.  A functional magnetic resonance imaging study of cortical regions associated with motor task execution and motor ideation in humans , 1995 .

[17]  M A Lebedev,et al.  Prefrontal cortex neurons reflecting reports of a visual illusion. , 2001, Journal of neurophysiology.

[18]  R. Nelson,et al.  Vibration-entrained and premovement activity in monkey primary somatosensory cortex. , 1994, Journal of neurophysiology.

[19]  S. Wise,et al.  Tuning for the orientation of spatial attention in dorsal premotor cortex , 2001, The European journal of neuroscience.

[20]  A. P. Georgopoulos,et al.  Variability and Correlated Noise in the Discharge of Neurons in Motor and Parietal Areas of the Primate Cortex , 1998, The Journal of Neuroscience.

[21]  Sonja Grün,et al.  Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation , 2000, Journal of Physiology-Paris.

[22]  Jerald D. Kralik,et al.  Representation of Attended Versus Remembered Locations in Prefrontal Cortex , 2004, PLoS biology.

[23]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[24]  M. Nicolelis,et al.  Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings , 1997, Neuron.

[25]  G E Alexander,et al.  Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. , 1997, Journal of neurophysiology.

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

[27]  Jerald D. Kralik,et al.  Techniques for long-term multisite neuronal ensemble recordings in behaving animals. , 2001, Methods.

[28]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[29]  E. Fetz,et al.  Functional classes of primate corticomotoneuronal cells and their relation to active force. , 1980, Journal of neurophysiology.

[30]  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.

[31]  M. Graziano Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[33]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[34]  A. Aertsen,et al.  Spike synchronization and rate modulation differentially involved in motor cortical function. , 1997, Science.

[35]  E. Vaadia,et al.  Primary motor cortex is involved in bimanual coordination , 1998, Nature.

[36]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[37]  D. Hoffman,et al.  Direction of action is represented in the ventral premotor cortex , 2001, Nature Neuroscience.

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

[39]  A. P. Georgopoulos,et al.  Neuronal population coding of movement direction. , 1986, Science.

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

[41]  M. Nicolelis,et al.  Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. , 1995, Science.

[42]  Michael I. Jordan,et al.  Optimal feedback control as a theory of motor coordination , 2002, Nature Neuroscience.

[43]  G. Holmes,et al.  Sensory disturbances from cerebral lesions , 1911 .

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

[45]  Miguel A L Nicolelis,et al.  Reduction of Single-Neuron Firing Uncertainty by Cortical Ensembles during Motor Skill Learning , 2004, The Journal of Neuroscience.

[46]  Isabelle Berry,et al.  Cortical Areas Involved in Virtual Movement of Phantom Limbs: Comparison with Normal Subjects , 2003, Neurosurgery.

[47]  E. Bizzi,et al.  Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. , 2004, Journal of neurophysiology.

[48]  Parag G. Patil,et al.  Ensemble Recordings Of Human Subcortical Neurons as a Source Of Motor Control Signals For a Brain-Machine Interface , 2004, Neurosurgery.

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

[50]  L. Paninski,et al.  Information about movement direction obtained from synchronous activity of motor cortical neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Sidarta Ribeiro,et al.  Multielectrode recordings: the next steps , 2002, Current Opinion in Neurobiology.

[52]  K. Zilles,et al.  Illusory Arm Movements Activate Cortical Motor Areas: A Positron Emission Tomography Study , 1999, The Journal of Neuroscience.

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

[54]  M. Nicolelis,et al.  Optimizing a Linear Algorithm for Real-Time Robotic Control using Chronic Cortical Ensemble Recordings in Monkeys , 2004, Journal of Cognitive Neuroscience.

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

[56]  Apostolos P Georgopoulos,et al.  Neural aspects of cognitive motor control , 2000, Current Opinion in Neurobiology.

[57]  G E Alexander,et al.  Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[58]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[59]  Stefan Geyer,et al.  Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. , 2003, Journal of neurophysiology.

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

[61]  A. Georgopoulos,et al.  Parietal representation of hand velocity in a copy task. , 2005, Journal of neurophysiology.

[62]  E. Vaadia,et al.  Preparatory activity in motor cortex reflects learning of local visuomotor skills , 2003, Nature Neuroscience.

[63]  R N Lemon,et al.  Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. , 2001, Journal of neurophysiology.

[64]  S. Wise,et al.  Changes in motor cortical activity during visuomotor adaptation , 1998, Experimental Brain Research.

[65]  Toshio Tsuji,et al.  Brain activation during manipulation of the myoelectric prosthetic hand: a functional magnetic resonance imaging study , 2004, NeuroImage.

[66]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[67]  Carolyn R. Mason,et al.  Central processes for the multiparametric control of arm movements in primates , 2001, Current Opinion in Neurobiology.

[68]  Eilon Vaadia,et al.  Learning-Induced Improvement in Encoding and Decoding of Specific Movement Directions by Neurons in the Primary Motor Cortex , 2004, PLoS biology.

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

[70]  Jerald D. Kralik,et al.  Chronic, multisite, multielectrode recordings in macaque monkeys , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[71]  E. Evarts Pyramidal tract activity associated with a conditioned hand movement in the monkey. , 1966, Journal of neurophysiology.

[72]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

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

[74]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[75]  R. Passingham,et al.  That's My Hand! Activity in Premotor Cortex Reflects Feeling of Ownership of a Limb , 2004, Science.

[76]  T. Ebner,et al.  Processing of multiple kinematic signals in the cerebellum and motor cortices , 2000, Brain Research Reviews.

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

[78]  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.

[79]  Eilon Vaadia,et al.  Viewing and doing: similar cortical mechanisms for perceptual and motor learning , 2004, Trends in Neurosciences.