Online detection of amplitude modulation of motor-related EEG desynchronization using a lock-in amplifier: Comparison with a fast Fourier transform, a continuous wavelet transform, and an autoregressive algorithm

BACKGROUND Neurofeedback of event-related desynchronization (ERD) in electroencephalograms (EEG) of the sensorimotor cortex (SM1) using a brain-computer interface (BCI) paradigm is a powerful tool to promote motor recovery from post-stroke hemiplegia. However, the feedback delay attenuates the degree of motor learning and neural plasticity. NEW METHOD The present study aimed to shorten the delay time to estimate amplitude modulation of the motor-imagery-related alpha and beta SM1-ERD using a lock-in amplifier (LIA) algorithm. The delay time was evaluated by calculating the value of the maximal correlation coefficient (MCC) between the time-series trace of ERDs extracted by the online LIA algorithm and those identified by an offline algorithm with the Hilbert transform (HT). RESULTS The MCC and delay values used to estimate the ERDs calculated by the LIA were 0.89±0.032 and 200±9.49ms, respectively. COMPARISON WITH EXISTING METHOD(S) The delay time and MCC values were significantly improved compared with those calculated by the conventional fast Fourier transformation (FFT), continuous Wavelet transformation (CWT), and autoregressive (AR) algorithms. Moreover, the coefficients of variance of the delay time and MCC values across trials were significantly lower in the LIA compared with the FFT, CWT, and AR algorithms. CONCLUSIONS These results indicate that the LIA improved the detection delay, accuracy, and stability for estimating amplitude modulation of motor-related SM1-ERD. This would be beneficial for BCI paradigms to facilitate neurorehabilitation in patients with motor deficits.

[1]  Michael L. Boninger,et al.  Brain computer interface learning for systems based on electrocorticography and intracortical microelectrode arrays , 2015, Front. Integr. Neurosci..

[2]  Cuntai Guan,et al.  A Large Clinical Study on the Ability of Stroke Patients to Use an EEG-Based Motor Imagery Brain-Computer Interface , 2011, Clinical EEG and neuroscience.

[3]  C. Braun,et al.  Chronic stroke recovery after combined BCI training and physiotherapy: a case report. , 2011, Psychophysiology.

[4]  Eric Leuthardt,et al.  Decoding covert spatial attention using electrocorticographic (ECoG) signals in humans , 2012, NeuroImage.

[5]  D. Tucker,et al.  Scalp electrode impedance, infection risk, and EEG data quality , 2001, Clinical Neurophysiology.

[6]  J. Ushiba,et al.  Event-related desynchronization reflects downregulation of intracortical inhibition in human primary motor cortex. , 2013, Journal of neurophysiology.

[7]  Monica A. Perez,et al.  Neural interface technology for rehabilitation: exploiting and promoting neuroplasticity. , 2010, Physical medicine and rehabilitation clinics of North America.

[8]  J. Wolpaw,et al.  Brain–computer interfaces in neurological rehabilitation , 2008, The Lancet Neurology.

[9]  Abdulhamit Subasi,et al.  EEG signal classification using wavelet feature extraction and a mixture of expert model , 2007, Expert Syst. Appl..

[10]  Gernot R. Müller-Putz,et al.  Comparison of DFT and lock-in amplifier features and search for optimal electrode positions in SSVEP-based BCI , 2008, Journal of Neuroscience Methods.

[11]  G. Prasad,et al.  Applying a brain-computer interface to support motor imagery practice in people with stroke for upper limb recovery: a feasibility study , 2010, Journal of NeuroEngineering and Rehabilitation.

[12]  S. Soekadar,et al.  Brain-machine interfaces for rehabilitation of poststroke hemiplegia. , 2016, Progress in brain research.

[13]  B. M. de Jong,et al.  Iterative versus Filtered Backprojection Reconstruction for Statistical Parametric Mapping of PET Activation Measurements: A Comparative Case Study , 2002, NeuroImage.

[14]  Hiroshi Imamizu,et al.  Physical delay but not subjective delay determines learning rate in prism adaptation , 2010, Experimental Brain Research.

[15]  L. Cohen,et al.  Brain–machine interface in chronic stroke rehabilitation: A controlled study , 2013, Annals of neurology.

[16]  Akio Kimura,et al.  Brain-computer interface with somatosensory feedback improves functional recovery from severe hemiplegia due to chronic stroke , 2014, Front. Neuroeng..

[17]  J. Ushiba,et al.  Sensorimotor event-related desynchronization represents the excitability of human spinal motoneurons , 2015, Neuroscience.

[18]  J. Ushiba,et al.  Effects of neurofeedback training with an electroencephalogram-based brain-computer interface for hand paralysis in patients with chronic stroke: a preliminary case series study. , 2011, Journal of rehabilitation medicine.

[19]  J. Burg THE RELATIONSHIP BETWEEN MAXIMUM ENTROPY SPECTRA AND MAXIMUM LIKELIHOOD SPECTRA , 1972 .

[20]  Piet M. T. Broersen,et al.  Autoregressive spectral estimation by application of the Burg algorithm to irregularly sampled data , 2002, IEEE Trans. Instrum. Meas..

[21]  J. Ushiba,et al.  Daily training with realistic visual feedback improves reproducibility of event-related desynchronisation following hand motor imagery , 2013, Clinical Neurophysiology.

[22]  Jon F. Claerbout,et al.  Fundamentals of Geophysical Data Processing: With Applications to Petroleum Prospecting , 1985 .

[23]  M. Feldman Hilbert transform in vibration analysis , 2011 .

[24]  Mark E. Dohring,et al.  Feasibility of a New Application of Noninvasive Brain Computer Interface (BCI): A Case Study of Training for Recovery of Volitional Motor Control After Stroke , 2009, Journal of neurologic physical therapy : JNPT.

[25]  Mathias Hegele,et al.  Feedback delay attenuates implicit but facilitates explicit adjustments to a visuomotor rotation , 2017, Neurobiology of Learning and Memory.

[26]  J. Kalaska,et al.  Learning to Move Machines with the Mind , 2022 .

[27]  Walter C. Michels,et al.  A Pentode Lock‐In Amplifier of High Frequency Selectivity , 1941 .

[28]  Ruimin Wang,et al.  Classification of Four-Class Motor Imagery Employing Single-Channel Electroencephalography , 2014, PloS one.

[29]  Amjed S. Al-Fahoum,et al.  Methods of EEG Signal Features Extraction Using Linear Analysis in Frequency and Time-Frequency Domains , 2014, ISRN neuroscience.

[30]  S. Kitazawa,et al.  Effects of delayed visual information on the rate and amount of prism adaptation in the human , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Akio Kimura,et al.  Multimodal Sensory Feedback Associated with Motor Attempts Alters BOLD Responses to Paralyzed Hand Movement in Chronic Stroke Patients , 2014, Brain Topography.

[32]  Minho Lee,et al.  Time-frequency analysis of band-limited EEG with BMFLC and Kalman filter for BCI applications , 2013, Journal of NeuroEngineering and Rehabilitation.

[33]  D. Nozaki,et al.  Adaptation to Visual Feedback Delay Influences Visuomotor Learning , 2012, PloS one.

[34]  Elif Derya Übeyli,et al.  Wavelet transform feature extraction from human PPG, ECG, and EEG signal responses to ELF PEMF exposures: A pilot study , 2008, Digit. Signal Process..

[35]  Akio Kimura,et al.  Efficacy of brain-computer interface-driven neuromuscular electrical stimulation for chronic paresis after stroke. , 2014, Journal of rehabilitation medicine.

[36]  C. Gerloff,et al.  Inhibitory control of acquired motor programmes in the human brain. , 2002, Brain : a journal of neurology.

[37]  J Kiessling,et al.  Frequency-following potentials in man by lock-in technique. , 1981, Electroencephalography and clinical neurophysiology.

[38]  Cuntai Guan,et al.  A Randomized Controlled Trial of EEG-Based Motor Imagery Brain-Computer Interface Robotic Rehabilitation for Stroke , 2015, Clinical EEG and neuroscience.

[39]  Qiang Ji,et al.  Decoding onset and direction of movements using Electrocorticographic (ECoG) signals in humans , 2012, Front. Neuroeng..

[40]  C. Braun,et al.  Combination of Brain-Computer Interface Training and Goal-Directed Physical Therapy in Chronic Stroke: A Case Report , 2010, Neurorehabilitation and neural repair.

[41]  S. Schacham,et al.  Detection and measurement of steady-state evoked potentials in real-time using a lock-in amplifier. Technical note. , 1985, Journal of neurosurgery.

[42]  Bernadette C. M. van Wijk,et al.  Movement-related beta oscillations show high intra-individual reliability , 2017, NeuroImage.

[43]  Dean J. Krusienski,et al.  Value of amplitude, phase, and coherence features for a sensorimotor rhythm-based brain–computer interface , 2012, Brain Research Bulletin.