Challenges and New Approaches to Proving the Existence of Muscle Synergies of Neural Origin

Abstract

Muscle coordination studies repeatedly show low-dimensionality of muscle activations for a wide variety of motor tasks. The basis vectors of this low-dimensional subspace, termed muscle synergies, are hypothesized to reflect neurally-established functional muscle groupings that simplify body control. However, the muscle synergy hypothesis has been notoriously difficult to prove or falsify. We use cadaveric experiments and computational models to perform a crucial thought experiment and develop an alternative explanation of how muscle synergies could be observed without the nervous system having controlled muscles in groups. We first show that the biomechanics of the limb constrains musculotendon length changes to a low-dimensional subspace across all possible movement directions. We then show that a modest assumption—that each muscle is independently instructed to resist length change—leads to the result that electromyographic (EMG) synergies will arise without the need to conclude that they are a product of neural coupling among muscles. Finally, we show that there are dimensionality-reducing constraints in the isometric production of force in a variety of directions, but that these constraints are more easily controlled for, suggesting new experimental directions. These counter-examples to current thinking clearly show how experimenters could adequately control for the constraints described here when designing experiments to test for muscle synergies—but, to the best of our knowledge, this has not yet been done. How the brain and spinal cord control the body is a fundamental question of critical scientific and clinical importance. The preferred experimental approach to answer this question has been to infer the neural control strategy by analyzing recordings of muscle activity and limb mechanics collected while animals and people use their limbs. This has led to a popular, but not yet proven, hypothesis that the brain and spinal cord simplify the control of the numerous muscles by grouping them into few functional units called neural synergies. Our detailed experiments and simulations challenge the utility of this approach and the validity of its interpretation. We point out that mechanical constraints can also explain those experimental recordings. In particular, the anatomy of the limb combined with the type of tasks studied and analysis used, suffice to give the appearance of neural synergies. To be clear, we do not disprove the neural synergy hypothesis. Rather, in the tradition of scientific debate, by showing an alternative explanation to the available data we challenge the community and ourselves to design novel experiments and analyses to conclusively test that hypothesis by ruling out the confounds we point out.