Principles of encoding motor commands in travelling waves of neural oscillations

Abstract

Travelling waves of oscillatory neuronal activity have been observed in most regions of the cortex, including motor cortex, yet their function is unknown. This thesis explores the computational principles by which the morphology of waves in motor cortex may encode movement commands, and how those commands may be decoded by the descending motor pathway to evoke specific postures in a simulated biomechanical limb. A series of numerical simulations are presented that provide support for this hypothesis. The first study investigates the generative principles of waves in cortex using a neurobiological model of coupled oscillators. It is shown that waves arise from inhibitory-surround neuronal connectivity and that wave morphology is governed by connection topology. Eliminating the inhibitory connections produces spatial synchrony, which is equated with motor rest in this hypothesis. The net oscillatory output of the model when switching between waves and synchrony closely resembles that of human motor cortex when switching between active movement and motor readiness. The second study explores the problem of translating cortical wave patterns into muscle movements. It is proposed that the primary output neurons of the motor cortex act as spatial filters that discriminate cortical wave patterns to selectively activate motor neurons in the spinal cord. The proposed corticospinal model not only modulates the descending motor drive but also replicates key aspects of corticospinal coherence observed in human movement physiology. The third study presents a three-link biomechanical limb model designed to exercise the proposed motor model. The limb is driven by antagonist pairs of muscle actuators that replicate the natural motions of muscle and joint. The stable operating ranges of antagonist muscles are surveyed and the impact of co-contraction on limb stability is demonstrated. The final study combines all previous studies into a model that spans the full motor pathway from cortex to limb. Specific wave patterns in cortex are shown to evoke specific postures in the limb which may be maintained indefinitely or relaxed by manipulating the inhibitory connections in cortex. The combined model thus demonstrates the proposed principle of encoding motor commands in cortex as travelling waves of neuronal oscillations.