Modulation of Muscle Synergy Recruitment in Primate Grasping

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Abstract
In grasping, the CNS controls a particularly large number of degrees of freedom. We tested the idea that this control is facilitated by the presence of muscle synergies. According to the strong version of this concept, these synergies are invariant, hard-wired patterns of activation across muscles. Synergies may serve as modules that linearly sum, each with specific amplitude and timing coefficients, to generate a large array of muscle patterns. We tested two predictions of the synergy model. A small number of synergies should (1) account for a large fraction of variation in muscle activity, and (2) be modulated in their recruitment by task variables, even in novel behavioral contexts. We also examined whether the synergies would (3) have broadly similar structures across animals. We recorded from 15 to 19 electrodes implanted in forelimb muscles of two rhesus macaques as they grasped and transported 25 objects of variable shape and size. We show that three synergies accounted for 81% of the electromyographic data variation in each monkey. Each synergy was modulated in its recruitment strength and/or timing by object shape and/or size. Even when synergies were extracted from a small subset of object shape and size conditions and then used to reconstruct the entire dataset, we observed highly similar synergies and patterns of modulation. The synergies were well conserved between monkeys, with two of the synergies exceeding chance structural similarity, and the third being recruited, in both animals, in proportion to the size of the object handled.