Mrachacz-Kersting N, Jiang N, Stevenson AJ, Niazi IK, Kostic V, Pavlovic A, Radovanovic S, Djuric-Jovicic M, Agosta F, Dremstrup K, Farina D. Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface. J Neurophysiol 115: 1410 -1421, 2016. First published December 30, 2015 doi:10.1152/jn.00918.2015 have the potential to improve functionality in chronic stoke patients when applied over a large number of sessions. Here we evaluated the effect and the underlying mechanisms of three BCI training sessions in a double-blind sham-controlled design. The applied BCI is based on Hebbian principles of associativity that hypothesize that neural assemblies activated in a correlated manner will strengthen synaptic connections. Twenty-two chronic stroke patients were divided into two training groups. Movement-related cortical potentials (MRCPs) were detected by electroencephalography during repetitions of foot dorsiflexion. Detection triggered a single electrical stimulation of the common peroneal nerve timed so that the resulting afferent volley arrived at the peak negative phase of the MRCP (BCI associative group) or randomly (BCI nonassociative group). Fugl-Meyer motor assessment (FM), 10-m walking speed, foot and hand tapping frequency, diffusion tensor imaging (DTI) data, and the excitability of the corticospinal tract to the target muscle [tibialis anterior (TA)] were quantified. The TA motor evoked potential (MEP) increased significantly after the BCI associative intervention, but not for the BCI nonassociative group. FM scores (0.8 Ϯ 0.46 point difference, P ϭ 0.01), foot (but not finger) tapping frequency, and 10-m walking speed improved significantly for the BCI associative group, indicating clinically relevant improvements. Corticospinal tract integrity on DTI did not correlate with clinical or physiological changes. For the BCI as applied here, the precise coupling between the brain command and the afferent signal was imperative for the behavioral, clinical, and neurophysiological changes reported. This association may become the driving principle for the design of BCI rehabilitation in the future. Indeed, no available BCIs can match this degree of functional improvement with such a short intervention.

It has been shown that the primary and secondary somatosensory cortex, as well as the supplementary motor area (SMA), are involved in central processing of proprioceptive signals during passive and active arm movements. However, it is not clear whether different cortical areas are involved in processing of different proprioceptive inputs (skin, joint, muscle receptors), what their relative contributions might be, where kinesthetic sensations are formed within the CNS, and how they interact when the full peripheral proprioceptive machinery acts. In this study we investigated the representation of the brain structures involved in the perception of passive limb movement and illusory movement generated by muscle tendon vibration. Changes in cortical activity as indicated by changes in regional cerebral blood flow (rCBF) were measured using positron emission tomography (PET). Twelve subjects were studied under four conditions: (1) passive flexion-extension movement (PM) of the left forearm; (2) induced illusions of movements (VI) similar to the real PM, induced by alternating vibration of biceps and triceps tendons (70-80 Hz) at the elbow; (3) alternating vibration of biceps and triceps tendons (with 20-50 Hz) without induced kinesthetic illusions (VN); and (4) rest condition (RE). The results show different patterns of cortex activation. In general, the activation during passive movement was higher in comparison with both kinds of vibration, and activation during vibrations with induced illusions of movement was more prominent than during vibrations without induced illusions. When the PM condition was contrasted with the other conditions we found the following areas of activation -- the primary motor (MI) and somatosensory area (SI), the SMA and the supplementary somatosensory area (SSA). In conditions where passive movements and illusory movements were contrasted with rest, some temporal areas, namely primary and associative auditory cortex, were activated, as well as secondary somatosensory cortex (SII). Our data show that different proprioceptive inputs, which induce sensation of movement, are associated with differently located activation patterns in the SI/MI and SMA areas of the cortex. In general, the comparison of activation intensities under different functional conditions indicates the involvement of SII in stimulus perception generation and of the SI/MI and SMA areas in the processing of proprioceptive input. Activation of the primary and secondary auditory cortex might reflect the interaction between somatosensory and auditory systems in movement sense generation. SSA might also be involved in movement sense generation and/or maintenance.

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