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Neuromuscular and biomechanical factors codetermine the solution to motor redundancy in rhythmic multijoint arm movement

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Abstract

How the CNS deals with the issue of motor redundancy remains a central question for motor control research. Here we investigate the means by which neuromuscular and biomechanical factors interact to resolve motor redundancy in rhythmic multijoint arm movements. We used a two-df motorised robot arm to manipulate the dynamics of rhythmic flexion–extension (FE) and supination–pronation (SP) movements at the elbow-joint complex. Participants were required to produce rhythmic FE and SP movements, either in isolation, or in combination (at the phase relationship of their choice), while we recorded the activity of key bi-functional muscles. When performed in combination, most participants spontaneously produced an in-phase pattern of coordination in which flexion is synchronised with supination. The activity of the Biceps Brachii (BB), the strongest arm muscle which also has the largest moment arms in both flexion and supination was significantly higher for FE and SP performed in combination than in isolation, suggesting optimal exploitation of the mechanical advantage of this muscle. In a separate condition, participants were required to produce a rhythmic SP movement while a rhythmic FE movement was imposed by the motorised robot. Simulations based upon a musculoskeletal model of the arm demonstrated that in this context, the most efficient use of the force–velocity relationship of BB requires that an anti-phase pattern of coordination (flexion synchronized with pronation) be produced. In practice, the participants maintained the in-phase behavior, and BB activity was higher than for SP performed in isolation. This finding suggests that the neural organisation underlying the exploitation of bifunctional muscle properties, in the natural context, constrains the system to maintain the “natural” coordination pattern in an altered dynamic environment, even at the cost of reduced biomechanical efficiency. We suggest an important role for afference from the imposed movement in promoting the “natural” pattern. Practical implications for the emerging field of robot-assisted therapy and rehabilitation are briefly mentioned.

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Acknowledgments

This work was supported by The Australian Research Council, The National Health and Medical Research Council, and a University of Queensland Early Career Researcher Grant awarded to the first author.

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Authors and Affiliations

  1. Perception and Motor Systems Laboratory, School of Human Movement Studies, The University of Queensland, Room 424, Building 26, St Lucia, Brisbane, QLD, 4072, Australia

    Aymar de Rugy, Stephan Riek, Yalchin Oytam, Timothy J. Carroll & Richard G. Carson

  2. A.E. Mann Institute for Biomedical Engineering, University of Southern California, Los Angeles, USA

    Rahman Davoodi

  3. School of Psychology, Queen’s University Belfast, Belfast, Northern Ireland

    Richard G. Carson

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  1. Aymar de Rugy
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  2. Stephan Riek
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  3. Yalchin Oytam
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  6. Richard G. Carson
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Correspondence to Aymar de Rugy.

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de Rugy, A., Riek, S., Oytam, Y. et al. Neuromuscular and biomechanical factors codetermine the solution to motor redundancy in rhythmic multijoint arm movement. Exp Brain Res 189, 421–434 (2008). https://doi.org/10.1007/s00221-008-1437-2

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