title: Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface.
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 (BCIassociative group) or randomly (BCInonassociative 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 BCIassociative intervention, but not for the BCInonassociative group. 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 BCIassociative 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.
authors.affiliation: Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark; nm@hst.aau.dk.
authors.forename: Natalie
authors.initials: N
authors.lastname: Mrachacz-Kersting
authors.affiliation: Department of Neurorehabilitation Engineering, Bernstein Focus Neurotechnology Göttingen, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Göttingen, Germany;
authors.forename: Ning
authors.identifier: http://orcid.org/0000-0003-1579-3114
authors.initials: N
authors.lastname: Jiang
authors.affiliation: Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark;
authors.forename: Andrew James Thomas
authors.initials: AJ
authors.lastname: Stevenson
authors.affiliation: Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark;
authors.forename: Imran Khan
authors.identifier: http://orcid.org/0000-0001-8752-7224
authors.initials: IK
authors.lastname: Niazi
authors.affiliation: Neurology Clinic, Clinical Center of Serbia, Faculty of Medicine, University of Belgrade, Belgrade, Serbia;
authors.forename: Vladimir
authors.initials: V
authors.lastname: Kostic
authors.affiliation: Neurology Clinic, Clinical Center of Serbia, Faculty of Medicine, University of Belgrade, Belgrade, Serbia;
authors.forename: Aleksandra
authors.initials: A
authors.lastname: Pavlovic
authors.affiliation: Neurology Clinic, Clinical Center of Serbia, Faculty of Medicine, University of Belgrade, Belgrade, Serbia;
authors.forename: Sasa
authors.initials: S
authors.lastname: Radovanovic
authors.affiliation: Innovation Center, School of Electrical Engineering (ICEF), Belgrade, Serbia; and.
authors.forename: Milica
authors.initials: M
authors.lastname: Djuric-Jovicic
authors.affiliation: Neuroimaging Research Unit, Division of Neuroscience, Institute of Experimental Neurology, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy.
authors.forename: Federica
authors.initials: F
authors.lastname: Agosta
authors.affiliation: Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark;
authors.forename: Kim
authors.initials: K
authors.lastname: Dremstrup
authors.affiliation: Department of Neurorehabilitation Engineering, Bernstein Focus Neurotechnology Göttingen, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Göttingen, Germany;
authors.forename: Dario
authors.initials: D
authors.lastname: Farina
mesh_terms: D000328:Adult; D000368:Aged; D001244:Association; D062207:Brain-Computer Interfaces; D019054:Evoked Potentials, Motor; D005260:Female; D005528:Foot / Q000502:physiology; D006225:Hand / Q000502:physiology; D006801:Humans; D008297:Male; D008875:Middle Aged; D018482:Muscle, Skeletal / Q000502:physiology; D009473:Neuronal Plasticity; D011712:Pyramidal Tracts / Q000502:physiology; D020127:Recovery of Function; D020521:Stroke / Q000503:physiopathology*; D000071939:Stroke Rehabilitation
keywords: Hebb; associativity; brain-computer interface; neuroplasticity; stroke