Fast Oscillatory Commands from the Motor Cortex Can Be Decoded by the Spinal Cord for Force Control.

Oscillations in the beta and gamma bands (13-30 Hz; 35-70 Hz) have often been observed in motor cortical outputs that reach the spinal cord, acting on motoneurons and interneurons. However, the frequencies of these oscillations are above the muscle force frequency range. A current view is that the transformation of the motoneuron pool inputs into force is linear. For this reason possible roles for these oscillations are unclear, since if this transformation is linear, the high frequencies in the motoneuron inputs (e.g., 20 Hz from pyramidal tract neurons) would be filtered out by the muscle and have no effect on force control. A biologically inspired mathematical model of the neuromuscular system was used to investigate the impact of high-frequency cortical oscillatory activity on force control. The model simulation results evidenced that a typical motoneuron pool has a nonlinear behavior that enables the decoding of a high-frequency oscillatory input. An input at a single frequency (e.g., beta band) leads to an increase in the steady-state force generated by the muscle. When the input oscillation was amplitude modulated at a given low frequency, the force oscillated at this frequency. In both cases, the mechanism relies on the recruitment and derecruitment of motor units in response to the oscillatory descending drive. Therefore, the results from this study suggest a potential role in force control for cortical oscillations at frequencies at or above the beta band, despite the low-pass behavior of the muscles. SIGNIFICANCE STATEMENT: The role of cortical oscillations in motor control has been a long-standing question, one view being that they are an epiphenomenon. Fast oscillations are known to reach the spinal cord, and hence they have been thought to affect muscle behavior. However, experimental limitations have hampered further advances to explain how they could influence muscle force. An approach for such a challenge was adopted in the present research: to study the problem through computer simulations of an advanced biologically compatible mathematical model. Using such a model, we found that the well-known mechanism of recruitment and derecruitment of the spinal cord motoneurons can allow the muscle to respond to cortical oscillations, suggesting that these oscillations are not epiphenomena in motor control.