Context-dependent low-dimensional neural dynamics unfold in distinct subspaces, dimensionality, and dynamical strength for natural walking and reaching

Abstract

Awake behaving animal experiments paired with multichannel electrode recordings have advanced motor systems neuroscience in creating models of how the mammalian brain controls move-ments. However, growing theoretical and experimental evidence question the generalizability of such findings from constrained studies to ambulatory behavior, highlighting a limitation in our understanding of how the brain controls movement. To address this question, spiking neural activity during highly-practiced, routine movement (walking) and goal-directed behavior (reach-ing towards food) were compared in an unconstrained setting. Kinematic trajectories of the contralateral arm during reaching and walking were statistically similar, as were the average single-neuron firing rates during these respective movements. However, the dimensionality of reaching was higher than that of walking and existed in largely non-overlapping subspaces. Further, when modeled as dynamical systems, reaching decayed 3-5 times more quickly than walking. Taken together, these findings demonstrate that the low-dimensional structure of motor cortex is more complex for goal-directed reaching than in highly-practiced natural movements. Since this difference is primarily observable at the state and dynamical systems level, these findings suggest behavioral context plays a significant role in the coordination of otherwise kinematically similar movements, providing indirect evidence for non-cortical circuits such as central pattern generators.