Experimental Brain Research

, Volume 83, Issue 2, pp 285–302 | Cite as

Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys

  • S. Hocherman
  • S. P. Wise
Article

Summary

Neuronal activity was studied in the primary (M1), supplementary (M2), dorsal premotor (PMd), and ventral premotor (PMv) cortex of awake, behaving rhesus monkeys. The animals performed forelimb movements to three targets, each approached by three different types of trajectories. With one trajectory type, the monkey moved its hand straight to the target, with another, the path curved in a clockwise direction, and with a third, the path curved in a counter-clockwise direction. We examined whether neuronal activity in these areas exclusively reflects a hand movement's net distance and direction or, alternatively, whether other factors also influence cortical activity. It was found that neuronal activity during all phases of a trial reflects aspects of movement in addition to target location. Among these aspects may be selection of an integrated motor act from memory, perhaps specifying the entirety of a path by which the hand moves to a target.

Key words

Cerebral cortex Motor system Motor cortex Premotor cortex Supplementary motor cortex Frontal lobe Movement trajectory Monkey 

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References

  1. Abend W, Bizzi E, Morasso P (1982) Human arm trajectory formation. Brain 105: 331–348Google Scholar
  2. Alexander GE, Crutcher MD (1990) Neural representation of the target (goal) of visually guided arm movements in three motor areas of the monkey. J Neurophysiol 64: 164–178Google Scholar
  3. Amos TM, Vermeersch CH, Park S-K, Ebner, TJ (1988). Principle [sic] component analysis of the responses of premotor cortical neurons to movement in two dimensions. Soc Neurosci Abstr 14: 343Google Scholar
  4. Bucy PC, Fulton JF (1933) Ipsilateral representation in the motor and premotor cortex of monkeys. Brain 56: 318–342Google Scholar
  5. Caminiti R, Johnson PB, Pastore RA, Urbano A (1989) The cortical representation of a coordinate system for the planning and execution of arm movements in space. In: Jeannerod M, Joseph JP (eds) Cortical control of sensory motor integration. Abstr EBBS workshop European Brain and Behavior Society, Lyon, France, p 25Google Scholar
  6. Caminiti R, Johnson PB, Urbano A (1990) Making arm movements within different parts of space: dynamic aspects in the primate motor cortex. J Neurosci 10: 2039–2058Google Scholar
  7. Crammond DJ, Kalaska JF (1989a) Neuronal discharge during an instructed-delay period. II. Premotor area 6. In: Jeannerod M, Joseph JP (eds) Cortical control of sensory-motor integration. Abstr EBBS workshop European Brain and Behavior Society, Lyon, France, p 15Google Scholar
  8. Crammond DJ, Kalaska JF (1989b) Neuronal activity in primate parietal cortex area 5 varies with intended movement direction during an instructed-delay period. Exp Brain Res 76: 458–462Google Scholar
  9. Crammond DJ, Kalaska JF (1989c) Comparison of cell activity in cortical areas 6, 4 and 5 recorded in an instructed delay task. Soc Neurosci Abstr 15: 786Google Scholar
  10. Crutcher MD, Alexander GE (1988) Supplementary motor area (SMA): coding of both preparatory and movement-related neural activity in spatial rather than joint coordinates. Soc Neurosci Abstr 14: 342Google Scholar
  11. Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31: 14–27Google Scholar
  12. Evarts EV (1969) Activity of pyramidal tract neurons during postural fixation. J Neurophysiol 32: 375–385Google Scholar
  13. Fulton JF (1935) Definition of the motor and premotor areas. Brain 58: 311–216Google Scholar
  14. Gentilucci M, Scandolara C, Pigarev IN, Rizzolatti G (1983) Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position. Exp Brain Res 50: 464–468Google Scholar
  15. Georgopoulos AP (1987) Cortical mechanisms subserving reaching. In: Bock G, O'Connor M, Marsh J (eds) Motor areas of the cerebral cortex. Ciba Foundation symposium 132. John Wiley & Sons, Chichester, pp 125–141Google Scholar
  16. Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 11: 1527–1537Google Scholar
  17. Georgopoulos AP, Caminiti R, Kalaska JF, Massey JT (1983) Spatial coding of movement: a hypothesis concerning the coding of movement direction by motor cortical populations. Exp Brain Res Suppl 7: 327–336Google Scholar
  18. Georgopoulos AP, Kalaska JF, Caminiti R (1985) The relations between two dimensional arm movement and single-cell discharge in motor cortex and area 5: movement direction vs. movement end-point. Exp Brain Res Suppl 10: 175–183Google Scholar
  19. Georgopoulos AP, Kettner RE, Schwartz B (1988) Primate motor cortex and.free arm movements to visual targets in threedimensional space. II. Coding of the direction of movement by a neuronal population. J Neurosci 8: 2928–2937Google Scholar
  20. Georgopoulos AP, Crutcher MD, Schwartz AB (1989) Cognitive spatial-motor processes. 3. Motor cortical prediction of movement direction during an instructed delay period. Exp Brain Res 75: 183–194Google Scholar
  21. Godschalk M, Lemon RN, Kuypers HGJM, van der Steen J (1985) The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements. Behav Brain Res 18: 143–157Google Scholar
  22. Hocherman S, Wise SP (1989) Movement trajectory or goal representation in primate premotor and primary motor cortex. Soc Neurosci Abstr 15: 789Google Scholar
  23. Hocherman S, Wise SP (1990) Trajectory-selective neuronal activity in the motor cortex of rhesus monkeys (Macaca mulatto). Behav Neurosci 104: 495–499Google Scholar
  24. Humphrey DR (1986) Representation of movements and muscles within the primate precentral motor cortex: historical and current perspective. Fed Proc 45: 2687–2699Google Scholar
  25. Humphrey DR, Schmidt EM, Thompson WD (1970) Predicting measures of motor performance from multiple cortical spike trains. Science 179: 758–762Google Scholar
  26. Kalaska JF, Cohen DAD, Hyde ML, Prud'homme M (1989) A comparison of movement direction-related versus load directionrelated activity in primate motor cortex, using a two-dimensional reaching task. J Neurosci 9: 2080–2102Google Scholar
  27. Karluk D, Ebner TJ (1989) Spatial representation of movement distance and direction in the premotor cortex. Soc Neurosci Abstr 15: 787Google Scholar
  28. Kurata K (1988) Motor programming in premotor cortex of the monkeys. Abstr Twelfth International Symposium of the Taniguchi Foundation. Toyobo Co, Katata, Ohtsu, Japan, pp 13–14Google Scholar
  29. Kurata K, Wise SP (1988) Premotor cortex of rhesus monkeys: setrelated activity during two conditional motor tasks. Exp Brain Res 69: 327–343Google Scholar
  30. Kwan HC, MacKay WA, Murphy JT, Wong YC (1981) Distribution of responses to visual cues for movement in precentral cortex of awake primates. Neurosci Lett 24: 123–128Google Scholar
  31. Kwan HC, MacKay WA, Murphy JT, Wong YC (1985) Properties of visual cue responses in primate precentral cortex. Brain Res 343: 24–35Google Scholar
  32. Mitz AR, Wise SP, Godschalk M (1989) Learning-dependent activity in premotor cortex of rhesus monkeys. Soc Neurosci Abstr 15: 787Google Scholar
  33. Moll L, Kuypers HGJM (1977) Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior. Science 198: 317–319Google Scholar
  34. Murray GM and Sessle BJ (1989) Coding of tongue movement direction by neurones in tongue region of motor cortex (MI) of awake monkeys (M.fascicularis). Soc Neurosci Abstr 15: 788Google Scholar
  35. Mussa-Ivaldi FA (1988) Do neurons in the motor cortex encode movement direction? An alternative hypothesis. Neurosic Lett 91: 106–111Google Scholar
  36. Passingham RE (1987) Two cortical systems for directing movement. In: Bock G, O'Connor M, Marsh J (eds) Motor areas of the cerebral cortex. Ciba Foundation Symposium 132. John Wiley & Sons, Chichester, pp 151–164Google Scholar
  37. Passingham RE (1988) Premotor cortex and preparation for movement. Exp Brain Res 70: 590–596Google Scholar
  38. Rea GL, Ebner TJ, Bloedel JR (1987). Evaluations of combined premotor and supplementary motor cortex lesions on a visually guided arm movement. Brain Res 418: 58–67Google Scholar
  39. Riehle A, Requin J (1989) Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. J Neurophysiol 61: 534–549Google Scholar
  40. Rizzolatti G, Gentilucci M, Fogassi L, Luppino G, Matelli M, Ponzoni-Maggi S (1987) Neurons related to goal-directed motor acts in inferior area 6 of the macaque monkey. Exp Brain Res 67: 220–224Google Scholar
  41. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res 71: 491–507Google Scholar
  42. Schwartz AB, Anderson BJ (1989) Motor cortical images of sinusoidal trajectories. Soc Neurosci Abstr 15: 788Google Scholar
  43. Schwartz AB, Kettner RE, Georgopoulos AP (1988) Primate motor cortex and free arm movements to visual targets in three-dimensional space. I. Relations between single cell discharge and direction of movement. J Neurosci 8: 2913–2927Google Scholar
  44. Tanji J, Evarts EV (1976) Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J Neurophysiol 39: 1062–1068Google Scholar
  45. Thach WT (1978) 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: 654–676Google Scholar
  46. Traverse J, Latto R (1986) Impairments in route negotiation through a maze after dorsolateral frontal, inferior parietal or premotor lesions in cynomolgus monkeys. Behav Brain Res 20: 203–215Google Scholar
  47. Wannier TMJ, Maier MA, Hepp-Reymond M-C (1989) Responses of motor cortex neurons to visual stimulation in the alert monkey. Neurosic Lett 98: 63–68Google Scholar
  48. Weinrich M, Wise SP (1982) The premotor cortex of the monkey. J Neurosci 2: 1329–1345Google Scholar
  49. Weinrich M, Wise SP, Mauritz K-H (1984) A neurophysiological analysis of the premotor cortex of the monkey. Brain 107: 385–414Google Scholar
  50. Wise SP (1984) Nonprimary motor cortex and its role in the cerebral control of movement. In: Edelman G, Cowan WM, Gall E (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 525–555Google Scholar
  51. Wise SP (1985) The primate premotor cortex: past, present, and preparatory. Ann Rev Neurosci 8: 1–19Google Scholar
  52. Wise SP, Mauritz K-H (1985) Set-related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set. Proc R Soc Lond B 223: 331–354Google Scholar
  53. Woolsey CN, Settlage PH, Meyer DR, Sencer W, Pinto Hamuy T, Travis AM (1952) Patterns of localization in precentral and “supplementary” motor areas and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv Ment Dis 30: 238–264Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • S. Hocherman
    • 1
  • S. P. Wise
    • 1
  1. 1.Laboratory of Neurophysiology, National Institute of Mental HealthPoolesvilleUSA
  2. 2.Department of Physiology, Faculty of MedicineTechnion Israel Institute of TechnologyHaifaIsrael

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