Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons.

We have adopted an analysis that produces a post hoc prediction of the time course of electromyogram (EMG) activity from the discharge of ensembles of neurons recorded sequentially from the primary motor cortex (M1) of a monkey. Over several recording sessions, we collected data from 50 M1 neurons and several distal forelimb muscles during a stereotyped precision grip task. Ensemble averages were constructed from 5 to 10 trials for each neuron and EMG signal. We used multiple linear regression on randomly chosen subsets of these neurons to find the best fit between the neuronal and EMG data. The fixed delay between neuronal and EMG signals that yielded the largest coefficient of determination (R(2)) between predicted and actual EMG was 50 ms. R(2) averaged 0.83 for ensembles composed of 15 neurons. If, instead, each neuronal signal was delayed by the time of its peak cross-correlation with the EMG signal, R(2) increased to 0.88. Using all 50 neurons, R(2) under these conditions averaged nearly 0.97. A similar analysis was conducted with signals recorded during both a power grip and a precision grip task. Quality of the fit dropped dramatically when parameters from the precision grip for a given set of neurons were used to fit data recorded during the power grip. However, when a single set of regression parameters was used to fit a combination of the two tasks, the quality of the fits decreased by <10% from that of a single task.

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

[2]  J. F. Soechting,et al.  Relationships between sensory input, motor output and unit activity in interpositus and red nuclei during intentional movement , 1978, Brain Research.

[3]  W. T. Thach Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. , 1978, Journal of neurophysiology.

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

[5]  Y Lamarre,et al.  Patterns of muscular and motor cortical activity during a simple arm movement in the monkey. , 1981, Canadian journal of physiology and pharmacology.

[6]  John F. Kalaska,et al.  Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations , 1983 .

[7]  H. Dr,et al.  Separate cortical systems for control of joint movement and joint stiffness: reciprocal activation and coactivation of antagonist muscles. , 1983 .

[8]  D. Humphrey,et al.  Separate cortical systems for control of joint movement and joint stiffness: reciprocal activation and coactivation of antagonist muscles. , 1983, Advances in neurology.

[9]  R. Lemon,et al.  Corticospinal neurons with a special role in precision grip , 1983, Brain Research.

[10]  F. Mussa-Ivaldi,et al.  Do neurons in the motor cortex encode movement direction? An alternative hypothesis , 1988, Neuroscience Letters.

[11]  J. Kalaska,et al.  A comparison of movement direction-related versus load direction- related activity in primate motor cortex, using a two-dimensional reaching task , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  E. Fetz,et al.  Control of forelimb muscle activity by populations of corticomotoneuronal and rubromotoneuronal cells. , 1989, Progress in brain research.

[13]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  R. Lemon,et al.  Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. , 1993, Journal of neurophysiology.

[15]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[16]  T Sinkjaer,et al.  Correlation of primate red nucleus discharge with muscle activity during free‐form arm movements. , 1993, The Journal of physiology.

[17]  A. Schwartz,et al.  A method for detecting the time course of correlation between single-unit activity and EMG during a behavioral task , 1995, Journal of Neuroscience Methods.

[18]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. , 1997, Journal of neurophysiology.

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

[20]  C. Heckman,et al.  Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. , 1998, Journal of neurophysiology.

[21]  T. Sinkjaer,et al.  Primate red nucleus discharge encodes the dynamics of limb muscle activity. , 1998, Journal of neurophysiology.

[22]  P. Cheney,et al.  Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic hand muscles during a reach and prehension task. , 1998, Journal of neurophysiology.

[23]  J. R. Rosenberg,et al.  Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans , 1998, Neuroscience Letters.

[24]  E. M. Pinches,et al.  The role of synchrony and oscillations in the motor output , 1999, Experimental Brain Research.

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

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

[27]  L M Jordan,et al.  Dendritic L‐type calcium currents in mouse spinal motoneurons: implications for bistability , 2000, The European journal of neuroscience.

[28]  P. Cheney,et al.  Correlations between corticomotoneuronal (CM) cell postspike effects and cell-target muscle covariation. , 2000, Journal of neurophysiology.

[29]  A. E. Schulman,et al.  Electroencephalographic measurement of motor cortex control of muscle activity in humans , 2000, Clinical Neurophysiology.

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

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

[32]  L. Miller,et al.  Primary motor cortical neurons encode functional muscle synergies , 2002, Experimental Brain Research.

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

[34]  A. Georgopoulos,et al.  On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional static isometric force , 2004, Experimental Brain Research.