Cue to action processing in motor cortex populations.

The primary motor cortex (MI) commands motor output after kinematics are planned from goals, thought to occur in a larger premotor network. However, there is a growing body of evidence that MI is involved in processes beyond action generation, and neuronal subpopulations may perform computations related to cue-to-action processing. From multielectrode array recordings in awake behaving Macaca mulatta monkeys, our results suggest that early MI ensemble activity during goal-directed reaches is driven by target information when cues are closely linked in time to action. Single-neuron activity spanned cue presentation to movement, with the earliest responses temporally aligned to cue and the later responses better aligned to arm movements. Population decoding revealed that MI's coding of cue direction evolved temporally, likely going from cue to action generation. We confirmed that a portion of MI activity is related to visual target processing by showing changes in MI activity related to the extinguishing of a continuously pursued visual target. These findings support a view that MI is an integral part of a cue-to-action network for immediate responses to environmental stimuli.

[1]  E. Fetz,et al.  Direct control of paralyzed muscles by cortical neurons , 2008, Nature.

[2]  K. Shenoy,et al.  Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. , 2007, Journal of neurophysiology.

[3]  Webster West,et al.  Continuous-time estimation of A change-point in a poisson process , 1997 .

[4]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Marie-Claude Hepp-Reymond,et al.  Responses of motor cortex neurons to visual stimulation in the alert monkey , 1989, Neuroscience Letters.

[6]  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.

[7]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

[8]  Dennis C. Tkach,et al.  Observation-based learning for brain–machine interfaces , 2008, Current Opinion in Neurobiology.

[9]  John P. Donoghue,et al.  Automated spike sorting using density grid contour clustering and subtractive waveform decomposition , 2007, Journal of Neuroscience Methods.

[10]  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.

[11]  J. Tanji,et al.  Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. , 1976, Journal of neurophysiology.

[12]  Dennis C. Tkach,et al.  Congruent Activity during Action and Action Observation in Motor Cortex , 2007, The Journal of Neuroscience.

[13]  Nicholas Hatsopoulos,et al.  Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. , 2004, Journal of neurophysiology.

[14]  J. Ashe.  Erratum to “Force and the motor cortex” [Behavioural Brain Research 86 (1997) 1–15] 1 PII of original article: S0166-4328(96)00145-3 1 , 1997, Behavioural Brain Research.

[15]  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.

[16]  E. Garcia-Rill,et al.  Responses of motor cortex cells to visual stimuli. , 1974, Brain research.

[17]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[18]  Richard A Andersen,et al.  Decoding Trajectories from Posterior Parietal Cortex Ensembles , 2008, The Journal of Neuroscience.

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

[20]  J. Tanji,et al.  Gating of motor cortex reflexes by prior instruction. , 1974, Brain research.

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

[22]  Arne D. Ekstrom,et al.  Single-Neuron Responses in Humans during Execution and Observation of Actions , 2010, Current Biology.

[23]  A P Georgopoulos,et al.  Effects of optic flow in motor cortex and area 7a. , 2001, Journal of neurophysiology.

[24]  M. M. Morrow,et al.  Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. , 2003, Journal of neurophysiology.

[25]  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.

[26]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[27]  Y. Amit,et al.  Encoding of Movement Fragments in the Motor Cortex , 2007, The Journal of Neuroscience.

[28]  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.

[29]  Y. Lamarre,et al.  Fast ballistic arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. I. Activity of precentral cortical neurons. , 1983, Journal of neurophysiology.

[30]  R. Andersen,et al.  The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements , 2006, Neuropsychologia.

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

[32]  E. Evarts,et al.  Transcortical reflexes and servo control of movement. , 1981, Canadian journal of physiology and pharmacology.

[33]  Roger Salamon,et al.  A statistical method for the estimation of neuronal response latency and its functional interpretation , 1983, Brain Research.

[34]  Gisbert Schneider,et al.  Support vector machine applications in bioinformatics. , 2003, Applied bioinformatics.

[35]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

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

[37]  Yali Amit,et al.  Single-unit stability using chronically implanted multielectrode arrays. , 2009, Journal of neurophysiology.

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

[39]  A. Georgopoulos,et al.  Cognitive neurophysiology of the motor cortex. , 1993, Science.

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

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

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

[43]  Steven P. Wise,et al.  Motor Cortex , 2013 .

[44]  J. Tanji,et al.  Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. , 1976, Journal of neurophysiology.

[45]  Michael J. Black,et al.  Decoding Complete Reach and Grasp Actions from Local Primary Motor Cortex Populations , 2010, The Journal of Neuroscience.

[46]  Byron M. Yu,et al.  Extracting Dynamical Structure Embedded in Neural Activity , 2005, NIPS.

[47]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

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

[49]  Gopal Santhanam,et al.  Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. , 2006, Journal of neurophysiology.

[50]  J. Ashe.  Force and the motor cortex , 1997, Behavioural Brain Research.

[51]  Masato Taira,et al.  Motor cortical activity preceding a memorized movement trajectory with an orthogonal bend , 1993, Experimental Brain Research.

[52]  N. Hatsopoulos,et al.  Sensing with the Motor Cortex , 2011, Neuron.

[53]  Juliana Dushanova,et al.  Neurons in primary motor cortex engaged during action observation , 2010, The European journal of neuroscience.

[54]  Stephen H. Scott,et al.  Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching , 1999, Journal of Neuroscience Methods.

[55]  J. Kalaska,et al.  Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task , 1996, Experimental Brain Research.

[56]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[57]  S. Scott.  The role of primary motor cortex in goal-directed movements: insights from neurophysiological studies on non-human primates , 2003, Current Opinion in Neurobiology.

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

[59]  E Salinas,et al.  Conversion of Sensory Signals into Motor Commands in Primary Motor Cortex , 1998, The Journal of Neuroscience.

[60]  J. Kalaska,et al.  Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. , 2000, Journal of neurophysiology.

[61]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[62]  R Shadmehr,et al.  Electromyographic Correlates of Learning an Internal Model of Reaching Movements , 1999, The Journal of Neuroscience.

[63]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.