A minimum transition hypothesis to account for motor synergies

Amir Karniel1, Ferdinando A. Mussa-Ivaldi 2, Andrea d’Avella3,
and Emilio Bizzi3

1Department of Electrical Engineering, Technion – Israel Institute of Technology, Israel

2Department of Physiology, Northwestern University Medical School, Chicago, Illinois

3Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts

"Nature sets in motion by signs and watchwords, which are made with little momentum.... Just as in the army the soldiers are set in motion by one word as if by a given signal and continue to move until they receive another signal to stop, so the muscles move in order and harmony from established custom." William Harvey (1578-1657)

The notion of muscle synergies reflects the hierarchical nature of the motor control system. This issue is extensively investigated, e.g., with regards to the relative role of the spinal cord and supraspinal systems, see Bizzi et al. Nature Reviews Neuroscience 1:101-108, 2000. In the midst of the previous millennium Harvey eloquently used the analogy of an army to describe this notion. Following this analogy, we present a general mathematical model and a premise that the role of synergism is to minimize the content of the motor command as measured by the number of transitions.

We describe the synergies by a matrix of filters. The inputs are motor commands and the outputs are muscle activations. We assume a simple motor command that consist of sparse combination of step functions, and consider the number of transitions in this vector of signals. The filters account for spinal neuronal circuits and for the muscle properties. Time-varying filters could also account for adaptation. The matrix of filters generalizes a constant matrix that was previously used and therefore allows complex time-varying signals (d'Avella and Tresch, NIPS 2001) with simple commands. The minimum transition hypothesis (MTH) asserts that the synergies (i.e., the matrix of filters) evolved to minimize the number of transitions in the motor command over the expected motor behavior of the animal.

We demonstrate the application of this theory to a set of 13 electromyography (EMG) signals recorded in intact frogs during different forms of behavior (jump, swim, kick and steps). We assess the predictions of the MTH by shuffling the EMG and by comparing possible static synergies that equivalently explain the variance of the data. The MTH and the mathematical framework provide new tools for the ongoing investigation of the superb dexterity in motor behavior.

Keywords: synergy, muscles, frog, electromyography

Presented at the twelfth annual neural control of movement meeting, Naples, Florida, April 16-21, 2002

[Poster in pdf]