Natalie Mrachacz-Kersting

Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity

Key points  •  Here we use the naturally generated brain activation when a person imagines a simple movement and combine this with the afferent inflow that would be generated had the movement been performed rather than imagined. •  We show that the excitability of the neural projections connecting the relevant brain areas to the target muscle is increased only when the afferent inflow arrives during the highest activation phase. •  Furthermore, the changes are specific to the task and the neural connections between the brain and muscle involved in the task. •  This novel intervention will open up the possibilities to alter afferent‐generated feedback depending on the demands of the movement to be performed.

Enhanced Low-Latency Detection of Motor Intention From EEG for Closed-Loop Brain-Computer Interface Applications

In recent years, the detection of voluntary motor intentions from electroencephalogram (EEG) has been used for triggering external devices in closed-loop brain-computer interface (BCI) research. Movement-related cortical potentials (MRCP), a type of slow cortical potentials, have been recently used for detection. In order to enhance the efficacy of closed-loop BCI systems based on MRCPs, a manifold method called Locality Preserving Projection, followed by a linear discriminant analysis (LDA) classifier (LPP-LDA) is proposed in this paper to detect MRCPs from scalp EEG in real time. In an online experiment on nine healthy subjects, LPP-LDA statistically outperformed the classic matched filter approach with greater true positive rate (79 ± 11% versus 68 ± 10%; p = 0.007) and less false positives (1.4 ± 0.8/min versus 2.3 ± 1.1/min; p = 0.016). Moreover, the proposed system performed detections with significantly shorter latency (315 ± 165 ms versus 460 ± 123 ms; p = 0.013), which is a fundamental characteristics to induce neuroplastic changes in closed-loop BCIs, following the Hebbian principle. In conclusion, the proposed system works as a generic brain switch, with high accuracy, low latency, and easy online implementation. It can thus be used as a fundamental element of BCI systems for neuromodulation and motor function rehabilitation.

Peripheral Electrical Stimulation Triggered by Self-Paced Detection of Motor Intention Enhances Motor Evoked Potentials

This paper proposes the development and experimental tests of a self-paced asynchronous brain-computer interfacing (BCI) system that detects movement related cortical potentials (MRCPs) produced during motor imagination of ankle dorsiflexion and triggers peripheral electrical stimulations timed with the occurrence of MRCPs to induce corticospinal plasticity. MRCPs were detected online from EEG signals in eight healthy subjects with a true positive rate (TPR) of 67.15±7.87% and false positive rate (FPR) of 22.05±9.07%. The excitability of the cortical projection to the target muscle (tibialis anterior) was assessed before and after the intervention through motor evoked potentials (MEP) using transcranial magnetic stimulation (TMS). The peak of the evoked potential significantly (P=0.02) increased after the BCI intervention by 53±43% (relative to preintervention measure), although the spinal excitability (tested by stretch reflexes) did not change. These results demonstrate for the first time that it is possible to alter the corticospinal projections to the tibialis anterior muscle by using an asynchronous BCI system based on online motor imagination that triggered peripheral stimulation. This type of repetitive proprioceptive feedback training based on self-generated brain signal decoding may be a requirement for purposeful skill acquisition in intact humans and in the rehabilitation of persons with brain damage.

A Closed-Loop Brain–Computer Interface Triggering an Active Ankle–Foot Orthosis for Inducing Cortical Neural Plasticity

In this paper, we present a brain-computer interface (BCI) driven motorized ankle-foot orthosis (BCI-MAFO), intended for stroke rehabilitation, and we demonstrate its efficacy in inducing cortical neuroplasticity in healthy subjects with a short intervention procedure (~15 min). This system detects imaginary dorsiflexion movements within a short latency from scalp EEG through the analysis of movement-related cortical potentials (MRCPs). A manifold-based method, called locality preserving projection, detected the motor imagery online with a true positive rate of 73.0 ± 10.3%. Each detection triggered the MAFO to elicit a passive dorsiflexion. In nine healthy subjects, the size of the motorevoked potential (MEP) elicited by transcranial magnetic stimulation increased significantly immediately following and 30 min after the cessation of this BCI-MAFO intervention for ~15 min (p = 0.009 and p <; 0.001, respectively), indicating neural plasticity. In four subjects, the size of the short latency stretch reflex component did not change following the intervention, suggesting that the site of the induced plasticity was cortical. All but one subject also performed two control conditions where they either imagined only or where the MAFO was randomly triggered. Both of these control conditions resulted in no significant changes in MEP size (p = 0.38 and p = 0.15). The proposed system provides a fast and effective approach for inducing cortical plasticity through BCI and has potential in motor function rehabilitation following stroke.

A brain–computer interface for single-trial detection of gait initiation from movement related cortical potentials

OBJECTIVE Applications of brain-computer interfacing (BCI) in neurorehabilitation have received increasing attention. The intention to perform a motor task can be detected from scalp EEG and used to control rehabilitation devices, resulting in a patient-driven rehabilitation paradigm. In this study, we present and validate a BCI system for detection of gait initiation using movement related cortical potentials (MRCP). METHODS The templates of MRCP were extracted from 9-channel scalp EEG during gait initiation in 9 healthy subjects. Independent component analysis (ICA) was used to remove artifacts, and the Laplacian spatial filter was applied to enhance the signal-to-noise ratio of MRCP. Following these pre-processing steps, a matched filter was used to perform single-trial detection of gait initiation. RESULTS ICA preprocessing was shown to significantly improve the detection performance. With ICA preprocessing, across all subjects, the true positive rate (TPR) of the detection was 76.9±8.97%, and the false positive rate was 2.93±1.09 per minute. CONCLUSION The results demonstrate the feasibility of detecting the intention of gait initiation from EEG signals, on a single trial basis. SIGNIFICANCE The results are important for the development of new gait rehabilitation strategies, either for recovery/replacement of function or for neuromodulation.

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

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.

Detection and classification of movement-related cortical potentials associated with task force and speed

OBJECTIVE In this study, the objective was to detect movement intentions and extract different levels of force and speed of the intended movement from scalp electroencephalography (EEG). We then estimated the performance of the closed loop system. APPROACH Cued movements were detected from continuous EEG recordings using a template of the initial phase of the movement-related cortical potential in 12 healthy subjects. The temporal features, extracted from the movement intention, were classified with an optimized support vector machine. The system performance was evaluated when combining detection with classification. MAIN RESULTS The system detected 81% of the movements and correctly classified 75 ± 9% and 80 ± 10% of these at the point of detection when varying the force and speed, respectively. When the detector was combined with the classifier, the system detected and correctly classified 64 ± 13% and 67 ± 13% of these movements. The system detected and incorrectly classified 21 ± 7% and 16 ± 9% of the movements. The movements were detected 317 ± 73 ms before the movement onset. SIGNIFICANCE The results indicate that it is possible to detect movement intentions with limited latencies, and extract and classify different levels of force and speed, which may be combined with assistive technologies for patient-driven neurorehabilitation.

Short-Latency Crossed Inhibitory Responses in the Human Soleus Muscle

Even though interlimb coordination is critical in bipedal locomotion, the role of muscle afferent mediated feedback is unknown. The aim of this study was to establish if ipsilateral muscle generated afferent feedback can influence contralateral muscle activation patterns in the human lower limb and to elucidate the mechanisms involved. The effect of ipsilateral tibial nerve stimulation on contralateral soleus (cSOL) responses were quantified. Three interventions were investigated, 1) electrical stimulation applied to the tibial nerve at stimulation intensities from 0 to 100% of maximal M-wave (M-max) with the cSOL contracted from 5 to 15% of maximal voluntary contraction (MVC) and 15 to 30% MVC, 2) ispsilateral tibial nerve stimulation at 75% M-max prior to, during, and following the application of ischemia to the ipsilateral thigh. 3) Electrical stimulation applied to the ipsilateral sural (SuN) and medial plantar nerves at stimulation intensities from 1 to 3 times perceptual threshold. A short-latency depression in the cSOL electromyogram (EMG; onset: 37-41 ms) was observed following ipsilateral tibial nerve stimulation. The magnitude of this depression increased (P = 0.0005 and P = 0.000001) with increasing stimulus intensities. Ischemia delayed the time of the minimum of the cSOL depression (P = 0.04). SuN and medial plantar nerve stimulation evoked a longer latency depression [average; 91.2 ms (SuN); 142 ms (medial plantar nerve)] and therefore do not contribute to the response. This is the first study to demonstrate a short-latency depression in the cSOL following ipsilateral tibial nerve stimulation. Due to its short latency, the response is spinally mediated. The involvement of crossed spinal interneurons receiving input from low-threshold muscle afferents is discussed.

Phase Modulation of the Short-Latency Crossed Spinal Response in the Human Soleus Muscle

Short-latency spinally mediated interlimb reflex pathways were recently reported between the left and right soleus muscles in the human lower-limb during sitting. The aim of the current study was to establish if these pathways were observed during a functional motor task such as human gait and modulated by the gait cycle phase and/or electrical stimulation intensity. The second aim was to elucidate on the afferents involved. Two interventions were investigated. First was ipsilateral tibial nerve (iTN) stimulation at motor threshold (MT), 35% of the maximal peak-to-peak M-wave(M-Max) and 85% M-Max (85M-Max) with stimuli applied at 60%, 70%, 80%, 90%, and 100%of the gait cycle of the ipsilateral leg. Second was ipsilateral sural nerve (SuN) and medial plantar nerve (MpN) stimulation at 1, 2, and 3X perceptual threshold at 90% of the gait cycle [corrected]. The root mean squared (RMS) of the contralateral soleus (cSOL) responses were analyzed in a time window, 40-55 ms (or 45-60 ms for subjects >50 y/o) following iTN stimulation. The most consistent responses occurred at 90 and 100% of the gait cycle at higher stimulation intensities of the iTN. Significantly inhibitory responses (P = 0.006) were reported at 60 versus 80% (P = 0.03), 90% (P = 0.006), and 100% (P = 0.002) and 70 versus 90% (P = 0.02) and 100% (P = 0.009) of the gait cycle at 85M-Max. The responses became more inhibitory with increasing stimulation intensities at 80% (P = 0.01), 90% (P = 0.001), and 100% (P = 0.004) of the gait cycle. Stimulation of the MpN and SuN at all stimulation intensities demonstrated no short-latency responses. Therefore, it is unlikely that afferents within these nerves contribute to the response. This is the first study to show short-latency spinally mediated responses in the cSOL following iTN stimulation, during walking. It provides evidence for a new spinal pathway contributing to motor control and demonstrates that the response likely has functional relevance.

Interlimb communication to the knee flexors during walking in humans

•  Following unexpected ipsilateral knee extension joint rotations applied during the late stance phase of the gait cycle in humans, a crossed reflex response was observed in the contralateral biceps femoris (cBF) muscle with a mean onset latency of 76 ms. •  Transcranial magnetic and electrical stimulation applied to the primary motor cortex revealed that a transcortical pathway probably contributes to the cBF response. •  We hypothesize that the cBF response signifies a preparation of the contralateral leg for early load bearing, helping the body to maintain dynamic stability during walking. •  This is the first study to show that a transcortical pathway contributes to an interlimb reflex in upper leg muscles. The transcortical nature of the response may allow for more adaptable responses than purely spinally mediated reflexes due to integration with other sensory information.