Signal processing methods for reducing artifacts in microelectrode brain recordings caused by functional electrical stimulation

OBJECTIVE Functional electrical stimulation (FES) is a promising technology for restoring movement to paralyzed limbs. Intracortical brain-computer interfaces (iBCIs) have enabled intuitive control over virtual and robotic movements, and more recently over upper extremity FES neuroprostheses. However, electrical stimulation of muscles creates artifacts in intracortical microelectrode recordings that could degrade iBCI performance. Here, we investigate methods for reducing the cortically recorded artifacts that result from peripheral electrical stimulation. APPROACH One participant in the BrainGate2 pilot clinical trial had two intracortical microelectrode arrays placed in the motor cortex, and thirty-six stimulating intramuscular electrodes placed in the muscles of the contralateral limb. We characterized intracortically recorded electrical artifacts during both intramuscular and surface stimulation. We compared the performance of three artifact reduction methods: blanking, common average reference (CAR) and linear regression reference (LRR), which creates channel-specific reference signals, composed of weighted sums of other channels. MAIN RESULTS Electrical artifacts resulting from surface stimulation were 175  ×  larger than baseline neural recordings (which were 110 µV peak-to-peak), while intramuscular stimulation artifacts were only 4  ×  larger. The artifact waveforms were highly consistent across electrodes within each array. Application of LRR reduced artifact magnitudes to less than 10 µV and largely preserved the original neural feature values used for decoding. Unmitigated stimulation artifacts decreased iBCI decoding performance, but performance was almost completely recovered using LRR, which outperformed CAR and blanking and extracted useful neural information during stimulation artifact periods. SIGNIFICANCE The LRR method was effective at reducing electrical artifacts resulting from both intramuscular and surface FES, and almost completely restored iBCI decoding performance (>90% recovery for surface stimulation and full recovery for intramuscular stimulation). The results demonstrate that FES-induced artifacts can be easily mitigated in FES  +  iBCI systems by using LRR for artifact reduction, and suggest that the LRR method may also be useful in other noise reduction applications.

[1]  Hannes Bleuler,et al.  Active tactile exploration enabled by a brain-machine-brain interface , 2011, Nature.

[2]  A. Schwartz,et al.  High-performance neuroprosthetic control by an individual with tetraplegia , 2013, The Lancet.

[3]  Thierry Keller,et al.  Detection and removal of stimulation artifacts in electroencephalogram recordings , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[4]  Marjorie E. Anderson,et al.  Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. , 2003, Journal of neurophysiology.

[5]  Alexander R. Kent,et al.  Recording evoked potentials during deep brain stimulation: development and validation of instrumentation to suppress the stimulus artefact , 2012, Journal of neural engineering.

[6]  James B. Fallon,et al.  A novel stimulus artifact removal technique for high-rate electrical stimulation , 2008, Journal of Neuroscience Methods.

[7]  Andrew S. Whitford,et al.  Cortical control of a prosthetic arm for self-feeding , 2008, Nature.

[8]  Christine H. Blabe,et al.  Signal-independent noise in intracortical brain–computer interfaces causes movement time properties inconsistent with Fitts’ law , 2017, Journal of neural engineering.

[9]  J. A. Freeman An electronic stimulus artifact suppressor. , 1971, Electroencephalography and Clinical Neurophysiology.

[10]  Nicolas Y. Masse,et al.  Neural Point-and-Click Communication by a Person With Incomplete Locked-In Syndrome , 2015, Neurorehabilitation and neural repair.

[11]  Steve M. Potter,et al.  Real-time multi-channel stimulus artifact suppression by local curve fitting , 2002, Journal of Neuroscience Methods.

[12]  P. G Musial,et al.  Signal-to-noise ratio improvement in multiple electrode recording , 2002, Journal of Neuroscience Methods.

[13]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[14]  Michael L. Boninger,et al.  Intracortical Microstimulation as a Feedback Source for Brain-Computer Interface Users , 2017, Brain-Computer Interface Research.

[15]  Michael J. Black,et al.  Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array , 2011 .

[16]  J R Wolpaw,et al.  Spatial filter selection for EEG-based communication. , 1997, Electroencephalography and clinical neurophysiology.

[17]  Bertrand Delgutte,et al.  Desynchronization of electrically evoked auditory-nerve activity by high-frequency pulse trains of long duration. , 2003, The Journal of the Acoustical Society of America.

[18]  P. Brown,et al.  Adaptive Deep Brain Stimulation In Advanced Parkinson Disease , 2013, Annals of neurology.

[19]  Spencer Kellis,et al.  A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback , 2014, Journal of neural engineering.

[20]  Patrick E. Crago,et al.  Stimulus artifact removal in EMG from muscles adjacent to stimulated muscles , 1996, Journal of Neuroscience Methods.

[21]  Nicolas Y. Masse,et al.  Reach and grasp by people with tetraplegia using a neurally controlled robotic arm , 2012, Nature.

[22]  Wolfgang Rosenstiel,et al.  Coupling BCI and cortical stimulation for brain-state-dependent stimulation: methods for spectral estimation in the presence of stimulation after-effects , 2012, Front. Neural Circuits.

[23]  Nicholas V. Annetta,et al.  Restoring cortical control of functional movement in a human with quadriplegia , 2016, Nature.

[24]  Nicolas Y. Masse,et al.  Virtual typing by people with tetraplegia using a self-calibrating intracortical brain-computer interface , 2015, Science Translational Medicine.

[25]  Kush Paul,et al.  Spectral cancellation of microstimulation artifact for simultaneous neural recording in situ , 2003, IEEE Transactions on Biomedical Engineering.

[26]  P. H. Peckham,et al.  Restoration of functional control by electrical stimulation in the upper extremity of the quadriplegic patient. , 1988, The Journal of bone and joint surgery. American volume.

[27]  Chethan Pandarinath,et al.  Feedback control policies employed by people using intracortical brain–computer interfaces , 2017, Journal of neural engineering.

[28]  Derek T O'Keeffe,et al.  Stimulus artifact removal using a software-based two-stage peak detection algorithm , 2001, Journal of Neuroscience Methods.

[29]  Takao Hashimoto,et al.  A template subtraction method for stimulus artifact removal in high-frequency deep brain stimulation , 2002, Journal of Neuroscience Methods.

[30]  Francis R. Willett,et al.  High performance communication by people with paralysis using an intracortical brain-computer interface , 2017, eLife.

[31]  Julie G Pilitsis,et al.  Effect of intraoperative subthalamic nucleus DBS on human single-unit activity in the ipsilateral and contralateral subthalamic nucleus. , 2012, Journal of neurosurgery.

[32]  A. Priori,et al.  An electronic device for artefact suppression in human local field potential recordings during deep brain stimulation , 2007, Journal of neural engineering.

[33]  Mikhail A Lebedev,et al.  Virtual Active Touch Using Randomly Patterned Intracortical Microstimulation , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[34]  Francis R. Willett,et al.  Restoration of reaching and grasping in a person with tetraplegia through brain-controlled muscle stimulation: a proof-of-concept demonstration , 2017, The Lancet.

[35]  Kevin L Kilgore,et al.  Implanted neuroprosthesis for restoring arm and hand function in people with high level tetraplegia. , 2014, Archives of physical medicine and rehabilitation.