Muscle Synergies Encoded Within the Spinal Cord: Evidence From Focal Intraspinal NMDA Iontophoresis in the Frog

Abstract

This paper relates to the problem of the existence of muscle synergies, that is whether the CNS command to muscles is simplified by controlling their activity in subgroups or synergies, rather than individually. We approach this problem with two methods that have been recently introduced: intraspinal N-methyl-D-aspartate (NMDA) microstimulation and a synergy-extracting algorithm. To search for a common set of synergies encoded for by the spinal cord whose combinations would account for a large range of electromyographic (EMG) patterns, we chose, rather than examining a large range of natural behaviors, to chemically microstimulate a large number of spinal cord interneuronal sites in different frogs. A possible advantage of this complementary method is that it is task-independent. Visual inspection suggested that the NMDA-elicited EMG patterns recorded from 12 leg muscles might indeed be constructed from smaller subgroups of muscles whose activity co-varied, suggestive of synergies. We used a modification of our extracting computational algorithm whereby a nonnegative least-squares method was employed to iteratively update both the synergies and their coefficients of activation in reconstructing the EMG patterns. Using this algorithm, a limited set of seven synergies was found whose linear combinations accounted for more than 91% of the variance in the pooled EMG data from 10 frogs, and more than 96% in individual frogs. The extracted synergies were similar among frogs. Further, preferred combinations of these synergies were clearly identified. This was found by extracting smaller sets of four, five, or six synergies and fitting each synergy from those sets as a combination from the set of seven synergies extracted from the same frog; the synergy combinations from each frog were then pooled together to examine their frequency of occurrence. Concordance with this method of identifying synergy combinations was found by examining how the synergies from the set of seven correlated pair-wise as they reconstructed the EMG data. These results support the existence of muscle synergies encoded within the spinal cord, which through preferred combinations, account for a large repertoire of spinal cord motor output. These findings are contrasted with previous approaches to the problem of synergies.

Combining modules for movement

“…Tresch found that the two sets of EMG responses were very similar to one another. In addition, the synergies evoked by NMDA were found by (Saltiel et al 2001) to be qualitatively similar to those described by Tresch.…”

“…Neither can it result from activating the fibers of passage of the descending fibers and those of the sensory systems. On the basis of these results, (Giszter et al, 1993 andSaltiel et al 2001) we have concluded that distinct interneuronal networks of the spinal cord must be the source of specific types of CFFs..…”

Learning effects on muscle modes and multi-mode postural synergies

“…Both lines of research follow the general idea that a smaller number of variables (M-modes in our study or "synergies" in most other studies) can be used to construct behaviors with different characteristics (Loeb et al 2000;Saltiel et al 2001;d'Avella and Bizzi 2005;Ting and Macpherson 2005). A recent comparison of different methods to identify such M-modes ("synergies") has suggested that the results are robust across a variety of methods including principal component analysis and independent component analysis (Tresch et al 2006).…”

Multi-muscle synergies in an unusual postural task: quick shear force production

“…At the lower level, muscles form groups, within which their levels of activation co-vary across a wide range of tasks. Such groups have been referred to as muscle modes (M-modes, Krishnamoorthy et al 2003a,b) or muscle synergies (Ivanenko et al 2004(Ivanenko et al , 2005(Ivanenko et al , 2006Ting and Macpherson 2005;Torres-Oviedo and Ting 2007;Saltiel et al 2001;D'Avela et al 2005). At the upper level, the M-modes are considered as the elemental variables, and their co-variation is organized in a task-specific manner to stabilize an important performance variable.…”