The effect of type of afferent feedback timed with motor imagery on the induction of cortical plasticity

Abstract

A peripherally generated afferent volley that arrives at the peak negative (PN) phase during the movement related cortical potential (MRCP) induces significant plasticity at the cortical level in healthy individuals and chronic stroke patients. Transferring this type of associative brain-computer interface (BCI) intervention into the clinical setting requires that the proprioceptive input is comparable to the techniques implemented during the rehabilitation process. These consist mainly of functional electrical stimulation (FES) and passive movement induced by an actuated orthosis. In this study, we compared these two interventions (BCI and BCI) where the afferent input was timed to arrive at the motor cortex during the PN of the MRCP. Twelve healthy participants attended two experimental sessions. They were asked to perform 30 dorsiflexion movements timed to a cue while continuous electroencephalographic (EEG) data were collected from FP1, Fz, FC1, FC2, C3, Cz, C4, CP1, CP2, and Pz, according to the standard international 10-20 system. MRCPs were extracted and the PN time calculated. Next, participants were asked to imagine the same movement 30 times while either FES (frequency: 20Hz, intensity: 8-35mAmp) or a passive ankle movement (amplitude and velocity matched to a normal gait cycle) was applied such that the first afferent inflow would coincide with the PN of the MRCP. The change in the output of the primary motor cortex (M1) was quantified by applying single transcranial magnetic stimuli to the area of M1 controlling the tibialis anterior (TA) muscle and measuring the motor evoked potential (MEP). Spinal changes were assessed pre and post by eliciting the TA stretch reflex. Both BCI and BCI led to significant increases in the excitability of the cortical projections to TA (F=4.44, p=0.024) without any concomitant changes at the spinal level. These effects were still present 30min after the cessation of both interventions. There was no significant main effect of intervention, F=0.38, p=0.550, indicating that the changes in MEP occurred independently of the type of afferent inflow. An afferent volley generated from a passive movement or an electrical stimulus arrives at the somatosensory cortex at similar times. It is thus likely that the similar effects observed here are strictly due to the tight coupling in time between the afferent inflow and the PN of the MRCP. This provides further support to the associative nature of the proposed BCI system.

Comparison of the Efficacy of a Real-Time and Offline Associative Brain-Computer-Interface

“…This timing is imperative as neither early nor late arrival results in plasticity induction ( Mrachacz-Kersting et al, 2012 ). The average PN time in the initial training set was similar to what we have reported previously and did not differ significantly for the BCI offline and BCI online sessions ( Mrachacz-Kersting et al, 2012 , 2017c ). Since participants did not alter their reaction time to the visual cue within the BCI offline intervention set (the PN time was similar to the initial 30 trials), we may assume that indeed 30 pairs with the appropriate time were applied.…”

“…It is currently not established how many pairs of peripheral and central inputs are required for such changes to be induced. In previous studies both 50 pairings ( Mrachacz-Kersting et al, 2012 , 2016 ) and 30 pairings ( Mrachacz-Kersting et al, 2017c ) have resulted in significant changes. In the original PAS studies (see review by Suppa et al, 2017 ), 90 pairs were applied when targeting hand muscles ( Stefan, 2000 ), and this could be further reduced to 50 when the muscle was pre-contracted ( Kujirai et al, 2006 ).…”

Brain Functional Networks Study of Subacute Stroke Patients With Upper Limb Dysfunction After Comprehensive Rehabilitation Including BCI Training

“…BCI systems can also be used to detect real-time primary motor cortex activation, i.e., the intention to move. As particularly relevant input to BCI systems, EEG signals have highly accurate temporal resolution, are suitable to clinical environments, and can provide matched sensory stimulation according to specific feedback protocols (15,16). Hence, BCI systems used for motor neurorehabilitation can induce activity-dependent plasticity in specific areas of the brain by requiring the user to pay close attention during task-oriented training, which activates sensorimotor areas (9,17,18).…”

Intra- and Inter-Rater Reliability of Manual Feature Extraction Methods in Movement Related Cortical Potential Analysis

“…An example of a context which requires reliable labelling of ERPs is in the delivery of an endogenous paired associative stimulation (ePAS) intervention, a non-invasive neuromodulatory intervention that has been shown to modulate corticomotor excitability in healthy people [7,[17][18][19] and people with stroke [20,21]. Based on traditional paired associative stimulation (PAS) [22][23][24], ePAS involves the delivery of 50 single pulses of peripheral electrical stimulation, each paired with an endogenous ERP signal known as the movement related cortical potential (MRCP) [7,17,18,20,21]. The MRCP is observed as an individual prepares and executes a voluntary or imagined movement [25,26] and is characterized by a slow (≈0.5 Hz) negative potential which begins approximately 1.5 to 2 s prior to movement and peaks around the onset of movement (amplitude -5 to -30 uV) [25,26].…”

“…This timing is achieved by triggering the peripheral electrical stimulation at a set number of milliseconds before the PN of the MRCP to account for the conduction time between the peripheral nerve and the M1 [7]. However, the neuromodulatory effects of ePAS present considerable between-participant variability [17][18][19][20][21]. For example, Olsen et al [17] showed increases in corticomotor excitability ranging from 4%-396% (n = 10).…”