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Rhythmic arm movement is not discrete

Nature Neuroscience volume 7, pages 1136–1143 (2004)Cite this article

An Erratum to this article was published on 01 November 2004

Abstract

Rhythmic movements, such as walking, chewing or scratching, are phylogenetically old motor behaviors found in many organisms, ranging from insects to primates. In contrast, discrete movements, such as reaching, grasping or kicking, are behaviors that have reached sophistication primarily in younger species, particularly primates. Neurophysiological and computational research on arm motor control has focused almost exclusively on discrete movements, essentially assuming similar neural circuitry for rhythmic tasks. In contrast, many behavioral studies have focused on rhythmic models, subsuming discrete movement as a special case. Here, using a human functional neuroimaging experiment, we show that in addition to areas activated in rhythmic movement, discrete movement involves several higher cortical planning areas, even when both movement conditions are confined to the same single wrist joint. These results provide neuroscientific evidence that rhythmic arm movement cannot be part of a more general discrete movement system and may require separate neurophysiological and theoretical treatment.

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Figure 1: Experimental setup and conditions.
Figure 2: Summary of brain activity in Experiment 1, superimposed on a Montreal Neurological Institute (MNI) coordinates normalized T1 brain template, included in the SPM software distribution.
Figure 3: Summary of brain activations of Experiment 2.

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References

  1. Marder, E. Motor pattern generation. Curr. Opin. Neurobiol. 10, 691–698. (2000).

    Article  CAS  Google Scholar 

  2. Lamb, T. & Yang, J.F. Could different directions of infant stepping be controlled by the same locomotor central pattern generator? J. Neurophysiol. 83, 2814–2824. (2000).

    Article  CAS  Google Scholar 

  3. Pinter, M.M. & Dimitrijevic, M.R. Gait after spinal cord injury and the central pattern generator for locomotion. Spinal Cord 37, 531–537 (1999).

    Article  CAS  Google Scholar 

  4. Dimitrijevic, M.R., Gerasimenko, Y. & Pinter, M.M. Evidence for a spinal central pattern generator in humans. Ann. N. Y. Acad. Sci. 860, 360–376 (1998).

    Article  CAS  Google Scholar 

  5. Kelso, J.A.S. Dynamic Patterns: The Self-Organization of Brain and Behavior (MIT Press, Cambridge, Massachusetts, USA, 1995).

    Google Scholar 

  6. Turvey, M.T. Coordination. Am. Psychol. 45, 938–953 (1990).

    Article  CAS  Google Scholar 

  7. Kugler, P.N. & Turvey, M.T. Information, Natural Law, and the Self-Assembly of Rhythmic Movement (Erlbaum, Hillsdale, New Jersey, USA, 1987).

    Google Scholar 

  8. Andersen, R.A., Snyder, L.H., Bradley, D.C. & Xing, J. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20, 303–330 (1997).

    Article  CAS  Google Scholar 

  9. Kalaska, J.F., Scott, S.H., Cisek, P. & Sergio, L.E. Cortical control of reaching movements. Curr. Opin. Neurobiol. 7, 849–859 (1997).

    Article  CAS  Google Scholar 

  10. Sabes, P.N. The planning and control of reaching movements. Curr. Opin. Neurobiol. 10, 740–746 (2000).

    Article  CAS  Google Scholar 

  11. Flash, T. & Sejnowski, T. Computational approaches to motor control. Curr. Opin. Neurobiol. 11, 655–662 (2001).

    Article  CAS  Google Scholar 

  12. Morasso, P. Spatial control of arm movements. Exp. Brain Res. 42, 223–227 (1981).

    Article  CAS  Google Scholar 

  13. Abend, W., Bizzi, E. & Morasso, P. Human arm trajectory formation. Brain 105, 331–348 (1982).

    Article  CAS  Google Scholar 

  14. Flash, T. & Hogan, N. The coordination of arm movements: An experimentally confirmed mathematical model. J. Neurosci. 5, 1688–1703 (1985).

    Article  CAS  Google Scholar 

  15. Uno, Y., Kawato, M. & Suzuki, R. Formation and control of optimal trajectory in human multijoint arm movement — Minimum torque-change model. Biol. Cybern. 61, 89–101 (1989).

    Article  CAS  Google Scholar 

  16. Kawato, M. Internal models for motor control and trajectory planning. Curr. Opin. Neurobiol. 9, 718–727 (1999).

    Article  CAS  Google Scholar 

  17. Feldman, A.G. Superposition of motor programs. I. Rhythmic forearm movements in man. Neuroscience 5, 81–90 (1980).

    Article  CAS  Google Scholar 

  18. Latash, M.L. Control of Human Movement (Human Kinetics, Champaign, Illinois, USA, 1993).

    Google Scholar 

  19. Soechting, J.F. & Terzuolo, C.A. Organization of arm movements in three dimensional space. Wrist motion is piecewise planar. Neuroscience 23, 53–61 (1987).

    Article  CAS  Google Scholar 

  20. Sternad, D. & Schaal, D. Segmentation of endpoint trajectories does not imply segmented control. Exp. Brain Res. 124, 118–136 (1999).

    Article  CAS  Google Scholar 

  21. Schaal, S. & Sternad, D. Origins and violations of the 2/3 power law in rhythmic 3D movements. Exp. Brain Res. 136, 60–72 (2001).

    Article  CAS  Google Scholar 

  22. Richardson, M.J. & Flash, T. Comparing smooth arm movements with the two-thirds power law and the related segmented-control hypothesis. J. Neurosci. 22, 8201–8211 (2002).

    Article  CAS  Google Scholar 

  23. Sternad, D., Dean, W.J. & Schaal, S. Interaction of rhythmic and discrete pattern generators in single joint movements. Hum. Mov. Sci. 19, 627–665 (2000).

    Article  Google Scholar 

  24. Sternad, D., De Rugy, A., Pataky, T. & Dean, W.J. Interaction of discrete and rhythmic movements over a wide range of periods. Exp. Brain Res. 147, 162–174 (2002).

    Article  Google Scholar 

  25. Wei, K., Wertman, G. & Sternad, D. Interactions between rhythmic and discrete components in a bimanual task. Motor Control 7, 134–155 (2003).

    Article  Google Scholar 

  26. Smits-Engelsman, B.C., Van Galen, G.P. & Duysens, J. The breakdown of Fitts' law in rapid, reciprocal aiming movements. Exp. Brain Res. 145, 222–230 (2002).

    Article  CAS  Google Scholar 

  27. Ijspeert, A., Nakanishi, J. & Schaal, S. in Advances in Neural Information Processing Systems 15 (eds. Becker, S., Thrun, S. & Obermayer, K.) 1547–1554 (MIT Press, Cambridge, Massachusetts, USA, 2003).

    Google Scholar 

  28. de Rugy, A. & Sternad, D. Interaction between discrete and rhythmic movements: reaction time and phase of discrete movement initiation during oscillatory movements. Brain Res. 994, 160–174 (2003).

    Article  CAS  Google Scholar 

  29. Sternad, D. & Dean, W.J. Rhythmic and discrete elements in multi-joint coordination. Brain Res. 989, 152–171 (2003).

    Article  CAS  Google Scholar 

  30. Picard, N. & Strick, P.L. Imaging the premotor areas. Curr. Opin. Neurobiol. 11, 663–672 (2001).

    Article  CAS  Google Scholar 

  31. Seitz, R.J., Stephan, K.M. & Binkofski, F. Control of action as mediated by the human frontal lobe. Exp. Brain Res. 133, 71–80 (2000).

    Article  CAS  Google Scholar 

  32. Gordon, A.M., Lee, J.H., Flament, D., Ugurbil, K. & Ebner, T.J. Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements. Exp. Brain Res. 121, 153–166 (1998).

    Article  CAS  Google Scholar 

  33. Debaere, F. et al. Brain areas involved in interlimb coordination: a distributed network. Neuroimage 14, 947–958 (2001).

    Article  CAS  Google Scholar 

  34. Rizzolatti, G. & Arbib, M.A. Language within our grasp. Trends Neurosci. 21, 188–194 (1998).

    Article  CAS  Google Scholar 

  35. Kertzman, C., Schwarz, U., Zeffiro, T.A. & Hallett, M. The role of posterior parietal cortex in visually guided reaching movements in humans. Exp. Brain Res. 114, 170–183 (1997).

    Article  CAS  Google Scholar 

  36. Grafton, S.T., Fagg, A.H., Woods, R.P. & Arbib, M.A. Functional anatomy of pointing and grasping in humans. Cereb. Cortex 6, 226–237 (1996).

    Article  CAS  Google Scholar 

  37. Fink, G.R., Frackowiak, R.S., Pietrzyk, U. & Passingham, R.E. Multiple nonprimary motor areas in the human cortex. J. Neurophysiol. 77, 2164–2174 (1997).

    Article  CAS  Google Scholar 

  38. Deiber, M.P., Honda, M., Ibanez, V., Sadato, N. & Hallett, M. Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. J. Neurophysiol. 81, 3065–3077 (1999).

    Article  CAS  Google Scholar 

  39. Thickbroom, G.W. et al. Differences in functional magnetic resonance imaging of sensorimotor cortex during static and dynamic finger flexion. Exp. Brain Res. 126, 431–438 (1999).

    Article  CAS  Google Scholar 

  40. Lewis, P.A. & Miall, R.C. Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr. Opin. Neurobiol. 13, 250–255 (2003).

    Article  CAS  Google Scholar 

  41. Brown, T.G. On the nature of the fundamental activity of the nervous centres; together with an analysis of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J. Physiol. (Lond.) 48, 18–46 (1914).

    Article  CAS  Google Scholar 

  42. Turner, R., Howseman, A., Rees, G.E., Josephs, O. & Friston, K. Functional magnetic resonance imaging of the human brain: data acquisition and analysis. Exp. Brain Res. 123, 5–12 (1998).

    Article  CAS  Google Scholar 

  43. Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging (Thieme, Stuttgard, Germany, 1988).

    Google Scholar 

  44. Brett, M., Christiff, K., Cusack, R. & Lancaster, J. Using the Talairach atlas with the MNI template. Neuroimage 13, S85 (2001).

    Article  Google Scholar 

  45. Friston, K.J., Frith, C.D., Liddle, P.F. & Frackowiak, R.S.J. Comparing functional (PET) images: the assessment of significant change. J. Cereb. Blood Flow Metab. 11, 690–699 (1991).

    Article  CAS  Google Scholar 

  46. Brett, M., Anton, J.-L., Valabregue, R. & Poline, J.-B. in 8th International Conference on Funcational Mapping of the Human Brain (Sendai, Japan, 2002).

    Google Scholar 

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Acknowledgements

This research was supported in part by US National Science Foundation grants ECS-0325383, IIS-0312802, IIS-0082995, ECS-0326095 and ANI-0224419, the ERATO Kawato Dynamic Brain Project funded by the Japanese Science and Technology Agency, and the National Institute of Information and Communications Technology (NICT).

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Authors and Affiliations

  1. Computer Science and Neuroscience, University of Southern California, Los Angeles, 90089-2520, California, USA

    Stefan Schaal

  2. Department of Kinesiology, Pennsylvania State University, 266 Rec. Hall, University Park, Pennsylvania, 16802, USA

    Dagmar Sternad

  3. ATR Computational Neuroscience Laboratories, 2-2-2 Hikaridai, Seika-cho, Soraku-gun, Kyoto, 619-0288, Japan

    Stefan Schaal, Rieko Osu & Mitsuo Kawato

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  1. Stefan Schaal
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Correspondence to Stefan Schaal.

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Schaal, S., Sternad, D., Osu, R. et al. Rhythmic arm movement is not discrete. Nat Neurosci 7, 1136–1143 (2004). https://doi.org/10.1038/nn1322

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