RelationshipbetweenUnconstrainedArmMovementsand Single-NeuronFiringintheMacaqueMotorCortex

The activity of single neurons in the monkey motor cortex was studied during semi-naturalistic, unstructured arm movements made spontaneouslybythemonkeyandmeasuredwithahighresolutionthree-dimensionaltrackingsystem.Weaskedhowmuchofthetotal neuronal variance could be explained by various models of neuronal tuning to movement. On average, tuning to the speed of the hand accountedfor1%ofthetotalvarianceinneuronalactivity,tuningtothedirectionofthehandinspaceaccountedfor8%,amorecomplex modelofdirectiontuning,inwhichthepreferreddirectionoftheneuronrotatedwiththestartingpositionofthearm,accountedfor13%, tuning to the final position of the hand in Cartesian space accounted for 22%, and tuning to the final multijoint posture of the arm accountedfor36%.Oneinterpretationisthatmotorcortexneuronsaresignificantlytunedtomanycontrolparametersimportantinthe animal’srepertoire,butthatdifferentcontrolparametersarerepresentedindifferentproportion,perhapsreflectingtheirprominencein everyday action. The final posture of a movement is an especially prominent control parameter although not the only one. A common mode of action of the monkey arm is to maintain a relatively stable overall posture while making local adjustments in direction during performanceofatask.Onespeculationisthatneuronsinmotorcortexreflectthispatterninwhichdirectiontuningpredominatesinlocal regionsofspaceandposturaltuningpredominatesoverthelargerworkspace.

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

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

[4]  Dylan F. Cooke,et al.  Sensorimotor integration in the precentral gyrus: polysensory neurons and defensive movements. , 2004, Journal of neurophysiology.

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

[6]  A. G. Feldman,et al.  The timing of control signals underlying fast point-to-point arm movements , 2001, Experimental Brain Research.

[7]  Dylan F. Cooke,et al.  Arm movements evoked by electrical stimulation in the motor cortex of monkeys. , 2005, Journal of neurophysiology.

[8]  Wei Wu,et al.  Evidence against a single coordinate system representation in the motor cortex , 2006, Experimental Brain Research.

[9]  Douglas M. Bates,et al.  Nonlinear Regression Analysis and Its Applications , 1988 .

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

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

[12]  Jacob Cohen,et al.  Applied multiple regression/correlation analysis for the behavioral sciences , 1979 .

[13]  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.

[14]  E. Fetz,et al.  Patterns of facilitation and suppression of antagonist forelimb muscles from motor cortex sites in the awake monkey. , 1985, Journal of neurophysiology.

[15]  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.

[16]  Dylan F. Cooke,et al.  Super-Flinchers and Nerves of Steel Defensive Movements Altered by Chemical Manipulation of a Cortical Motor Area , 2004, Neuron.

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

[18]  T. Aflalo,et al.  Partial tuning of motor cortex neurons to final posture in a free-moving paradigm. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Loukia D. Loukopoulos,et al.  Planning reaches by evaluating stored postures. , 1995, Psychological review.

[20]  S. Wise,et al.  Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys , 2004, Experimental Brain Research.

[21]  C. Prablanc,et al.  Postural control of three-dimensional prehension movements. , 1997, Journal of neurophysiology.

[22]  M. Graziano,et al.  Mapping from motor cortex to biceps and triceps altered by elbow angle. , 2004, Journal of neurophysiology.

[23]  S. Scott,et al.  Random change in cortical load representation suggests distinct control of posture and movement , 2005, Nature Neuroscience.

[24]  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.

[25]  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.

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

[27]  John F. Kalaska,et al.  Relations between two-dimensional arm movements and single-cell discharge in motor cortex and area 5: movement direction versus movement end point , 1985 .

[28]  Robert L Sainburg,et al.  Handedness: dominant arm advantages in control of limb dynamics. , 2002, Journal of neurophysiology.

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

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

[31]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[32]  A. Schwartz,et al.  On the relationship between joint angular velocity and motor cortical discharge during reaching. , 2001, Journal of neurophysiology.

[33]  A. G. Feldman.  Once More on the Equilibrium-Point Hypothesis (λ Model) for Motor Control , 1986 .