Flexible adaptation to an artificial recurrent connection from muscle to peripheral nerve in man

Abstract

Controlling a neuroprosthesis requires learning a novel input-output transformation; however, how subjects incorporate this into limb control remains obscure. To elucidate the underling mechanisms, we investigated the motor adaptation process to a novel artificial recurrent connection (ARC) from a muscle to a peripheral nerve in healthy humans. In this paradigm, the ulnar nerve was electrically stimulated in proportion to the activation of the flexor carpi ulnaris (FCU), which is ulnar-innervated and monosynaptically innervated from Ia afferents of the FCU, defined as the “homonymous muscle,” or the palmaris longus (PL), which is not innervated by the ulnar nerve and produces similar movement to the FCU, defined as the “synergist muscle.” The ARC boosted the activity of the homonymous muscle and wrist joint movement during a visually guided reaching task. Participants could control muscle activity to utilize the ARC for the volitional control of wrist joint movement and then readapt to the absence of the ARC to either input muscle. Participants reduced homonymous muscle recruitment with practice, regardless of the input muscle. However, the adaptation process in the synergist muscle was dependent on the input muscle. The activity of the synergist muscle decreased when the input was the homonymous muscle, whereas it increased when it was the synergist muscle. This reorganization of the neuromotor map, which was maintained as an aftereffect of the ARC, was observed only when the input was the synergist muscle. These findings demonstrate that the ARC induced reorganization of neuromotor map in a targeted and sustainable manner.