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

Natalie Mrachacz-Kersting, Ning Jiang, Andrew James Thomas Stevenson, Imran Khan Niazi, Vladimir Kostic, Aleksandra M. Pavlović, Sasa Radovanovic, Milica Djuric-Jovicic, Federica Agosta, Kim Dremstrup, Dario Farina

Research output: Contribution to journalJournal articleResearchpeer-review

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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 evaluate 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 hypothesizes that neural assemblies activated in a correlated manner will strengthen synaptic connections. Twenty-two chronic stroke patients were allocated into two training groups. Movement-related cortical potentials (MRCPs) were detected using elecroencephalography 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 (BCInon-associative group). Fugl-Meyer motor assessment (FM), 10-m walking speed, foot and hand tapping frequency and the excitability of the corticospinal tract to the target muscle (tibialis anterior (TA)) were quantified. The TA motor evoked potential increased significantly following the BCIassociative intervention, but not for the BCInon-associative group. Fugl-Meyer motor 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. 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.
Original languageEnglish
JournalJournal of Neurophysiology
Volume115
Issue number3
Pages (from-to)1410-1421
ISSN0022-3077
DOIs
Publication statusPublished - 2016

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Brain-Computer Interfaces
Neuronal Plasticity
Stroke
Foot
Motor Evoked Potentials
Peroneal Nerve
Pyramidal Tracts
Electric Stimulation
Fingers
Rehabilitation
Hand
Muscles
Brain

Cite this

Mrachacz-Kersting, Natalie ; Jiang, Ning ; Stevenson, Andrew James Thomas ; Niazi, Imran Khan ; Kostic, Vladimir ; Pavlović, Aleksandra M. ; Radovanovic, Sasa ; Djuric-Jovicic, Milica ; Agosta, Federica ; Dremstrup, Kim ; Farina, Dario. / Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface. In: Journal of Neurophysiology. 2016 ; Vol. 115, No. 3. pp. 1410-1421.
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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 evaluate 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 hypothesizes that neural assemblies activated in a correlated manner will strengthen synaptic connections. Twenty-two chronic stroke patients were allocated into two training groups. Movement-related cortical potentials (MRCPs) were detected using elecroencephalography 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 (BCInon-associative group). Fugl-Meyer motor assessment (FM), 10-m walking speed, foot and hand tapping frequency and the excitability of the corticospinal tract to the target muscle (tibialis anterior (TA)) were quantified. The TA motor evoked potential increased significantly following the BCIassociative intervention, but not for the BCInon-associative group. Fugl-Meyer motor 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. 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.",
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Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface. / Mrachacz-Kersting, Natalie; Jiang, Ning; Stevenson, Andrew James Thomas; Niazi, Imran Khan; Kostic, Vladimir; Pavlović, Aleksandra M.; Radovanovic, Sasa; Djuric-Jovicic, Milica; Agosta, Federica; Dremstrup, Kim; Farina, Dario.

In: Journal of Neurophysiology, Vol. 115, No. 3, 2016, p. 1410-1421.

Research output: Contribution to journalJournal articleResearchpeer-review

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AU - Mrachacz-Kersting, Natalie

AU - Jiang, Ning

AU - Stevenson, Andrew James Thomas

AU - Niazi, Imran Khan

AU - Kostic, Vladimir

AU - Pavlović, Aleksandra M.

AU - Radovanovic, Sasa

AU - Djuric-Jovicic, Milica

AU - Agosta, Federica

AU - Dremstrup, Kim

AU - Farina, Dario

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N2 - Brain-computer interfaces (BCIs) have the potential to improve functionality in chronic stoke patients when applied over a large number of sessions. Here, we evaluate 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 hypothesizes that neural assemblies activated in a correlated manner will strengthen synaptic connections. Twenty-two chronic stroke patients were allocated into two training groups. Movement-related cortical potentials (MRCPs) were detected using elecroencephalography 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 (BCInon-associative group). Fugl-Meyer motor assessment (FM), 10-m walking speed, foot and hand tapping frequency and the excitability of the corticospinal tract to the target muscle (tibialis anterior (TA)) were quantified. The TA motor evoked potential increased significantly following the BCIassociative intervention, but not for the BCInon-associative group. Fugl-Meyer motor 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. 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.

AB - Brain-computer interfaces (BCIs) have the potential to improve functionality in chronic stoke patients when applied over a large number of sessions. Here, we evaluate 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 hypothesizes that neural assemblies activated in a correlated manner will strengthen synaptic connections. Twenty-two chronic stroke patients were allocated into two training groups. Movement-related cortical potentials (MRCPs) were detected using elecroencephalography 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 (BCInon-associative group). Fugl-Meyer motor assessment (FM), 10-m walking speed, foot and hand tapping frequency and the excitability of the corticospinal tract to the target muscle (tibialis anterior (TA)) were quantified. The TA motor evoked potential increased significantly following the BCIassociative intervention, but not for the BCInon-associative group. Fugl-Meyer motor 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. 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.

U2 - 10.1152/jn.00918.2015

DO - 10.1152/jn.00918.2015

M3 - Journal article

VL - 115

SP - 1410

EP - 1421

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

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