Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Direction of action is represented in the ventral premotor cortex

Nature Neuroscience volume 4, pages 1020–1025 (2001)Cite this article

Abstract

The ventral premotor area (PMv) is a major source of input to the primary motor cortex (M1). To examine the potential hierarchical processing between these motor areas, we recorded the activity of PMv neurons in a monkey trained to perform wrist movements in different directions with the wrist in three different postures. The task dissociated three major variables of wrist movement: muscle activity, direction of joint movement and direction of movement in space. Many PMv neurons were directionally tuned. Nearly all of these neurons (61/65, 94%) were 'extrinsic-like'; they seemed to encode the direction of movement in space independent of forearm posture. These results are strikingly different from results from M1 of the same animal, and suggest that intracortical processing between PMv and M1 may contribute to a sensorimotor transformation between extrinsic and intrinsic coordinate frames.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Directionally tuned activity of three neurons in the PMv.
Figure 2: Spatiotemporal maps of extrinsic-like activity in the PMv.
Figure 3: Distribution of neuron types in the PMv and M1.
Figure 4: Preferred directions of neurons and forearm muscles.
Figure 5: Extrinsic-like neurons in the PMv.
Figure 6: Timing contrast between extrinsic-like neurons in the PMv and M1.

Similar content being viewed by others

References

  1. Alexander, G. E. & Crutcher, M. D. Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J. Neurophysiol. 64, 133–150 (1990).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Soechting, J. F. & Flanders, M. Moving in three-dimensional space: frames of reference, vectors and coordinate systems. Annu. Rev. Neurosci. 15, 167–191 (1992).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Matsumura, M. & Kubota, K. Cortical projection of hand-arm motor area from post-arcuate area in macaque monkey: a histological study of retrograde transport of horseradish peroxidase. Neurosci. Lett. 11, 241–246 (1979).

    Article  CAS  Google Scholar 

  6. Muakkassa, K. F. & Strick, P. L. Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized premotor areas. Brain Res. 177, 176–182 (1979).

    Article  CAS  Google Scholar 

  7. Dum, R. P. & Strick, P. L. in Motor Control: Concepts and Issues (eds Humphrey, D.R. & Freund, H.-J.) 383–397 (John Wiley and Sons, New York, 1991).

    Google Scholar 

  8. Kurata, K. Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys. Neurosci. Res. 12, 263–280 (1991).

    Article  CAS  Google Scholar 

  9. Matelli, M., Camarda, R., Glickstein, M. & Rizzolatti, G. Afferent and efferent projections of the inferior area 6 in the macaque monkey. J. Comp. Neurol. 251, 281–298 (1986).

    Article  CAS  Google Scholar 

  10. Lu, M.-T., Preston, J. B. & Strick, P. L. Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J. Comp. Neurol. 341, 375–392 (1994).

    Article  CAS  Google Scholar 

  11. Kubota, K. & Hamada, I. Visual tracking and neuron activity in the post-arcuate area in monkeys. J. Physiol. (Paris) 74, 297–312 (1978).

    CAS  Google Scholar 

  12. Rizzolatti, G., Scandolara, C., Matelli, M. & Gentilucci, M. Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses. Behav. Brain Res. 2, 125–146 (1981).

    Article  CAS  Google Scholar 

  13. Rizzolatti, G., Scandolara, C., Matelli, M. & Gentilucci, M. Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav. Brain Res. 2, 147–163 (1981).

    Article  CAS  Google Scholar 

  14. Fogassi, L. et al. Coding of peripersonal space in inferior premotor cortex (area F4). J. Neurophysiol. 76, 141–157 (1996).

    Article  CAS  Google Scholar 

  15. Graziano, M. S. A., Hu, X. T. & Gross, C. G. Visuospatial properties of ventral premotor cortex. J. Neurophysiol. 77, 2268–2292 (1997).

    Article  CAS  Google Scholar 

  16. Godschalk, M., Lemon, R. N., Nijs, H. G. T. & Kuypers, H. G. J. M. Behaviour of neurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements. Exp. Brain Res. 44, 113–116 (1981).

    Article  CAS  Google Scholar 

  17. Gentilucci, M. et al. Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements. Exp. Brain Res. 71, 475–490 (1988).

    Article  CAS  Google Scholar 

  18. Boussaoud, D. & Wise, S. P. Primate frontal cortex: effects of stimulus and movement. Exp. Brain Res. 95, 28–40 (1993).

    CAS  PubMed  Google Scholar 

  19. Kurata, K. Premotor cortex of monkeys: set- and movement-related activity reflecting amplitude and direction of wrist movements. J. Neurophysiol. 69, 187–200 (1993).

    Article  CAS  Google Scholar 

  20. Moll, L. & Kuypers, H. G. J. M. Premotor cortical ablation in monkeys: contralateral changes in visually guided reaching behavior. Science 198, 317–319 (1977).

    Article  CAS  Google Scholar 

  21. Shen, L. & Alexander, G. E. Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. J. Neurophysiol. 77, 1171–1194 (1997).

    Article  CAS  Google Scholar 

  22. Rizzolatti, G. et al. Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp. Brain Res. 71, 491–507 (1988).

    Article  CAS  Google Scholar 

  23. Rizzolatti, G., Luppino, G. & Matelli, M. The organization of the cortical motor system: new concepts. Electroenceph. Clin. Neurophysiol. 106, 283–296 (1998).

    Article  CAS  Google Scholar 

  24. Fogassi, L. et al. Cortical mechanism for the visual guidance of hand grasping movements in the monkey. A reversible inactivation study. Brain 124, 571–586 (2001).

    Article  CAS  Google Scholar 

  25. Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593–609 (1996).

    Article  Google Scholar 

  26. Luppino, G., Murata, A., Govoni, P. & Matelli, M. Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4). Exp. Brain Res. 128, 181–187 (1999).

    Article  CAS  Google Scholar 

  27. Murata, A. et al. Object representation in the ventral premotor cortex (area F5) of the monkey. J. Neurophysiol. 78, 2226–2230 (1997).

    Article  CAS  Google Scholar 

  28. Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361–365 (2000).

    Article  CAS  Google Scholar 

  29. Hoffman, D. S. & Strick, P. L. Step-tracking movements of the wrist in humans. I. Kinematic analysis. J. Neurosci. 6, 3309–3318 (1986).

    Article  CAS  Google Scholar 

  30. Weinrich, M. & Wise, S. P. The premotor cortex of the monkey. J. Neurosci. 2, 1329–1345 (1982).

    Article  CAS  Google Scholar 

  31. Kurata, K. & Tanji, J. Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements. J. Neurosci. 6, 403–411 (1986).

    Article  CAS  Google Scholar 

  32. Kurata, K. Distribution of neurons with set- and movement-related activity before hand and foot movements in the premotor cortex of rhesus monkeys. Exp. Brain Res. 77, 245–256 (1989).

    Article  CAS  Google Scholar 

  33. Hoffman, D. S. & Strick, P. L. Step-tracking movements of the wrist. IV. Muscle activity associated with movements in different directions. J. Neurophysiol. 81, 319–333 (1999).

    Article  CAS  Google Scholar 

  34. 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 

  35. Schwartz, A. B., Kettner, R. E. & Georgopoulos, A. P. 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, 2913–2927 (1988).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank A.P. Georgopoulos, J.F. Kalaska, S.I. Helms-Tillery and L.E. Sergio for help with the statistical analysis. We thank E. Stappenbeck for care and training of the animal, K. Hughes and M. O'Malley-Davis for technical assistance, and M. Page and W. Hartz for computer program development. This work was supported by funds from the Department of Veterans Affairs, Medical Research Service and Rehabilitation Research and Development Service (P. L. Strick).

Author information

Authors and Affiliations

  1. Research Service, Veterans Affairs Medical Center, University of Pittsburgh School of Medicine, W1640 Biomedical Science Tower, 200 Lothrop Street, Pittsburgh, 15261, Pennsylvania, USA

    Shinji Kakei, Donna S. Hoffman & Peter L. Strick

  2. Department of Neurobiology, University of Pittsburgh School of Medicine, W1640 Biomedical Science Tower, 200 Lothrop Street, Pittsburgh, 15261, Pennsylvania, USA

    Shinji Kakei, Donna S. Hoffman & Peter L. Strick

  3. Department of Psychiatry, University of Pittsburgh School of Medicine, W1640 Biomedical Science Tower, 200 Lothrop Street, Pittsburgh, 15261, Pennsylvania, USA

    Peter L. Strick

  4. Center for the Neural Basis of Cognition, University of Pittsburgh School of Medicine, W1640 Biomedical Science Tower, 200 Lothrop Street, Pittsburgh, 15261, Pennsylvania, USA

    Shinji Kakei, Donna S. Hoffman & Peter L. Strick

Authors
  1. Shinji Kakei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donna S. Hoffman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter L. Strick
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter L. Strick.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kakei, S., Hoffman, D. & Strick, P. Direction of action is represented in the ventral premotor cortex. Nat Neurosci 4, 1020–1025 (2001). https://doi.org/10.1038/nn726

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn726

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing