Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface

Author:

Mrachacz-Kersting Natalie1,Jiang Ning2ORCID,Stevenson Andrew James Thomas1,Niazi Imran Khan1ORCID,Kostic Vladimir3,Pavlovic Aleksandra3,Radovanovic Sasa3,Djuric-Jovicic Milica4,Agosta Federica5,Dremstrup Kim1,Farina Dario2

Affiliation:

1. Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark;

2. Department of Neurorehabilitation Engineering, Bernstein Focus Neurotechnology Göttingen, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Göttingen, Germany;

3. Neurology Clinic, Clinical Center of Serbia, Faculty of Medicine, University of Belgrade, Belgrade, Serbia;

4. Innovation Center, School of Electrical Engineering (ICEF), Belgrade, Serbia; and

5. Neuroimaging Research Unit, Division of Neuroscience, Institute of Experimental Neurology, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy

Abstract

Brain-computer interfaces (BCIs) 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 (BCIassociativegroup) or randomly (BCInonassociativegroup). 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 BCIassociativeintervention, but not for the BCInonassociativegroup. FM scores (0.8 ± 0.46 point difference, P = 0.01), foot (but not finger) tapping frequency, and 10-m walking speed improved significantly for the BCIassociativegroup, 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.

Funder

Danish Agency for Science and Technology

EU project BETTER

MESTD of Serbia

Publisher

American Physiological Society

Subject

Physiology,General Neuroscience

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