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Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements

Abstract

Rhythmic bimanual movements are highly constrained in the temporal domain, with the gestures of the two hands tightly synchronized. Previous studies have implicated a subcortical locus for temporal coupling based on the observation that these constraints persist in callosotomy patients. We now report that such coupling is restricted to movements entailing a discrete event (such as a movement onset). Three callosotomy patients exhibited a striking lack of temporal coupling during continuous movements, with the two hands oscillating at non-identical frequencies. We propose a subcortical locus of temporal coupling for movements involving discrete events. In contrast, synchronization between the hands during continuous movements depends on interhemispheric transmission across the corpus callosum.

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Figure 1: Temporal uncoupling during a single trial of symmetric, maximum rate circling in a patient.
Figure 2: Callosotomy patients exhibit a large difference in cycling rate between the two hands.
Figure 3: Increase in instability during asymmetric circling at maximum rate is only found in performance of control participants.
Figure 4: Increased dispersion of relative phase in a patient.
Figure 5: Summary of relative phase variability for controls and callosotomy patients.
Figure 6: Dissociation of temporal coupling during continuous and discrete movements in a modified tapping experiment.

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References

  1. Kelso, J. S., Southard, D. L. & Goodman, D. On the coordination of two-handed movements. J. Exp. Psychol. Hum. Percept. Perform. 5, 229–238 (1979).

    Article  CAS  Google Scholar 

  2. Marteniuk, R. G., MacKenzie, C. L. & Baba, D. M. Bimanual movement control: information processing and interaction effects. Q. J. Exp. Psychol. A. 36, 335–365 (1984).

    Article  Google Scholar 

  3. Kelso, S. J. A., Putnam, C. A. & Goodman, D. On the space-time structure of human interlimb co-ordination. Q. J. Exp. Psychol. A. 35, 347–375 (1983).

    Article  CAS  Google Scholar 

  4. Franz, E. A. Spatial coupling in the coordination of complex actions. Q. J. Exp. Psychol. A. 50, 684–704 (1997).

    Article  CAS  Google Scholar 

  5. Franz, E. A., Zelaznik, H. N. & McCabe, G. Spatial topological constraints in a bimanual task. Acta Psychol. 77, 137–151 (1991).

    Article  CAS  Google Scholar 

  6. Franz, E. A., Eliassen, J. C., Ivry, R. B. & Gazzaniga, M. S. Dissociation of spatial and temporal coupling in the bimanual movements of callosotomy patients. Psychol. Sci. 7, 306–310 (1996).

    Article  Google Scholar 

  7. Eliassen, J. C., Baynes, K. & Gazzaniga, M. S. Direction information coordinated via the posterior third of the corpus callosum during bimanual movements. Exp. Brain. Res. 128, 573–577 (1999).

    Article  CAS  Google Scholar 

  8. Ivry, R. B. & Hazeltine, E. Subcortical locus of temporal coupling in the bimanual movements of a callosotomy patient. Hum. Mov. Sci. 18, 345–375 (1999).

    Article  Google Scholar 

  9. Preilowski, B. F. Possible contribution of the anterior forebrain commissures to bilateral motor coordination. Neuropsychologia 10, 267–277 (1972).

    Article  CAS  Google Scholar 

  10. Tuller, B. & Kelso, J. A. Environmentally specified patterns of movement coordination in normal and split-brain subjects. Exp. Brain. Res. 75, 306–316 (1989).

    Article  CAS  Google Scholar 

  11. Zaidel, D. & Sperry, R. W. Some long-term motor effects of cerebral commissurotomy in man. Neuropsychologia 15, 193–204 (1977).

    Article  CAS  Google Scholar 

  12. Robertson, S. D. et al. Correlations for timing consistency among tapping and drawing tasks: evidence against a single timing process for motor control. J. Exp. Psychol. Hum. Percept. Perform. 25, 1316–1330 (1999).

    Article  CAS  Google Scholar 

  13. Carson, R. G., Thomas, J., Summers, J. J., Walters, M. R. & Semjen, A. The dynamics of bimanual circle drawing. Q. J. Exp. Psychol. A. 50, 664–683 (1997).

    Article  CAS  Google Scholar 

  14. Semjen, A., Summers, J. J. & Cattaert, D. Hand coordination in bimanual circle drawing. J. Exp. Psychol. Hum. Percept. Perform. 21, 1139–1157 (1995).

    Article  Google Scholar 

  15. Kelso, J. A. S. Dynamic Patterns: the Self-organization of Brain and Behaviour (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  16. Cattaert, D., Semjen, A. & Summers, J. J. Simulating a neural cross-talk model for between-hand interference during bimanual circle-drawing. Biol. Cybern. 81, 343–358 (1999).

    Article  CAS  Google Scholar 

  17. Georgopoulos, A. P., Schwartz, A. B. & Kettner, R. E. Neuronal population coding of movement direction. Science 233, 1416–1419 (1986).

    Article  CAS  Google Scholar 

  18. Hollerbach, J. M. An oscillation theory of handwriting. Biol. Cybern. 42, 139–156 (1981).

    Article  Google Scholar 

  19. Ivry, R. B., Franz, E. A., Kingstone, A. & Johnston, J. C. The psychological refractory period effect following callosotomy: uncoupling of lateralized response codes. J. Exp. Psychol. Hum. Percept. Perform. 24, 463–480 (1998).

    Article  CAS  Google Scholar 

  20. 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 

  21. 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 

  22. Porter, R. & Lemon, R. Corticospinal Function and Voluntary Movement (Oxford Univ. Press, 1993).

    Google Scholar 

  23. Serrien, D. J., Nirkko, A. C., Lovblad, K. O. & Wiesendanger, M. Damage to the parietal lobe impairs bimanual coordination. Neuroreport 12, 2721–2724 (2001).

    Article  CAS  Google Scholar 

  24. Eliassen, J. C., Baynes, K. & Gazzaniga, M. S. Anterior and posterior callosal contributions to simulataneous bimanual movements of the hand and fingers. Brain 123, 2501–2511 (2000).

    Article  Google Scholar 

  25. Zelaznik, H. N., Spencer, R. M. & Doffin, J. G. Temporal precision in tapping and circle drawing movements at preferred rates is not correlated: further evidence against timing as a general-purpose ability. J. Motor Behav. 32, 193–199 (2000).

    Article  CAS  Google Scholar 

  26. Bullock, D. & Grossberg, S. Neural dynamics of planned arm movements: emergent invariants and speed-accuracy properties during trajectory formation. Psychol. Rev. 95, 49–90 (1988).

    Article  CAS  Google Scholar 

  27. Ivry, R. B. & Richardson, T. Temporal control and coordination: the multiple timer model. Brain Cogn. (in press).

  28. Verschueren, S. M., Swinnen, S. P., Cordo, P. J. & Dounskaia, N. V. Proprioceptive control of multijoint movement: bimanual circle drawing. Exp. Brain. Res. 127, 182–192 (1999).

    Article  CAS  Google Scholar 

  29. Sidtis, J. J., Volpe, B. T., Wilson, D. H., Rayport, M. & Gazzaniga, M. S. Variability in right hemisphere language function after callosal section: evidence for a continuum of generative capacity. J. Neurosci. 1, 323–331 (1981).

    Article  CAS  Google Scholar 

  30. Gazzaniga, M. S., Holtzman, J. D., Deck, M. D. & Lee, B. C. MRI assessment of human callosal surgery with neuropsychological correlates. Neurology 35, 1763–1766 (1985).

    Article  CAS  Google Scholar 

  31. Corballis, P. M., Inati, S., Funnell, M. G., Grafton, S. T. & Gazzaniga, M. S. MRI assessment of spared fibers following callosotomy: a second look. Neurology 57, 1345–1346 (2001).

    Article  CAS  Google Scholar 

  32. Fisher, N. I. Statistical Analysis of Circular Data (Cambridge Univ. Press, 1993).

    Book  Google Scholar 

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Acknowledgements

This work was supported by NIH grants P50 NS17778 and R01 NS30256. The authors are grateful to Noam Sobel, Bekki Spencer and Howard Zelaznik for their comments on this manuscript and to Paul Corballis for his assistance with the data collection.

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Correspondence to Richard B. Ivry.

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Kennerley, S., Diedrichsen, J., Hazeltine, E. et al. Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements. Nat Neurosci 5, 376–381 (2002). https://doi.org/10.1038/nn822

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