Reliable recording and analysis of MEG-based corticokinematic coherence in the presence of strong magnetic artifacts

OBJECTIVE Corticokinematic coherence (CKC) is the coupling between magnetoencephalographic (MEG) signals and limb kinematics during fast movements. Our objective was to assess the robustness of CKC-based identification of the primary sensorimotor (SM1) cortex of subjects producing strong magnetic artifacts when the MEG signals were cleaned with temporal signal space separation (tSSS). METHODS We recorded MEG during active and passive forefinger movements and during median-nerve stimulation in the following conditions: (1) artifact-free, (2) a magnetic wire attached to the scalp at C3 location, and (3) a magnetic wire attached behind the lower central incisors. Data were pre-processed with tSSS and analyzed using standard CKC methods, somatosensory evoked fields (SEFs), and dipole modeling. RESULT Artifacts were effectively suppressed by tSSS, enabling successful identification of the SM1 cortex in all subjects based on CKC and SEFs. The sources were in artifact conditions ∼5 mm away from the sources identified in artifact-free conditions. CONCLUSION tSSS suppressed artifacts strongly enough to enable reliable identification of the SM1 cortex on the basis of CKC mapping, with localization accuracy comparable to SEF-based mapping. SIGNIFICANCE The results suggest that CKC can be used for SM1 cortex identification and for studies of proprioception even in patients implanted with magnetic material.

[1]  J. R. Baker,et al.  Simultaneous functional magnetic resonance imaging and electrophysiological recording , 1995 .

[2]  V. Jousmäki,et al.  Cardiac artifacts in magnetoencephalogram. , 1996, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[3]  Luca Faes,et al.  Surrogate data analysis for assessing the significance of the coherence function , 2004, IEEE Transactions on Biomedical Engineering.

[4]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[5]  M. D’Esposito,et al.  Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging , 2003, Nature Reviews Neuroscience.

[6]  Evelien Carrette,et al.  Magnetoencephalography in epilepsy patients carrying a vagus nerve stimulator , 2011, Epilepsy Research.

[7]  M. D’Esposito,et al.  Functional magnetic resonance imaging of regional brain activity in patients with intracerebral gliomas: findings and implications for clinical management. , 1996, Neurosurgery.

[8]  S Warach,et al.  Monitoring the patient's EEG during echo planar MRI. , 1993, Electroencephalography and clinical neurophysiology.

[9]  P M Rossini,et al.  Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? , 2004, Brain : a journal of neurology.

[10]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[11]  F E Bloom,et al.  Intrasubject reliability and validity of somatosensory source localization using a large array biomagnetometer. , 1994, Electroencephalography and clinical neurophysiology.

[12]  Naoaki Tanaka,et al.  Clinical applications of magnetoencephalography , 2009, Human brain mapping.

[13]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[14]  S. Taulu,et al.  Presentation of electromagnetic multichannel data: The signal space separation method , 2005 .

[15]  Christopher Nimsky,et al.  Correlation of Sensorimotor Activation with Functional Magnetic Resonance Imaging and Magnetoencephalography in Presurgical Functional Imaging: A Spatial Analysis , 2001, NeuroImage.

[16]  O. Foerster,et al.  THE MOTOR CORTEX IN MAN IN THE LIGHT OF HUGHLINGS JACKSON'S DOCTRINES , 1936 .

[17]  Riitta Hari,et al.  Removal of magnetoencephalographic artifacts with temporal signal‐space separation: Demonstration with single‐trial auditory‐evoked responses , 2009, Human brain mapping.

[18]  M. Bourguignon,et al.  Corticokinematic coherence during active and passive finger movements , 2013, Neuroscience.

[19]  R. Hari,et al.  Magnetoencephalography in the study of human somatosensory cortical processing. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  D. L. Schomer,et al.  Niedermeyer's Electroencephalography: Basic Principles, Clinical Applications, and Related Fields , 2012 .

[21]  Riitta Hari,et al.  Corticokinematic coherence mainly reflects movement-induced proprioceptive feedback , 2015, NeuroImage.

[22]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[23]  Elizabeth W. Pang,et al.  Event-related beamforming: A robust method for presurgical functional mapping using MEG , 2007, Clinical Neurophysiology.

[24]  B. Bourgeois,et al.  Magnetoencephalographic analysis in patients with vagus nerve stimulator. , 2009, Pediatric neurology.

[25]  Geirmund Unsgård,et al.  Preoperative Blood Oxygen Level-dependent Functional Magnetic Resonance Imaging in Patients with Primary Brain Tumors: Clinical Application and Outcome , 2004, Neurosurgery.

[26]  Pavel Sovka,et al.  Approximation of statistical distribution of magnitude squared coherence estimated with segment overlapping , 2007, Signal Process..

[27]  Siu Wing Or,et al.  Dynamic magnetomechanical properties of Terfenol-D/epoxy pseudo 1-3 composites , 2005 .

[28]  Erkki Oja,et al.  Independent component approach to the analysis of EEG and MEG recordings , 2000, IEEE Transactions on Biomedical Engineering.

[29]  A M Amjad,et al.  A framework for the analysis of mixed time series/point process data--theory and application to the study of physiological tremor, single motor unit discharges and electromyograms. , 1995, Progress in biophysics and molecular biology.

[30]  Karl J. Friston,et al.  Optimized beamforming for simultaneous MEG and intracranial local field potential recordings in deep brain stimulation patients , 2010, NeuroImage.

[31]  Riitta Hari,et al.  MEG-compatible pneumatic stimulator to elicit passive finger and toe movements , 2015, NeuroImage.

[32]  H. Steinmetz,et al.  Craniocerebral topography within the international 10-20 system. , 1989, Electroencephalography and clinical neurophysiology.

[33]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[34]  Samu Taulu,et al.  Signal Space Separation Algorithm and Its Application on Suppressing Artifacts Caused by Vagus Nerve Stimulation for Magnetoencephalography Recordings , 2009, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[35]  Mathieu Bourguignon,et al.  Neuronal network coherent with hand kinematics during fast repetitive hand movements , 2012, NeuroImage.

[36]  Jyrki P. Mäkelä,et al.  Effects of subthalamic nucleus stimulation on spontaneous sensorimotor MEG activity in a Parkinsonian patient , 2007 .

[37]  Heidi E Kirsch,et al.  American Clinical Magnetoencephalography Society Clinical Practice Guideline 2: Presurgical Functional Brain Mapping Using Magnetic Evoked Fields* , 2011, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[38]  V. Jousmäki,et al.  Comprehensive Functional Mapping Scheme for Non-Invasive Primary Sensorimotor Cortex Mapping , 2012, Brain Topography.

[39]  O Salonen,et al.  Three‐dimensional integration of brain anatomy and function to facilitate intraoperative navigation around the sensorimotor strip , 2001, Human brain mapping.

[40]  T. Yoshimoto,et al.  Accuracy and Limitation of Functional Magnetic Resonance Imaging for Identification of the Central Sulcus: Comparison with Magnetoencephalography in Patients with Brain Tumors , 1999, NeuroImage.

[41]  Christo Pantev,et al.  Reproducibility and Validity of Neuromagnetic Source Localization Using A Large Array Biomagnetometer , 1991 .

[42]  Antti Korvenoja,et al.  Sensorimotor cortex localization: comparison of magnetoencephalography, functional MR imaging, and intraoperative cortical mapping. , 2006, Radiology.

[43]  Richard C. Burgess,et al.  Utility of temporally-extended signal space separation algorithm for magnetic noise from vagal nerve stimulators , 2013, Clinical Neurophysiology.

[44]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

[45]  Riitta Hari,et al.  Functional motor-cortex mapping using corticokinematic coherence , 2011, NeuroImage.

[46]  Samu Taulu,et al.  Fine tuning the correlation limit of spatio-temporal signal space separation for magnetoencephalography , 2009, Journal of Neuroscience Methods.

[47]  B. W. van Dijk,et al.  Feasibility of clinical Magnetoencephalography (MEG) functional mapping in the presence of dental artefacts , 2013, Clinical Neurophysiology.

[48]  Ludomir Stefańczyk,et al.  Cortical mapping by functional magnetic resonance imaging in patients with brain tumors , 2005, European Radiology.

[49]  A. Bartsch,et al.  Diagnostic functional MRI: Illustrated clinical applications and decision‐making , 2006, Journal of magnetic resonance imaging : JMRI.

[50]  G. Curio,et al.  The effect of artifact rejection by signal-space projection on source localization accuracy in MEG measurements , 1999, IEEE Transactions on Biomedical Engineering.

[51]  K Willmes,et al.  Functional MRI for presurgical planning: problems, artefacts, and solution strategies , 2001, Journal of neurology, neurosurgery, and psychiatry.

[52]  Riitta Hari,et al.  Coherence between magnetoencephalography and hand-action-related acceleration, force, pressure, and electromyogram , 2013, NeuroImage.

[53]  Charles A. Pelizzari,et al.  Noninvasive identification of human central sulcus: a comparison of gyral morphology, functional MRI, dipole localization, and direct cortical mapping , 2003, NeuroImage.