Nature Neuroscience
- 9, 1364 - 1366 (2006)
Published online: 8 October 2006; | doi:10.1038/nn1785
Limited transfer of learning between unimanual and bimanual skills within the same limbDaichi Nozaki1, 2, 3, Isaac Kurtzer1 & Stephen H Scott11 Centre for Neuroscience Studies, Department of Anatomy and Cell Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada. 2 Department of Rehabilitation for Movement Functions, Research Institute of National Rehabilitation Center for Persons with Disabilities, Tokorozawa, Saitama 359-8555, Japan. 3 Present address: Graduate School of Education, University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan.
Correspondence should be addressed to Daichi Nozaki nozaki@p.u-tokyo.ac.jp or Stephen H Scott steve@biomed.queensu.ca Although a limb's motion appears to be similar across unimanual and bimanual movements, here we demonstrate partial, but not complete, transfer of learning across these behavioral contexts, hidden learning that remains intact (but invisible) until the original context is again encountered, and the ability to associate two conflicting force fields simultaneously, one with each context. These results suggest partial, but not complete, overlap in the learning processes involved in the acquisition of unimanual and bimanual skills.
A common form of sports training is to break down a complex whole-body skill into isolated training of the skill's components. For example, swimmers will alternately swim lengths of a pool using one arm while the other arm is maintained straight in front1. This training approach assumes that motor skills learned from one context (unimanual practice) will transfer to subsequent performance in another context (bimanual performance). Here we address the efficacy of learning across these behavioral contexts.
We trained right-handed human subjects to reach with their left arm against an unfamiliar force field delivered by a bilateral robot (Fig. 1 and ref. 2, KINARM, BKIN Technologies; details in Supplementary Methods and Supplementary Fig. 1 online). All experiments were approved by the Queen's University Human Ethics Committee. Consistent with previous studies3,
4, the applied force led to substantial rightward deviations on the initial reach, followed by a return to near-baseline movement patterns within 40 trials (Fig. 1b,c). We then tested motor adaptation by removing the force field (that is, in 'catch trials') and observing any leftward deviations of the arm (that is, 'aftereffects'). The aftereffect's magnitude indicates the degree of motor learning3,
4 and can be compared between unimanual and bimanual trials.
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Aftereffects of the same arm were significantly smaller for bimanual reaching than unimanual reaching (73.8  18.0% (mean s.d.); F1,7 = 13.18, P < 0.01; Fig. 1d). This pattern was reversed if subjects had been trained on bimanual movements (unimanual compared to bimanual, 58.9 11.7%; F1,7 = 45.45, P < 0.001; Fig. 1e,f, and Supplementary Note and Supplementary Figs. 2 and 3 online); hence, incomplete transfer reflects a change in intralimb control rather than an additional bimanual constraint. Even though there are known differences in motor learning for dominant and nondominant arms5, we observed similar results with perturbations to the right arm (Supplementary Note and Supplementary Fig. 4 online). Also, hand motion of the unloaded right limb was unaffected by the learning process (Supplementary Note and Supplementary Fig. 5 online).
This experiment (Experiment 1) suggested that there is a partial, but not complete, overlap in control processes for unimanual and bimanual skills. This predicts that the unlearning of a force field is also context dependent. Whereas the repeated presentation of catch trials (3–10 in a row) normally eliminates force-field learning3,
4, we predicted incomplete washout if the learning and unlearning contexts differ due to incomplete overlap (Fig. 2a,b). In fact, our second experiment demonstrated that following unimanual training and bimanual washout, subjects immediately re-expressed a significant aftereffect when performing their first unimanual catch trial (versus baseline or final bimanual trial, P < 0.001 by t-test; Fig. 2c). Some of the unimanual learning remained intact (though 'invisible') until the proper probe trial, unimanual reaching, was re-performed. We obtained identical results when the training and washout contexts were reversed (versus baseline or final unimanual trial, P < 0.001 by t-test; Fig. 2d). Moreover, the difference in unimanual and bimanual aftereffects (c1 – c2 in Fig. 2e) successfully predicted the magnitude of residual learning (w in Fig. 2e; Fig. 2f).
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In a control experiment, we confirmed that complete washout occurred if the training and initial washout were the same (Supplementary Note and Supplementary Fig. 6 online). Catch trial effects and re-expressed aftereffects were much smaller if subjects learned the force field with their left arm while synchronously flexing their right ankle (P < 0.01 by t-test; green dots in Fig. 2f). Therefore, the magnitude of unimanual and bimanual interaction is specific to upper limb contexts; a gradient of interactions may reflect the somatotopic gradient of the motor system.
Our third experiment examined adaptation to conflicting force fields presented in alternation. Normally, this situation is extremely difficult to learn6,
7, but we predict that adaptation can occur simply by having one force field associated with unimanual movements and the other with bimanual movements.
This prediction was tested by exposing the subject's left arm to a rightward force field during unimanual movements and to a leftward force field during bimanual movements. Subjects exhibited significant learning between the early (trials 2–4) and late (trials 31–40) trials during this 'combined' task and significant aftereffects during catch trials (Holm's test, P < 0.05; Fig. 3). Subjects also exhibited a much slower washout than that normally observed, possibly reflecting the interaction of unimanual and bimanual washout trials. In contrast, when subjects reached with unimanual movements and the force direction was explicitly cued, they had no significant adaptation when the force fields were present (Holm's test, P > 0.05; Fig. 3b–d), and aftereffects were smaller for this 'unimanual-only' condition compared to the combined condition (Holm's test, P < 0.05; Fig. 3e, and Supplementary Note and Supplementary Fig. 7 online).
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It seems that behavioral context—unimanual versus bimanual—has a profound influence on learning and probably reflects differences in control processes for these two skills. Bimanual movements require substantive interhemispheric interactions8,
9 to coordinate movements of the two limbs, as well as greater involvement of cortical regions such as the supplementary motor area10, which we believe alters neural processing throughout the sensorimotor system. A partial, but not complete, overlap in load-related activity in primary motor cortex has been observed between posture and movement11. A similar shift in load-related processing in the neural circuitry between unimanual and bimanual contexts may underlie the present observations on learning.
The present results also illustrate the efficacy and limits on the transfer between unimanual and bimanual skills in sports and rehabilitation. Isolated practice with a single limb permits athletes or patients to focus their attention on specific details of motor performance. Here we show that such skill development can be transferred partially but that full transfer may never be possible owing to constraints on how the brain controls unimanual and bimanual movements. Thus, maximal performance of complex multilimb skills necessarily requires practice of the task in its entirety. Correspondingly, rehabilitation may be facilitated by bimanual motor practice12 but is likely to require further unimanual training to maximize motor recovery.
Note: Supplementary information is available on the Nature Neuroscience website.
Author contributions
This study was designed by all three authors. Data collection and data analysis were performed predominantly by D.N. All three authors contributed to the writing of the paper.
Received 21 June 2006; Accepted 18 September 2006; Published online: 8 October 2006.
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Acknowledgments
We thank J.R. Flanagan, J.A. Pruszynski, T. Herter and T. Lillicrap for helpful comments, K. Moore for expert technical help, and N. Nozaki for preparation of the figures. This work was supported by a Japan Society for the Promotion of Science (JSPS) bilateral program and a JSPS Grant-in-Aid for Scientific Research (C, #18500456) to D.N., and a grant from the National Science and Engineering Research Council to S.H.S.
Competing interests statement:
The authors declare competing financial interests. |
