Timing-dependent synergies between noninvasive motor cortex and spinal cord stimulation in chronic cervical spinal cord injury

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Abstract Precise movement requires integrating descending motor control with sensory feedback. Sensory networks interact strongly with descending motor circuits within the spinal cord. We targeted this interaction by pairing stimulation of the motor cortex with coordinated stimulation of the cervical spinal cord. We used separate non-invasive and epidural experiments to test the hypothesis that the strongest muscle response would occur when paired brain and spinal cord stimuli simultaneously converge within the spinal cord. For non-invasive experiments, we measured arm and hand muscle motor evoked potentials (MEPs) in response to transcranial magnetic stimulation (TMS) and transcutaneous spinal cord stimulation (TSCS) in 16 individuals with chronic spinal cord injury (SCI) and 15 uninjured individuals. We compared this noninvasive approach to intraoperative paired stimulation experiments using dorsal epidural electrodes in 38 individuals undergoing surgery for cervical myelopathy. We observed augmented muscle responses to suprathreshold TMS when subthreshold TSCS stimuli were timed to converge synchronously in the spinal cord. At convergent timing, target muscle MEPs increased by 11.0% overall (13.3% in people with SCI, 6.2% in uninjured individuals) compared to non-convergent time intervals. Facilitation correlated with TSCS intensity, with intensity close to movement threshold being most effective. Facilitation did not correlate with SCI level or severity, indicating spared circuits were sufficient for this effect. Noninvasive pairing produced less facilitation compared to intraoperative (epidural) pairing. Thus, sensorimotor interactions in the cervical spinal spinal cord can be targeted with paired stimulation in health and after SCI. Highlights Electrical stimulation of spinal sensory circuits can augment cortical motor evoked potentials, but only when they are timed to arrive synchronously in the spinal cord. Facilitation was at least as large in people with spinal cord injury compared with uninjured controls, suggesting that the necessary circuits for this facilitation were spared by injury. The magnitude of facilitation with noninvasive facilitation was smaller than the facilitation effect observed with epidural stimulation during elective spinal surgery, but they both rely on precisely timed interactions. Facilitation of hand and arm muscle responses correlated with the transcutaneous spinal stimulation intensity, suggesting that the magnitude of the pairing effect can be improved. Pairing was effective both in uninjured participants and those with SCI, independently of injury level, severity, or chronicity.

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