Assessment and elimination of the effects of head movement on MEG resting-state measures of oscillatory brain activity

Abstract Magnetoencephalography (MEG) is increasingly being used to study brain function because of its excellent temporal resolution and its direct association with brain activity at the neuronal level. One possible cause of error in the analysis of MEG data comes from the fact that participants, even MEG‐experienced ones, move their head in the MEG system. Head movement can cause source localization errors during the analysis of MEG data, which can result in the appearance of source variability that does not reflect brain activity. The MEG community places great importance in eliminating this source of possible errors as is evident, for example, by recent efforts to develop head casts that limit head movement in the MEG system. In this work we use software tools to identify, assess and eliminate from the analysis of MEG data any possible correlations between head movement in the MEG system and widely‐used measures of brain activity derived from MEG resting‐state recordings. The measures of brain activity we study are a) the Hilbert‐transform derived amplitude envelope of the beamformer time series and b) functional networks; both measures derived by MEG resting‐state recordings. Ten‐minute MEG resting‐state recordings were performed on healthy participants, with head position continuously recorded. The sources of the measured magnetic signals were localized via beamformer spatial filtering. Temporal independent component analysis was subsequently used to derive resting‐state networks. Significant correlations were observed between the beamformer envelope time series and head movement. The correlations were substantially reduced, and in some cases eliminated, after a participant‐specific temporal high‐pass filter was applied to those time series. Regressing the head movement metrics out of the beamformer envelope time series had an even stronger effect in reducing these correlations. Correlation trends were also observed between head movement and the activation time series of the default‐mode and frontal networks. Regressing the head movement metrics out of the beamformer envelope time series completely eliminated these correlations. Additionally, applying the head movement correction resulted in changes in the network spatial maps for the visual and sensorimotor networks. Our results a) show that the results of MEG resting‐state studies that use the above‐mentioned analysis methods are confounded by head movement effects, b) suggest that regressing the head movement metrics out of the beamformer envelope time series is a necessary step to be added to these analyses, in order to eliminate the effect that head movement has on the amplitude envelope of beamformer time series and the network time series and c) highlight changes in the connectivity spatial maps when head movement correction is applied. Graphical abstract Symbol. No caption available. HighlightsHead movement effects on MEG resting‐state measures of brain activity are evaluated.Regressing head movement metrics out of beamformer envelope time series is essential.Regressing head movement metrics out of network activation time series is essential.Regressing out head movement metrics changes some spatial network connectivity maps.

[1]  Swathi P. Iyer,et al.  Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data , 2012, Front. Syst. Neurosci..

[2]  Richard Coppola,et al.  Group differences in MEG-ICA derived resting state networks: Application to major depressive disorder , 2015, NeuroImage.

[3]  G. Sandini,et al.  Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. , 2009, Brain : a journal of neurology.

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

[5]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[6]  Khalid Hamandi,et al.  Resting‐state oscillatory dynamics in sensorimotor cortex in benign epilepsy with centro‐temporal spikes and typical brain development , 2015, Human brain mapping.

[7]  S. Rombouts,et al.  Loss of ‘Small-World’ Networks in Alzheimer's Disease: Graph Analysis of fMRI Resting-State Functional Connectivity , 2010, PloS one.

[8]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

[9]  Yong He,et al.  Addressing head motion dependencies for small-world topologies in functional connectomics , 2013, Front. Hum. Neurosci..

[10]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[11]  M. Siegel,et al.  A framework for local cortical oscillation patterns , 2011, Trends in Cognitive Sciences.

[12]  M. Filippi,et al.  Changes of brain resting state functional connectivity predict the persistence of cognitive rehabilitation effects in patients with multiple sclerosis , 2014, Multiple sclerosis.

[13]  Kevin Murphy,et al.  Resting-state fMRI confounds and cleanup , 2013, NeuroImage.

[14]  Winfried Schlee,et al.  Resting-state slow wave power, healthy aging and cognitive performance , 2014, Scientific Reports.

[15]  Mark W. Woolrich,et al.  Using variance information in magnetoencephalography measures of functional connectivity , 2013, NeuroImage.

[16]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[17]  Matteo Fraschini,et al.  Changes in MEG resting-state networks are related to cognitive decline in type 1 diabetes mellitus patients , 2014, NeuroImage: Clinical.

[18]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[19]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[20]  Panagiotis G. Simos,et al.  Altered temporal correlations in resting-state connectivity fluctuations in children with reading difficulties detected via MEG , 2013, NeuroImage.

[21]  Mark W. Woolrich,et al.  How reliable are MEG resting-state connectivity metrics? , 2016, NeuroImage.

[22]  Aapo Hyvärinen,et al.  Independent component analysis of short-time Fourier transforms for spontaneous EEG/MEG analysis , 2010, NeuroImage.

[23]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[24]  P. Peigneux,et al.  Inter- and Intra-Subject Variability of Neuromagnetic Resting State Networks , 2014, Brain Topography.

[25]  Cornelis J. Stam,et al.  Magnetoencephalographic evaluation of resting-state functional connectivity in Alzheimer's disease , 2006, NeuroImage.

[26]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

[27]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[28]  K. Uutela,et al.  Detecting and Correcting for Head Movements in Neuromagnetic Measurements , 2001, NeuroImage.

[29]  Robert Oostenveld,et al.  Online and offline tools for head movement compensation in MEG , 2013, NeuroImage.

[30]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[31]  Karl J. Friston,et al.  Broadband Cortical Desynchronization Underlies the Human Psychedelic State , 2013, The Journal of Neuroscience.

[32]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[33]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  Lars T. Westlye,et al.  Network-specific effects of age and in-scanner subject motion: A resting-state fMRI study of 238 healthy adults , 2012, NeuroImage.

[35]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[36]  Yong Liu,et al.  Disrupted Small-World Brain Networks in Moderate Alzheimer's Disease: A Resting-State fMRI Study , 2012, PloS one.

[37]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[38]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[39]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

[40]  Antoine Lutti,et al.  High precision anatomy for MEG , 2014, NeuroImage.

[41]  Seppo P. Ahlfors,et al.  Head movements of children in MEG: Quantification, effects on source estimation, and compensation , 2008, NeuroImage.