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Abstract
Repeated paired stimulation of two peripheral nerves can produce lasting changes in motor cortical excitability, but little is known of the underlying neuronal basis. Here, we trained two macaque monkeys to perform selective thumb and index finger abduction movements. Neural activity was recorded from the contralateral primary motor cortex during task performance, and following stimulation of the ulnar and median nerves, and the nerve supplying the extensor digitorum communis (EDC) muscle. Responses were compared before and after 1 h of synchronous or asynchronous paired ulnar/median nerve stimulation. Task performance was significantly enhanced after asynchronous and impaired after synchronous stimulation. The amplitude of short latency neural responses to median and ulnar nerve stimulation was increased after asynchronous stimulation; later components were reduced after synchronous stimulation. Synchronous stimulation increased neural activity during thumb movement and decreased it during index finger movement; asynchronous stimulation decreased activity during both movements. To assess how well neural activity could separate behavioral or sensory conditions, linear discriminant analysis was used to decode which nerve was stimulated, or which digit moved. Decoding accuracy for nerve stimulation was decreased after synchronous and increased after asynchronous paired stimulation. Decoding accuracy for task performance was decreased after synchronous but was unchanged after asynchronous paired stimulation. Paired stimulation produces changes in motor cortical circuits that outlast the stimulation. Some of these changes depend on precise stimulus timing.NEW & NOTEWORTHY Paired stimulation of peripheral nerves for 1 h induced lasting changes in neural responses within the motor cortex to nerve stimulation and to performance of a behavioral task. These changes were sufficient to alter the efficiency with which activity could encode stimulus type. Stimuli that can be easily applied noninvasively in human subjects can alter central motor circuits.
Highlights
Synaptic connections within the motor systems are not fixed but can be modified based on experience
We show that long-term plastic changes can be induced in M1 activity following a period of paired nerve stimulation
Paired nerve stimulation can be applied in humans noninvasively for long periods, suggesting that it may prove to be a useful tool in the armory of neurostimulation approaches to aid functional recovery in patients
Summary
Synaptic connections within the motor systems are not fixed but can be modified based on experience. Plasticity can be induced by repetitive TMS [4], or by pairing TMS with a peripheral stimulus [5,6,7], with natural activity generated during voluntary movements [8,9,10] or with motor imagery [11, 12] These different approaches each have advantages and disadvantages, for example, in their relative ability to produce plastic changes in different muscle groups [13]. All share the disadvantage of requiring a bulky and expensive TMS machine and precise placement of the stimulating coil on the scalp. This limits their applicability to a laboratory setting, and the number of stimuli is constrained to what is feasible during a laboratory visit. Larger plastic changes might be generated by more stimuli (e.g., 14); this could
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