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The Journal of Neuroscience, July 6, 2005, 25(27):6419-6434; doi:10.1523/JNEUROSCI.4904-04.2005

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Behavioral/Systems/Cognitive
Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors

Vincent C. K. Cheung,^1,2 Andrea d'Avella,³ Matthew C. Tresch,⁴ and Emilio Bizzi^2,5

¹Division of Health Sciences and Technology, Harvard Medical School and Massachusetts Institute of Technology, and ²Department of Brain and Cognitive Sciences and McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, ³Department of Neuromotor Physiology, Istituto di Ricovero e Cura a Carattere Scientifico, Fondazione Santa Lucia, 00179 Rome, Italy, ⁴Department of Biomedical Engineering, Northwestern University and Rehabilitation Institute of Chicago, Chicago, Illinois 60208, and ⁵European Brain Research Institute, 00143 Rome, Italy

Previous studies have suggested that the motor system may simplify control by combining a small number of muscle synergies represented as activation profiles across a set of muscles. The role of sensory feedback in the activation and organization of synergies has remained an open question. Here, we assess to what extent the motor system relies on centrally organized synergies activated by spinal and/or supraspinal commands to generate motor outputs by analyzing electromyographic (EMG) signals collected from 13 hindlimb muscles of the bullfrog during swimming and jumping, before and after deafferentation. We first established that, for both behaviors, the intact and deafferented data sets possess low and similar dimensionalities. Subsequently, we used a novel reformulation of the non-negative matrix factorization algorithm to simultaneously search for synergies shared by, and synergies specific to, the intact and deafferented data sets. Most muscle synergies were identified as shared synergies, suggesting that EMGs of locomotor behaviors are generated primarily by centrally organized synergies. Both the amplitude and temporal patterns of the activation coefficients of most shared synergies, however, were altered by deafferentation, suggesting that sensory inflow modulates activation of those centrally organized synergies. For most synergies, effects of deafferentation on the activation coefficients were not consistent across frogs, indicating substantial interanimal variability of feedback actions. We speculate that sensory feedback might adapt recruitment of muscle synergies to behavioral constraints, and the few synergies specific to the intact or deafferented states might represent afferent-specific modules or feedback reorganization of spinal neuronal networks.

Key words: deafferentation; locomotion; frog; feedback; afferent; non-negative matrix factorization; central pattern generators; jumping; swimming

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Received July 29, 2004; revised May 19, 2005; accepted May 20, 2005.

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