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Independent learning of internal models for kinematic and dynamic control of reaching

Abstract

Psychophysical studies of reaching movements suggest that hand kinematics are learned from errors in extent and direction in an extrinsic coordinate system, whereas dynamics are learned from proprioceptive errors in an intrinsic coordinate system. We examined consolidation and interference to determine if these two forms of learning were independent. Learning and consolidation of two novel transformations, a rotated spatial reference frame and altered intersegmental dynamics, did not interfere with each other and consolidated in parallel. Thus separate kinematic and dynamic models were constructed simultaneously based on errors computed in different coordinate frames, and possibly, in different sensory modalities, using separate working-memory systems. These results suggest that computational approaches to motor learning should include two separate performance errors rather than one.

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Figure 1: Kinematic learning: consolidation and interference.
Figure 2: Dynamic learning is characterized by reduction in direction-dependent errors.
Figure 3: Dynamic learning: consolidation and interference.
Figure 4: Consolidation after consecutive learning of kinematics and dynamics.
Figure 5: Kinematics and dynamics are learned in parallel.

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References

  1. Flanders, M., Helms Tillery, S. I. & Soechting, J. F. Early stages in a sensorimotor transformation. Behav. Brain Sci. 15, 309– 362 (1992).

    Article  Google Scholar 

  2. Desmurget, M., Pelisson, D., Rossetti, Y. & Prablanc, C. From eye to hand: planning goal-directed movements. Neurosci. Biobehav. Rev. 22, 761–788 ( 1998).

    Article  CAS  Google Scholar 

  3. Gordon, J., Ghilardi, M. F. & Ghez, C. Accuracy of planar reaching movements. I. Independence of direction and extent variability. Exp. Brain Res. 99, 97–111 (1994).

    Article  CAS  Google Scholar 

  4. Ghilardi, M. F., Gordon, J. & Ghez, C. Learning a visuomotor transformation in a local area of work space produces directional biases in other areas. J. Neurophysiol. 73, 2535–2539 ( 1995).

    Article  CAS  Google Scholar 

  5. Gordon, J., Ghilardi, M. F., Cooper, S. E. & Ghez, C. Accuracy of planar reaching movements. II. Systematic extent errors resulting from inertial anisotropy. Exp. Brain Res. 99, 112–130 (1994).

    Article  CAS  Google Scholar 

  6. Vindras, P. & Viviani, P. Frames of reference and control parameters in visuomanual pointing. J. Exp. Psychol. 24, 1–23 (1998).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Pine, Z. M., Krakauer, J., Gordon, J. & Ghez, C. Learning of scaling factors and reference axes for reaching movements. Neuroreport 7, 2357–2361 ( 1996).

    Article  CAS  Google Scholar 

  9. Wolpert, D. M., Ghahramani, Z. & Jordan, M. Are arm trajectories planned in kinematic or dynamic coordinates? An adaptation study. Exp Brain. Res. 103 , 460–470 (1995).

    Article  CAS  Google Scholar 

  10. Flanagan, J. R. & Rao, A. K. Trajectory adaptation to a nonlinear visuomotor transformation: evidence of motion planning in visually perceived space. J. Neurophysiol. 74, 2174 –2178 (1995).

    Article  CAS  Google Scholar 

  11. Hollerbach, J. M. & Flash, T. Dynamic interactions between limb segments during planar arm movement. Biol. Cybern. 44, 67–77 ( 1982).

    Article  CAS  Google Scholar 

  12. Hoy, M. G. & Zernicke, R. F. The role of intersegmental dynamics during rapid limb oscillations. J. Biomech. 19, 867–877 (1986).

    Article  CAS  Google Scholar 

  13. Shadmehr, R. & Mussa-Ivaldi, F. A. Adaptive representation of dynamics during learning of a motor task. J. Neurosci. 14, 3208–3224 (1994).

    Article  CAS  Google Scholar 

  14. Sainburg, R. L., Ghez, C. & Kalakanis, D. Intersegmental dynamics are controlled by sequential anticipatory, error correction, and postural mechanisms. J. Neurophysiol. 81, 1045–1056 ( 1999).

    Article  CAS  Google Scholar 

  15. Ghez, C., Gordon, J., Ghilardi, M. F., Christakos, C. N. & Cooper, S. E. Roles of proprioceptive input in the programming of arm trajectories. Cold Spring Harb. Symp. Quant. Biol. 55, 837–847 (1990).

    Article  CAS  Google Scholar 

  16. Gordon, J., Ghilardi, M. F. & Ghez, C. Impairments of reaching movements in patients without proprioception. I. Spatial errors. J. Neurophysiol. (1995).

  17. Sainburg, R. L., Ghilardi, M. F., Poizner, H. & Ghez, C. The control of limb dynamics in normal subjects and patients without proprioception. J. Neurophysiol. 73, 820– 835. (1995).

    Article  CAS  Google Scholar 

  18. Lajoie, Y. et al. Mirror drawing in a deafferented patient and normal subjects: visuoproprioceptive conflict. Neurology 42, 1104–1106 (1992).

    Article  CAS  Google Scholar 

  19. Gandolfo, F., Mussa-Ivaldi, F. A. & Bizzi, E. Motor learning by field approximation. Proc. Natl. Acad. Sci. USA 93, 3843–3846 (1996).

    Article  CAS  Google Scholar 

  20. Ghez, C., Krakauer, J. W., Sainburg, R. & Ghilardi, M. F. in The Cognitive Neurosciences 2nd edn. (ed. Gazzaniga, M.) 501–514 (MIT Press, Cambridge, Massachusetts, in press).

  21. Jordan, M. I. in Handbook of Perception and Action, V. II Motor Skills Vol. 2 (eds. Heuer, H. & Keele, S. W.) 71–118 (Academic, San Diego, 1996).

    Google Scholar 

  22. Shadmehr, R. & Brashers-Krug, T. Functional stages in the formation of human long-term motor memory. J. Neurosci. 17, 409–419 (1997).

    Article  CAS  Google Scholar 

  23. Shadmehr, R. & Holcomb, H. H. Neural correlates of motor memory consolidation. Science 277, 821– 825 (1997).

    Article  CAS  Google Scholar 

  24. Baddeley, A. D. Working Memory (Clarendon, Oxford, 1986).

    Google Scholar 

  25. Baddeley, A. Working memory. Science 255, 556– 559 (1992).

    Article  CAS  Google Scholar 

  26. Wolpert, D. M. & Kawato, M. Multiple paired forward and inverse models for motor control. Neural Net. 11, 1317–1329 (1998).

    Article  CAS  Google Scholar 

  27. Clower, D., Hoffman, J., Votaw, J., Faber, T. & Woods, R. Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 383, 618–621 (1996).

    Article  CAS  Google Scholar 

  28. Moeller, J. R. et al. in Quantitative Functional Brain Imaging with Positron Emission Tomography (eds. Carson, R., Daube-Witherspoon, M. & Herscovitch, P.) 165–172.

  29. Asanuma, H. & Mackel, R. Direct and indirect sensory input pathways to the motor cortex; its structure and function in relation to learning of motor skills. Jpn. J. Physiol. 39, 1– 19 (1989).

    Article  CAS  Google Scholar 

  30. Asanuma, H. Functional role of sensory inputs to the motor cortex. Prog. Neurobiol. 16, 241–262 ( 1981).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Cathleen Song and Thomas Frontera for technical assistance with the experiments and the data analysis and Walton Comer and Hao Huang for computer software. Supported by NS 22713 and NS 01961.

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Correspondence to Claude Ghez.

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Krakauer, J., Ghilardi, MF. & Ghez, C. Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci 2, 1026–1031 (1999). https://doi.org/10.1038/14826

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