Distributed Neural Dynamics Underlie the Shift from Movement Preparation to Execution

Understanding how neural population activity supports the transition from movement preparation to execution remains a central challenge in systems neuroscience. Invasive recordings in nonhuman primates indicate that motor preparation and execution occupy orthogonal subspaces within the primary motor cortex (M1), yet how these neural dynamics evolve across broader networks and support skilled, memory-guided action remains poorly understood. We used source-resolved magnetoencephalography during a memory-guided finger-sequence task to track population dynamics across a cortico-hippocampal network. Manifold trajectories and decoding revealed that preparation and execution of movement sequences occupy distinct, yet not fully orthogonal, neural subspaces-a separation that generalized across all regions but was most pronounced in motor regions. Crucially, we identified a hierarchical spatio-temporal transition across the brain: The state shift originated in the hippocampus via theta-band modulations and rippled through the pre-SMA, SMA, and lateral premotor areas before culminating in M1 via broadband activity. This progression follows the functional hierarchy of descending motor pathways, with M1 shifting last, 160 msec before the first button press. Although sequence identity could be decoded from all areas during execution, only the hippocampus and M1 maintained predictive representations of upcoming sequences during preparation. These findings demonstrate that the initiation of complex motor sequences relies on a well-timed integration of hippocampal memory systems with primary motor output, rather than being a process localized to the motor cortices alone.