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Direct cortical control of muscle activation in voluntary arm movements: a model

Nature Neuroscience volume 3, pages 391–398 (2000)Cite this article

Abstract

What neural activity in motor cortex represents and how it controls ongoing movement remain unclear. Suggestions that cortex generates low-level muscle control are discredited by correlations with higher-level parameters of hand movement, but no coherent alternative exists. I argue that the view of low-level control is in principle correct, and that seeming contradictions result from overlooking known properties of the motor periphery. Assuming direct motor cortical activation of muscle groups and taking into account the state dependence of muscle-force production and multijoint mechanics, I show that cortical population output must correlate with hand kinematics in quantitative agreement with experimental observations. The model reinterprets the ‘neural population vector’ to afford unified control of posture, movement and force production.

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Figure 1: Mechanistic model of the motor periphery.
Figure 2: Composition of the MI signal, showing the signals for a 10-cm, 500-ms straight movement with a bell-shaped speed profile.
Figure 3: Predicted population vectors.
Figure 4: Effects of curvature on PV direction.
Figure 5: Statistical biases in cell classification.
Figure 6: Effects of kinematic scaling.

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References

  1. Evarts, E. V. in Handbook of Physiology (ed. Brooks, V. B.) 1083– 1120 (Williams and Wilkins, Baltimore, 1981).

    Google Scholar 

  2. Johnson, P. B. in Control of Arm Movement in Space: Neurophysiological and Computational Approaches (eds. Caminiti, R., Johnson, P. B. & Burnod, Y.) (Springer, Berlin, 1992).

    Google Scholar 

  3. Evarts, E. Relation of pyramidal tract activity to force exerted during voluntary movement . J. Neurophysiol. 31, 14– 27 (1968).

    Article  CAS  Google Scholar 

  4. Dum, R. P. & Strick, P. L. The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11, 667–669 (1991).

    Article  CAS  Google Scholar 

  5. Fetz, E. E. & Cheney, P. D. Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J. Neurophysiol. 44, 751–772 ( 1980).

    Article  CAS  Google Scholar 

  6. Georgopoulos, A., Kalaska, J., Caminiti, R. & Massey, J. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J. Neurosci. 2, 1527–1537 (1982).

    Article  CAS  Google Scholar 

  7. Schwartz, A. B. Direct cortical representation of drawing. Science 265, 540–542 (1994).

    Article  CAS  Google Scholar 

  8. Moran, D. W. & Schwartz, A. B. Motor cortical representation of speed and direction during reaching. J. Neurophysiol. 82, 2676–2692 (1999).

    Article  CAS  Google Scholar 

  9. Kalaska, J. F., Cohen, D. A. D., Hyde, M. L. & Prud'homme, M. A comparison of movement direction-related versus load direction-related activity in primate motor cortex, using a two-dimensional reaching task. J. Neurosci. 9, 2080–2102 (1989).

    Article  CAS  Google Scholar 

  10. Sergio, L. E. & Kalaska, J. F. Changes in the temporal pattern of primary motor cortex activity in a directional isometric force versus limb movement task. J. Neurophysiol. 80, 1577 –1583 (1998).

    Article  CAS  Google Scholar 

  11. Kettner, R. E., Schwartz, A. B. & Georgopoulos, A. P. 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. J. Neurosci. 8, 2938–2947 ( 1988).

    Article  CAS  Google Scholar 

  12. Flament, D. & Hore, J. Relations of motor cortex neural discharge to kinematics of passive and active elbow movements in the monkey. J. Neurophysiol. 60, 1268–1284 (1988).

    Article  CAS  Google Scholar 

  13. Thach, W. T. Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of intended next movement in motor cortex and cerebellum. J. Neurophysiol. 41, 654– 676 (1978).

    Article  CAS  Google Scholar 

  14. Alexander, G. E. & Crutcher, M. D. Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. J. Neurophysiol. 64, 164– 178 (1990).

    Article  CAS  Google Scholar 

  15. Fu, Q.-G., Flament, D., Coltz, J. D. & Ebner, T. J. Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J. Neurophysiol. 73, 836–854 (1995).

    Article  CAS  Google Scholar 

  16. Hocherman, S. & Wise, S. P. Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys. Exp. Brain Res. 83, 285–302 ( 1991).

    Article  CAS  Google Scholar 

  17. Humphrey, D. R. & Reed, D. J. in Advances in Neurology: Motor Control Mechanisms in Health and Disease (ed. Desmedt, J. E.) 347–372 (Raven, New York, 1983).

    Google Scholar 

  18. Carpenter, A. F., Georgopoulos, A. P. & Pellizzer, G. Motor cortical encoding of serial order in a context-recall task. Science 283, 1752– 1757 (1999).

    Article  CAS  Google Scholar 

  19. Georgopoulos, A. P., Lurito, J. T., Petrides, M., Schwartz, A. B. & Massey, J. T. Mental rotation of the neuronal population vector. Science 243, 234– 236 (1989).

    Article  CAS  Google Scholar 

  20. Scott, S. & Kalaska, J. Changes in motor cortex activity during reaching movements with similar hand paths but different arm postures . J. Neurophysiol. 73, 2563– 2567 (1995).

    Article  CAS  Google Scholar 

  21. Ashe, J. & Georgopoulos, A. P. Movement parameters and neural activity in motor cortex and Area 5. Cereb. Cortex 6, 590–600 (1994).

    Article  Google Scholar 

  22. Fetz, E. E. Are movement parameters recognizably coded in the activity of single neurons? Behav. Brain Sci. 15, 679– 690 (1992).

    Google Scholar 

  23. Joyce, G. C., Rack, P. M. H. & Westbury, D. R. The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements. J. Physiol. (Lond.) 204, 461–474 ( 1969).

    Article  CAS  Google Scholar 

  24. Zajac, F. E. Muscle and tendon: properties, models, scaling, and application to biomechanics and motor control. Crit. Rev. Biomed. Eng. 17, 359–411 (1989).

    CAS  PubMed  Google Scholar 

  25. Winter, D. A. Biomechanics and Motor Control of Human Movement (Wiley, New York, 1990).

    Google Scholar 

  26. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 ( 1962).

    Article  CAS  Google Scholar 

  27. Crammond, D. J. & Kalaska, J. F. Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task. Exp. Brain Res. 108, 45–61 ( 1996).

    Article  CAS  Google Scholar 

  28. Kalaska, J. F. & Crammond, D. J. Cerebral cortical mechanisms of reaching movements. Science 255, 1517–1523 (1992).

    Article  CAS  Google Scholar 

  29. Kalaska, J. F., Crammond, D. J., Cohen, D. A. D., Prud'homme, M. & Hyde, M. L. in Control of Arm Movement in Space: Neurophysiological and Computational Approaches (eds. Caminiti, R., Johnson, P. B. & Burnod, Y.) (Springer, Berlin, 1992).

    Google Scholar 

  30. Taira, M., Boline, J., Smyrnis, N., Georgopoulos, A. & Ashe, J. On the relations between single cell activity in the motor cortex and the direction and magnitude of three-dimensional static isometric force. Exp. Brain Res. 109, 367– 376 (1996).

    Article  CAS  Google Scholar 

  31. Bennett, D. J., Hollerbach, J. M., Xu, Y. & Hunter, I. W. Time-varying stiffness of human elbow joint during cyclic voluntary movement . Exp. Brain Res. 88, 433– 442 (1992).

    Article  CAS  Google Scholar 

  32. Bullock, D., Cisek, P. & Grossberg, S. Cortical networks for control of voluntary arm movements under variable force conditions. Cereb. Cortex 8, 48–62 (1998).

    Article  CAS  Google Scholar 

  33. Caminiti, R., Johnson, P. & Urbano, A. Making arm movements within different parts of space: dynamic aspects in the primate motor cortex. J. Neurosci. 10, 2039–2058 (1990).

    Article  CAS  Google Scholar 

  34. Scott, S. & Kalaska, J. Reaching movements with similar hand paths but different arm orientation. I. Activity of individual cells in motor cortex. J. Neurophysiol. 77, 826 –852 (1997).

    Article  CAS  Google Scholar 

  35. Tanaka, S. Hypothetical joint-related coordinate systems in which populations of motor cortical neurons code direction of voluntary arm movements. Neurosci. Lett. 180, 83–86 ( 1994).

    Article  CAS  Google Scholar 

  36. Kakei, S., Hoffman, D. & Strick, P. Muscle and movement representations in the primary motor cortex. Science 285, 2136– 2139 (1999).

    Article  CAS  Google Scholar 

  37. Fetz, E. E., Cheney, P. D., Mewes, K. & Palmer, S. Control of forelimb muscle activity by populations of corticomotoneuronal and rubromotoneuronal cells. Prog. Brain Res. 80, 437– 449 (1989).

    Article  CAS  Google Scholar 

  38. Miller, L. E. & Sinkjaer, T. Primate red nucleus discharge encodes the dynamics of limb muscle activity. J. Neurophysiol. 80, 59–70 (1998).

    Article  CAS  Google Scholar 

  39. Gottlieb, G. L. On the voluntary movement of compliant (inertial-viscoelastic) loads by parcellated control mechanisms. J. Neurophysiol. 76, 3207–3228 (1996).

    Article  CAS  Google Scholar 

  40. Khatib, O. A unified approach to motion and force control of robotic manipulators: the operational space formulation. IEEE J. Robotics Automat. RA-3, 43–53 (1987).

    Article  Google Scholar 

  41. Scott, S. H. Comparison of onset time and magnitude of activity for proximal arm muscles and motor cortical cells before reaching movements. J. Neurophysiol. 77, 1016–1022 ( 1997).

    Article  CAS  Google Scholar 

  42. Bizzi, E., Mussa-Ivaldi, F. A. & Giszter, S. F. Computations underlying the execution of movement: a biological perspective. Science 253, 287 –291 (1991).

    Article  CAS  Google Scholar 

  43. Galagan, J. Spinal Mechanisms of Motor Control. Thesis, MIT (1999 ).

  44. Tsuji, T., Morasso, P. G., Goto, K. & Ito, K. Human hand impedance characteristics during maintained posture. Biol. Cybern. 72, 475–485 (1995).

    Article  CAS  Google Scholar 

  45. Gomi, H. & Kawato, M. Equilibrium-point control hypothesis examined by measured arm stiffness during multijoint movement. Nature 272, 117–120 ( 1996).

    CAS  Google Scholar 

  46. Wolpert, D., Gharahmani, Z. & Jordan, M. An internal model for sensorimotor integration. Science 269, 1880–1882 ( 1995).

    Article  CAS  Google Scholar 

  47. Mussa-Ivaldi, F. A. Do neurons in the motor cortex encode movement direction? An alternative hypothesis . Neurosci. Lett. 91, 106– 111 (1988).

    Article  CAS  Google Scholar 

  48. Schmidt, R. A., Zelaznik, H., Hawkins, B., Frank, J. S. & Quinn, J. T. J. Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol. Rev. 86, 415–451 (1979).

    Article  Google Scholar 

  49. Sanes, J. N. & Shadmehr, R. Sense of muscular effort and somatesthetic afferent information in humans. Can. J. Physiol. Pharmacol. 73, 223–233 (1995).

    Article  CAS  Google Scholar 

  50. Fu, Q.-G., Suarez, J. & Ebner, T. Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. J. Neurophysiol. 70, 2097–2116 (1993).

    Article  CAS  Google Scholar 

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Acknowledgements

I thank Zoubin Ghahramani and Stephen Scott for their suggestions.

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  1. Gatsby Computational Neuroscience Unit, University College London, 17 Queen Square, London, WC1N 3 AR, UK

    Emanuel Todorov

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Correspondence to Emanuel Todorov.

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Todorov, E. Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci 3, 391–398 (2000). https://doi.org/10.1038/73964

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