Abstract
The cerebellum has been hypothesized to provide internal models for limb movement control. If the cerebellum is the site of an inverse dynamics model, then cerebellar neural activity should signal limb dynamics and be coupled to arm muscle activity. To address this, we recorded from 166 task-related Purkinje cells in two monkeys performing circular manual tracking under varying viscous and elastic loads. Hand forces and arm muscle activity increased with the load, and their spatial tuning differed markedly between the viscous and elastic fields. In contrast, the simple spike firing of 91.0% of the Purkinje cells was not significantly modulated by the force nor was their spatial tuning affected. For the 15 cells with a significant force effect, changes were small and isolated. These results do not support the hypothesis that Purkinje cells represent the output of an inverse dynamics model of the arm. Instead these neurons provide a kinematic representation of arm movements.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Miall, R.C., Weir, D.J., Wolpert, D.M. & Stein, J.F. Is the cerebellum a Smith predictor? J. Mot. Behav. 25, 203–216 (1993).
Wolpert, D.M., Miall, R.C. & Kawato, M. Internal models in the cerebellum. Trends Cogn. Sci. 2, 338–347 (1998).
Kawato, M. Internal models for motor control and trajectory planning. Curr. Opin. Neurobiol. 9, 718–727 (1999).
Hollerbach, J.M. & Flash, T. Dynamic interactions between limb segments during planar arm movement. Biol. Cybern. 44, 67–77 (1982).
Shidara, M., Kawano, K., Gomi, H. & Kawato, M. Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365, 50–52 (1993).
Gomi, H. et al. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys I. Simple spikes. J. Neurophysiol. 80, 818–831 (1998).
Schweighofer, N., Arbib, M.A. & Kawato, M. Role of the cerebellum in reaching movements in humans. I. Distributed inverse dynamics control. Eur. J. Neurosci. 10, 86–94 (1998).
Johansson, R.S. & Cole, K.J. Sensory-motor coordination during grasping and manipulative actions. Curr. Opin. Neurobiol. 2, 815–823 (1992).
Flanagan, J. & Wing, A. The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J. Neurosci. 17, 1519–1528 (1997).
Shadmehr, R. & Mussa-Ivaldi, F.A. Adaptive representation of dynamics during learning of a motor task. J. Neurosci. 14, 3208–3224 (1994).
Thoroughman, K.A. & Shadmehr, R. Electromyographic correlates of learning an internal model of reaching movements. J. Neurosci. 19, 8573–8588 (1999).
Thoroughman, K.A. & Shadmehr, R. Learning of action through adaptive combination of motor primitives. Nature 407, 742–747 (2000).
Li, C.S., Padoa-Schioppa, C. & Bizzi, E. Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30, 593–607 (2001).
Gribble, P.L. & Scott, S.H. Overlap of internal models in motor cortex for mechanical loads during reaching. Nature 417, 938–941 (2002).
Padoa-Schioppa, C., Li, C.S. & Bizzi, E. Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron 36, 751–765 (2002).
Xiao, J., Padoa-Schioppa, C. & Bizzi, E. Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey. Exp. Brain Res. 168, 106–119 (2006).
Shadmehr, R. & Holcomb, H.H. Neural correlates of motor memory consolidation. Science 277, 821–825 (1997).
Wolpert, D.M. & Miall, R.C. Forward models for physiological motor control. Neural Netw. 9, 1265–1279 (1996).
Maschke, M., Gomez, C.M., Ebner, T.J. & Konczak, J. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J. Neurophysiol. 91, 230–238 (2004).
Imamizu, H. et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403, 192–195 (2000).
Kawato, M. et al. Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog. Brain Res. 142, 171–188 (2003).
Martin, T.A., Keating, J.G., Goodkin, H.P., Bastian, A.J. & Thach, W.T. Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119, 1183–1198 (1996).
Timmann, D. et al. Visuomotor learning in cerebellar patients. Behav. Brain Res. 81, 99–113 (1996).
Richter, S. et al. Adaptive motor behavior of cerebellar patients during exposure to unfamiliar external forces. J. Mot. Behav. 36, 28–38 (2004).
Ostry, D.J. & Feldman, A.G. A critical evaluation of the force control hypothesis in motor control. Exp. Brain Res. 153, 275–288 (2003).
Roitman, A.V., Pasalar, S., Johnson, M.T. & Ebner, T.J. Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J. Neurosci. 25, 9244–9257 (2005).
Coltz, J.D., Johnson, M.T. & Ebner, T.J. Cerebellar Purkinje cell simple spike discharge encodes movement velocity in primates during visuomotor arm tracking. J. Neurosci. 19, 1782–1803 (1999).
Suh, M., Leung, H.C. & Kettner, R.E. Cerebellar flocculus and ventral paraflocculus Purkinje cell activity during predictive and visually driven pursuit in monkey. J. Neurophysiol. 84, 1835–1850 (2000).
Smith, A.M. & Bourbonnais, D. Neuronal activity in cerebellar cortex related to control of prehensile force. J. Neurophysiol. 45, 286–303 (1981).
Frysinger, R.C., Bourbonnais, D., Kalaska, J.F. & Smith, A.M. Cerebellar cortical activity during antagonist cocontraction and reciprocal inhibition of forearm muscles. J. Neurophysiol. 51, 32–49 (1984).
Mason, C.R., Hendrix, C.M. & Ebner, T.J. Purkinje cells signal hand shape and grasp force during reach-to-grasp in the monkey. J. Neurophysiol. 95, 144–158 (2006).
Fortier, P.A., Kalaska, J.F. & Smith, A.M. Cerebellar neuronal activity related to whole-arm reaching movements in the monkey. J. Neurophysiol. 62, 198–211 (1989).
Fu, Q.G., Flament, D., Coltz, J.D. & Ebner, T.J. Relationship of cerebellar Purkinje cell simple spike discharge to movement kinematics in the monkey. J. Neurophysiol. 78, 478–491 (1997).
Kawato, M., Furukawa, K. & Suzuki, R. A hierarchical neural-network model for control and learning of voluntary movement. Biol. Cybern. 57, 169–185 (1987).
Marple-Horvat, D.E. & Stein, J.F. Neuronal activity in the lateral cerebellum of trained monkeys, related to visual stimuli or to eye movements. J. Physiol. (Lond.) 428, 595–614 (1990).
Norris, S.A., Greger, B., Hathaway, E.N. & Thach, W.T. Purkinje cell spike firing in the posterolateral cerebellum: correlation with visual stimulus, oculomotor response, and error feedback. J. Neurophysiol. 92, 1867–1879 (2004).
Liu, X., Robertson, E. & Miall, R.C. Neuronal activity related to the visual representation of arm movements in the lateral cerebellar cortex. J. Neurophysiol. 89, 1223–1237 (2003).
Evarts, E.V. Relation of pyramidal tract activity to force exerted during voluntary movement. J. Neurophysiol. 31, 14–27 (1968).
Cheney, P.D. & Fetz, E.E. Functional classes of primate corticomotoneuronal cells and their relation to active force. J. Neurophysiol. 44, 773–791 (1980).
Kakei, S., Hoffman, D.S. & Strick, P.L. Muscle and movement representations in the primary motor cortex. Science 285, 2136–2139 (1999).
Thach, W.T. 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, 654–676 (1978).
Monzee, J. & Smith, A.M. Responses of cerebellar interpositus neurons to predictable perturbations applied to an object held in a precision grip. J. Neurophysiol. 91, 1230–1239 (2004).
Schieber, M.H. & Thach, W.T. Trained slow tracking. II. Bidirectional discharge patterns of cerebellar nuclear, motor cortex, and spindle afferent neurons. J. Neurophysiol. 54, 1228–1270 (1985).
Goodkin, H.P. & Thach, W.T. Cerebellar control of constrained and unconstrained movements. II. EMG and nuclear activity. J. Neurophysiol. 89, 896–908 (2003).
Pasalar, S., Roitman, A.V. & Ebner, T.J. Effects of speeds and force fields on submovements during circular manual tracking in humans. Exp. Brain Res. 163, 214–225 (2005).
Batschelet, E. Circular Statistics in Biology (Academic Press, London 1981).
Amirikian, B. & Georgopoulos, A.P. Directional tuning profiles of motor cortical cells. Neurosci. Res. 36, 73–79 (2000).
Acknowledgements
We thank M. McPhee for assistance with graphics and S. Allison for assistance with programming. This work was supported in part by the US National Institutes of Health (grant RO1-NS-18338) and a grant from the Minnesota Medical Foundation.
Author information
Authors and Affiliations
Contributions
S.P. and A.V.R. conducted the experiments and performed the analyses, and also participated in the design of the experiments. All authors contributed to discussions of the data and to writing the paper. T.J.E. was instrumental in the design of the experiments and supervised the project including experimentation, data analysis and writing.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Pasalar, S., Roitman, A., Durfee, W. et al. Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci 9, 1404–1411 (2006). https://doi.org/10.1038/nn1783
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1783
This article is cited by
-
Heterogeneous encoding of temporal stimuli in the cerebellar cortex
Nature Communications (2023)
-
Cerebellar Representations of Errors and Internal Models
The Cerebellum (2022)
-
Mini-review: The Role of the Cerebellum in Visuomotor Adaptation
The Cerebellum (2022)
-
Cerebellar contribution to sensorimotor adaptation deficits in humans with spinal cord injury
Scientific Reports (2021)
-
Seeing motion of controlled object improves grip timing in adults with autism spectrum condition: evidence for use of inverse dynamics in motor control
Experimental Brain Research (2021)