A wavelet method for modeling and despiking motion artifacts from resting-state fMRI time series

The impact of in-scanner head movement on functional magnetic resonance imaging (fMRI) signals has long been established as undesirable. These effects have been traditionally corrected by methods such as linear regression of head movement parameters. However, a number of recent independent studies have demonstrated that these techniques are insufficient to remove motion confounds, and that even small movements can spuriously bias estimates of functional connectivity. Here we propose a new data-driven, spatially-adaptive, wavelet-based method for identifying, modeling, and removing non-stationary events in fMRI time series, caused by head movement, without the need for data scrubbing. This method involves the addition of just one extra step, the Wavelet Despike, in standard pre-processing pipelines. With this method, we demonstrate robust removal of a range of different motion artifacts and motion-related biases including distance-dependent connectivity artifacts, at a group and single-subject level, using a range of previously published and new diagnostic measures. The Wavelet Despike is able to accommodate the substantial spatial and temporal heterogeneity of motion artifacts and can consequently remove a range of high and low frequency artifacts from fMRI time series, that may be linearly or non-linearly related to physical movements. Our methods are demonstrated by the analysis of three cohorts of resting-state fMRI data, including two high-motion datasets: a previously published dataset on children (N = 22) and a new dataset on adults with stimulant drug dependence (N = 40). We conclude that there is a real risk of motion-related bias in connectivity analysis of fMRI data, but that this risk is generally manageable, by effective time series denoising strategies designed to attenuate synchronized signal transients induced by abrupt head movements. The Wavelet Despiking software described in this article is freely available for download at www.brainwavelet.org.

[1]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[2]  M. Fukunaga,et al.  Sources of functional magnetic resonance imaging signal fluctuations in the human brain at rest: a 7 T study. , 2009, Magnetic resonance imaging.

[3]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[4]  J. Hajnal,et al.  Artifacts due to stimulus correlated motion in functional imaging of the brain , 1994, Magnetic resonance in medicine.

[5]  Catie Chang,et al.  Relationship between respiration, end-tidal CO2, and BOLD signals in resting-state fMRI , 2009, NeuroImage.

[6]  Marko Wilke,et al.  An alternative approach towards assessing and accounting for individual motion in fMRI timeseries , 2012, NeuroImage.

[7]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[8]  Hang Joon Jo,et al.  Effective Preprocessing Procedures Virtually Eliminate Distance-Dependent Motion Artifacts in Resting State FMRI , 2013, J. Appl. Math..

[9]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.

[10]  Ingrid Daubechies,et al.  Ten Lectures on Wavelets , 1992 .

[11]  D. Norris,et al.  BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: Parallel‐acquired inhomogeneity‐desensitized fMRI , 2006, Magnetic resonance in medicine.

[12]  S. Mallat A wavelet tour of signal processing , 1998 .

[13]  E. Bullmore,et al.  Fractal connectivity of long-memory networks. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  A. Snyder,et al.  Longitudinal analysis of neural network development in preterm infants. , 2010, Cerebral cortex.

[15]  Simon B. Eickhoff,et al.  An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data , 2013, NeuroImage.

[16]  Abraham Z. Snyder,et al.  Steps toward optimizing motion artifact removal in functional connectivity MRI; a reply to Carp , 2013, NeuroImage.

[17]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[18]  J. Polimeni,et al.  Blipped‐controlled aliasing in parallel imaging for simultaneous multislice echo planar imaging with reduced g‐factor penalty , 2012, Magnetic resonance in medicine.

[19]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[20]  Tom Johnstone,et al.  Motion correction and the use of motion covariates in multiple‐subject fMRI analysis , 2006, Human brain mapping.

[21]  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.

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

[23]  Joshua Carp,et al.  Optimizing the order of operations for movement scrubbing: Comment on Power et al. , 2013, NeuroImage.

[24]  Wen-Ming Luh,et al.  Differentiating BOLD and non-BOLD signals in fMRI time series using multi-echo EPI , 2012, NeuroImage.

[25]  Daniel P. Kennedy,et al.  Largely typical patterns of resting-state functional connectivity in high-functioning adults with autism. , 2014, Cerebral cortex.

[26]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

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

[28]  E. Bullmore,et al.  Methods for diagnosis and treatment of stimulus‐correlated motion in generic brain activation studies using fMRI , 1999, Human brain mapping.

[29]  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.

[30]  A. Walden,et al.  Wavelet Methods for Time Series Analysis , 2000 .

[31]  E. Bullmore,et al.  Statistical methods of estimation and inference for functional MR image analysis , 1996, Magnetic resonance in medicine.

[32]  Kevin Murphy,et al.  Removing motion and physiological artifacts from intrinsic BOLD fluctuations using short echo data , 2013, NeuroImage.