Coherent oscillations across the human brain, spinal cord, and muscle network.

Abstract

Voluntary human movement emerges from dynamic interactions between the brain, spinal cord, and sensory afferents. Spinal cord function has proven particularly difficult to study non-invasively in humans due to its deep anatomical location and narrow diameter. As a result, sensorimotor interactions are often studied using cortico-muscular coupling, which captures interactions between brain and muscle but cannot reveal how these signals propagate through the spinal cord. Here, we use concurrent brain and spinal cord imaging with optically pumped magnetometers (OPMs) and electromyography (EMG) to test whether endogenous synchronization within the human sensorimotor system can be detected and characterized non-invasively across cortical, spinal, and muscular levels. Participants (n = 9) performed a sustained isometric hand contraction while we recorded cortical and spinal cord magnetic fields using OPMs and hand muscle activity using EMG, and we compared rhythmic activity propagating through the cortico-spinal-muscular loop with the state at rest. We show that the spinal contribution to cortico-muscular coupling manifests as coherent 10-35 Hz activity linking the contralateral sensorimotor cortex, cervical spinal cord, and muscle. This synchronization forms a distributed, bidirectionally interacting network with physiologically plausible temporal delays. The spatial organization of this activity accords with known sensorimotor anatomy, localizing to cervical segments appropriate for upper-limb control. Our results provide the first direct, non-invasive magnetic field evidence in humans of coherent brain and spinal cord oscillations and demonstrate the feasibility of concurrent, spatiotemporally resolved imaging of the central nervous system to open new avenues for studying human sensorimotor physiology.