Muscle Synergy Organization Is Robust Across a Variety of Postural Perturbations

Abstract

. We recently showed that four muscle synergies can reproduce multiple muscle activation patterns in cats during postural responses to support surface translations. We now test the robustness of functional muscle synergies, which specify muscle groupings and the active force vectors produced during postural responses under several biomechanically distinct conditions. We aimed to determine whether such synergies represent a generalized control strategy for postural control or if they are merely specific to each postural task. Postural responses to multidirectional translations at different fore-hind paw distances and to multidirectional rotations at the preferred stance distance were analyzed. Five synergies were required to adequately reconstruct responses to translation at the preferred stance distance-four were similar to our previous analysis of translation, whereas the fifth accounted for the newly added background activity during quiet stance. These five control synergies could account for Ͼ80% total variability or r 2 Ͼ 0.6 of the electromyographic and force tuning curves for all other experimental conditions. Forces were successfully reconstructed but only when they were referenced to a coordinate system that rotated with the limb axis as stance distance changed. Finally, most of the functional muscle synergies were similar across all of the six cats in terms of muscle synergy number, synergy activation patterns, and synergy force vectors. The robustness of synergy organization across perturbation types, postures, and animals suggests that muscle synergies controlling task-variables are a general construct used by the CNS for balance control. I N T R O D U C T I O NRecent findings suggest that the CNS simplifies motor control by constraining muscles to be activated in fixed groups, or synergies, where each synergy is defined as a set of muscles recruited by a single neural command signal. Complex muscle activation patterns in a wide range of motor tasks including locomotion, finger spelling, and postural tasks, can be decomposed into the summed activation of just a few muscle synergies d'Avella et al. 2003;Ivanenko et al. 2003Ivanenko et al. , 2004Krishnamoorthy et al. 2003;Poppele and Bosco 2003;Poppele et al. 2002;Ting and Macpherson 2005;Tresch et al. 1999;Weiss and Flanders 2004). A muscle synergy control structure provides an attractive simplifying strategy for the control of complex movements because it reduces the number of output patterns that the nervous system must specify for a large number of muscles yet allows flexibility in the final expression of muscle activation.A synergy control structure not only simplifies the motor output pattern for muscle activation but may also be functionally related to high-level control parameters-global biomechanical variables that are important for movement control. For example, Ting and Macpherson (2005) demonstrated in cats that four muscle synergies could account for the spatial tuning patterns of the automatic postural response elicited by support surface ...

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

“…Namely, the "push-back" and "pushforward" M-modes, likely related to the A-eigenmovement, were found in studies involving large COP shift and relatively small COM motion such as during whole-body sway (DannaDos-Santos et al 2007), preparation to stepping (Wang et al 2005(Wang et al , 2006, and anticipatory postural adjustments prior to self-induced perturbations (Krishnamoorthy et al 2003b). In contrast, M-modes likely related to the H-eigenmovement were found in studies involving fast and large COM displacements such as during balance recovery following an external perturbation (Torres-Oviedo et al 2006;Torres-Oviedo and Ting 2007) and large COM acceleration accompanied by a relatively small COP shift (as in the current study).…”

“…The notion of multi-muscle synergies has been invoked in many studies of postural tasks (Krishnamoorthy et al 2003a(Krishnamoorthy et al ,b, 2004Ivanenko et al 2005Ivanenko et al , 2006 ; Ting and Macpherson 2005;Wang et al 2005Wang et al , 2006Torres-Oviedo et al 2006;Danna-Dos-Santos et al 2007) as a means of reducing (but not eliminating) the notorious redundancy of the multi-muscle system (cf. Bernstein 1967).…”

Functional muscle synergies constrain force production during postural tasks

“…We used a static musculoskeletal model of the cat hindlimb (McKay et al 2007) and kinematic and kinetic data of three cats performing a horizontal translation balance task at four (cats Bi and Ru) or three (cat Ni) postural configurations to simulate functional muscle synergies based on those of Torres-Oviedo et al (2006). Model postures approximating the average background period kinematics of each animal in each postural configuration (11 in total) were calculated as in (McKay et al 2007).…”

“…In a recent study (Torres-Oviedo et al 2006), we demonstrated that electromyographic and kinetic data from automatic postural responses in cats could be simultaneously decomposed into a small set of five "functional" muscle synergies, which specify both a fixed pattern of hindlimb muscle activation (a muscle synergy) and a correlated "synergy force vector" at the ground. Variation in the muscle activation patterns and forces produced when the cats stood in different postural configuration (anterior-posterior "stance distances, " Macpherson 1994) could be accounted for by the same muscle synergies if we assumed that the forces generated by each muscle synergy rotated with the limb axis as it varied in the sagittal plane.…”

“…While our prior analysis demonstrated that the measured EMG and force components could be correlated via the assumed muscle synergy to endpoint force transformation, we could not demonstrate that this relationship was biomechanically causal. In this study, synergy force vectors identified in the control posture of each animal from the previous work (Torres-Oviedo et al 2006) were used as source data, and simulated muscle synergies corresponding to each hypothesized synergy force vector were determined with numerical optimization (e.g., Crowninshield and Brand 1981;Harris and Wolpert 1998;Kurtzer et al 2006;Valero-Cuevas et al 1998). We then applied these muscle synergies to the model in other postures to test whether the resulting force vectors were oriented consistently with respect to the limb axis.…”