Specificity of Pairing Afferent and Efferent Activity for Inducing Neural Plasticity with an Associative Brain–Computer Interface

Brain-computer interface-based (BCI) training induces neural plasticity and promotes motor recovery in stroke patients by pairing movement intentions with congruent electrical stimulation of the affected limb, eliciting somatosensory afferent feedback. However, this training can potentially be refined further to enhance rehabilitation outcomes. It is not known how specific the afferent feedback needs to be with respect to the efferent activity from the brain. This study investigated how corticospinal excitability, a marker of neural plasticity, was modulated by four types of BCI-like interventions that varied in the specificity of afferent feedback relative to the efferent activity. Fifteen able-bodied participants performed four interventions: (1) wrist extensions paired with radial nerve peripheral electrical stimulation (PES) (matching feedback), (2) wrist extensions paired with ulnar nerve PES (non-matching feedback), (3) wrist extensions paired with sham radial nerve PES (no feedback), and (4) palmar grasps paired with radial nerve PES (partially matching feedback). Each intervention consisted of 100 pairings between visually cued movements and PES. The PES was triggered based on the peak of maximal negativity of the movement-related cortical potential associated with the visually cued movement. Before, immediately after, and 30 min after the intervention, transcranial magnetic stimulation-elicited motor-evoked potentials were recorded to assess corticospinal excitability. Only wrist extensions paired with radial nerve PES significantly increased the corticospinal excitability with 57 ± 49% and 65 ± 52% immediately and 30 min after the intervention, respectively, compared to the pre-intervention measurement. In conclusion, maximizing the induction of neural plasticity with an associative BCI requires that the afferent feedback be precisely matched to the efferent brain activity.