Improving Sensitivity to Functional Responses without a Loss of Spatiotemporal Precision in Human Brain Imaging

As the neuroimaging field moves towards detecting smaller effects at higher spatial resolutions, and faster sampling rates, there is increased attention given to the deleterious contribution of unstructured, thermal noise. Here, we critically evaluate the performance of a recently developed reconstruction method, termed NORDIC, for suppressing thermal noise using datasets acquired with various field strengths, voxel sizes, sampling rates, and task designs.Following minimal preprocessing, statistical activation (t-values) of NORDIC processed data was compared to the results obtained with alternative denoising methods. Additionally, the consistency of unbiased estimations of task responses at the single-voxel, single run level, using a finite impulse response model were evaluated. To examine the potential impact on effective image resolution, the overall smoothness of the data processed with different methods was examined. Finally, to determine if NORDIC alters or removes important temporal information, an exhaustive K-fold cross validation approach was employed, using unbiased task responses to predict held out timeseries, quantified using R2.After NORDIC, the t-values are increased, an improvement comparable to what could be achieved by 1.5 voxels smoothing, and task events are clearly visible and have less cross-run error. These advantages are achieved without significant compromises in spatial and temporal resolution. Cross-validated R2s based on the unbiased models show that NORDIC is not distorting the temporal structure of the data and is the best predictor of non-denoised time courses. The results demonstrate that 1 run of NORDIC data is equivalent to using 2 to 3 original runs, and performs equally well across a diverse array of functional imaging protocols.For functional neuroimaging, the increasing availability of higher field strengths and ever higher spatiotemporal resolutions has led to concomitant increase in concerns about the deleterious effects of thermal noise. Historically this noise source was suppressed using methods that reduce spatial precision such as image blurring or averaging over a large number of trials or sessions, which necessitates large data collection efforts. Here, we critically evaluate the performance of a recently developed reconstruction method, termed NORDIC. Across datasets varying in field strength, voxel sizes, sampling rates, and task designs, NORDIC produces substantial gains in data quality. Both conventional t-statistics derived from general linear models and coefficients of determination for predicting unseen data are improved, without notably increasing image smoothness.

[1]  Katherine L. Bottenhorn,et al.  TE-dependent analysis of multi-echo fMRI with tedana , 2021, J. Open Source Softw..

[2]  Laura D. Lewis,et al.  Imaging faster neural dynamics with fast fMRI: A need for updated models of the hemodynamic response , 2021, Progress in Neurobiology.

[3]  Logan T Dowdle,et al.  Statistical power or more precise insights into neuro-temporal dynamics? Assessing the benefits of rapid temporal sampling in fMRI , 2021, Progress in Neurobiology.

[4]  Rainer Goebel,et al.  LayNii: A software suite for layer-fMRI , 2021, NeuroImage.

[5]  N. Zaretskaya Zooming-in on higher-level vision: High-resolution fMRI for understanding visual perception and awareness , 2021, Progress in Neurobiology.

[6]  J. Veraart,et al.  Improved Task-based Functional MRI Language Mapping in Patients with Brain Tumors through Marchenko-Pastur Principal Component Analysis Denoising. , 2020, Radiology.

[7]  Cheryl A. Olman,et al.  Forging a path to mesoscopic imaging success with ultra-high field functional magnetic resonance imaging , 2020, Philosophical Transactions of the Royal Society B.

[8]  F. De Martino,et al.  A Paradigm Change in Functional Brain Mapping: Suppressing the Thermal Noise in fMRI , 2020 .

[9]  Laurentius Huber,et al.  Higher and deeper: Bringing layer fMRI to association cortex , 2020, Progress in Neurobiology.

[10]  Steen Moeller,et al.  NOise reduction with DIstribution Corrected (NORDIC) PCA in dMRI with complex-valued parameter-free locally low-rank processing , 2020, NeuroImage.

[11]  Essa Yacoub,et al.  Clarifying the role of higher-level cortices in resolving perceptual ambiguity using ultra high field fMRI , 2020, NeuroImage.

[12]  Paul A Taylor,et al.  To pool or not to pool: Can we ignore cross-trial variability in FMRI? , 2020, NeuroImage.

[13]  J. Polimeni,et al.  Laminar (f)MRI: A short history and future prospects , 2019, NeuroImage.

[14]  Lawrence L. Wald,et al.  Intracortical smoothing of small-voxel fMRI data can provide increased detection power without spatial resolution losses compared to conventional large-voxel fMRI data , 2019, NeuroImage.

[15]  Chun-Hung Yeh,et al.  MRtrix3: A fast, flexible and open software framework for medical image processing and visualisation , 2019, NeuroImage.

[16]  Joseph V. Hajnal,et al.  Complex diffusion-weighted image estimation via matrix recovery under general noise models , 2018, NeuroImage.

[17]  Laurentius Huber,et al.  Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex , 2018, NeuroImage.

[18]  Paul M. Thompson,et al.  A resting state fMRI analysis pipeline for pooling inference across diverse cohorts: an ENIGMA rs-fMRI protocol , 2018, Brain Imaging and Behavior.

[19]  Jung Hwan Kim,et al.  Characterization of the hemodynamic response function across the majority of human cerebral cortex , 2018, NeuroImage.

[20]  Jonathan R. Polimeni,et al.  Neuroimaging with ultra-high field MRI: Present and future , 2018, NeuroImage.

[21]  Guy B. Williams,et al.  Accurate autocorrelation modeling substantially improves fMRI reliability , 2017, Nature Communications.

[22]  Paul M. Thompson,et al.  Heritability estimates on resting state fMRI data using the ENIGMA analysis pipeline , 2017, PSB.

[23]  Kamil Ugurbil,et al.  Imaging at ultrahigh magnetic fields: History, challenges, and solutions , 2017, NeuroImage.

[24]  Lars Muckli,et al.  Laminar fMRI: Applications for cognitive neuroscience , 2017, NeuroImage.

[25]  Benedikt A. Poser,et al.  Multi-echo fMRI: A review of applications in fMRI denoising and analysis of BOLD signals , 2017, NeuroImage.

[26]  Lawrence L. Wald,et al.  Impacting the effect of fMRI noise through hardware and acquisition choices – Implications for controlling false positive rates , 2017, NeuroImage.

[27]  Jonathan R. Polimeni,et al.  Analysis strategies for high-resolution UHF-fMRI data , 2017, NeuroImage.

[28]  Essa Yacoub,et al.  The impact of ultra-high field MRI on cognitive and computational neuroimaging , 2017, NeuroImage.

[29]  Steen Moeller,et al.  Functional Sensitivity of 2D Simultaneous Multi-Slice Echo-Planar Imaging: Effects of Acceleration on g-factor and Physiological Noise , 2017, Front. Neurosci..

[30]  Paul A. Taylor,et al.  FMRI Clustering in AFNI: False-Positive Rates Redux , 2017, Brain Connect..

[31]  Wietske van der Zwaag,et al.  Ultra-high field MRI: Advancing systems neuroscience towards mesoscopic human brain function , 2017, NeuroImage.

[32]  Jan Sijbers,et al.  Denoising of diffusion MRI using random matrix theory , 2016, NeuroImage.

[33]  Jelle Veraart,et al.  Diffusion MRI noise mapping using random matrix theory , 2016, Magnetic resonance in medicine.

[34]  David C. Jangraw,et al.  Evaluation of multi-echo ICA denoising for task based fMRI studies: Block designs, rapid event-related designs, and cardiac-gated fMRI , 2016, NeuroImage.

[35]  Kamil Ugurbil,et al.  What is feasible with imaging human brain function and connectivity using functional magnetic resonance imaging , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  Maarten Mennes,et al.  Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI , 2015, NeuroImage.

[37]  J. S. Guntupalli,et al.  Decoding neural representational spaces using multivariate pattern analysis. , 2014, Annual review of neuroscience.

[38]  Robert Turner,et al.  Slab‐selective, BOLD‐corrected VASO at 7 Tesla provides measures of cerebral blood volume reactivity with high signal‐to‐noise ratio , 2014, Magnetic resonance in medicine.

[39]  Kamil Ugurbil,et al.  Magnetic Resonance Imaging at Ultrahigh Fields , 2014, IEEE Transactions on Biomedical Engineering.

[40]  Jonathan Winawer,et al.  GLMdenoise: a fast, automated technique for denoising task-based fMRI data , 2013, Front. Neurosci..

[41]  Mark W. Woolrich,et al.  Resting-state fMRI in the Human Connectome Project , 2013, NeuroImage.

[42]  Steen Moeller,et al.  Pushing spatial and temporal resolution for functional and diffusion MRI in the Human Connectome Project , 2013, NeuroImage.

[43]  R. Goebel,et al.  Cortical Depth Dependent Functional Responses in Humans at 7T: Improved Specificity with 3D GRASE , 2013, PloS one.

[44]  K. Uğurbil,et al.  Layer-Specific fMRI Reflects Different Neuronal Computations at Different Depths in Human V1 , 2012, PloS one.

[45]  Noah D. Brenowitz,et al.  Whole-brain, time-locked activation with simple tasks revealed using massive averaging and model-free analysis , 2012, Proceedings of the National Academy of Sciences.

[46]  Jack L. Gallant,et al.  Encoding and decoding in fMRI , 2011, NeuroImage.

[47]  Pradeep Ravikumar,et al.  ENCODING AND DECODING V1 FMRI RESPONSES TO NATURAL IMAGES WITH SPARSE NONPARAMETRIC MODELS. , 2011, The annals of applied statistics.

[48]  Lawrence L. Wald,et al.  Physiological noise and signal-to-noise ratio in fMRI with multi-channel array coils , 2011, NeuroImage.

[49]  John C. Gore,et al.  Differentiation of somatosensory cortices by high-resolution fMRI at 7T , 2011, NeuroImage.

[50]  D. Norris,et al.  Layer‐specific BOLD activation in human V1 , 2010, Human brain mapping.

[51]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[52]  Tobias Kober,et al.  MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field , 2010, NeuroImage.

[53]  Michael Wong Yiu Ming Correspondence on ‘‘Effect of Acupuncture on the Brain in Children With Spastic Cerebral Palsy Using Functional Neuroimaging (fMRI)’’ , 2009, Journal of Child Neurology.

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

[55]  Michael S. Beauchamp,et al.  A new method for improving functional-to-structural MRI alignment using local Pearson correlation , 2009, NeuroImage.

[56]  Jeff H. Duyn,et al.  Making the most of fMRI at 7 T by suppressing spontaneous signal fluctuations , 2009, NeuroImage.

[57]  Essa Yacoub,et al.  High-field fMRI unveils orientation columns in humans , 2008, Proceedings of the National Academy of Sciences.

[58]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[59]  Jeff H. Duyn,et al.  Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal , 2007, NeuroImage.

[60]  Essa Yacoub,et al.  Spatio-temporal point-spread function of fMRI signal in human gray matter at 7 Tesla , 2007, NeuroImage.

[61]  Lawrence L. Wald,et al.  Effect of spatial smoothing on physiological noise in high-resolution fMRI , 2006, NeuroImage.

[62]  Bostjan Likar,et al.  Intensity inhomogeneity correction of multispectral MR images , 2006, NeuroImage.

[63]  Ping Wang,et al.  Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: Insights into hemodynamic regulation , 2006, NeuroImage.

[64]  Thomas E. Nichols,et al.  Non-white noise in fMRI: Does modelling have an impact? , 2006, NeuroImage.

[65]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[66]  Lawrence L. Wald,et al.  Comparison of physiological noise at 1.5 T, 3 T and 7 T and optimization of fMRI acquisition parameters , 2005, NeuroImage.

[67]  Mark D'Esposito,et al.  Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses , 2004, NeuroImage.

[68]  K. Uğurbil,et al.  Spin‐echo fMRI in humans using high spatial resolutions and high magnetic fields , 2003, Magnetic resonance in medicine.

[69]  Richard A. Harshman,et al.  Noise Reduction in BOLD-Based fMRI Using Component Analysis , 2002, NeuroImage.

[70]  Dae-Shik Kim,et al.  Localized cerebral blood flow response at submillimeter columnar resolution , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[71]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[72]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[73]  K. Uğurbil,et al.  Retinotopic mapping of lateral geniculate nucleus in humans using functional magnetic resonance imaging. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[74]  P. Mitra,et al.  The nature of spatiotemporal changes in cerebral hemodynamics as manifested in functional magnetic resonance imaging , 1997, Magnetic resonance in medicine.

[75]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[76]  X. Hu,et al.  Reduction of signal fluctuation in functional MRI using navigator echoes , 1994, Magnetic resonance in medicine.

[77]  Xiaoping Hu,et al.  Potential pitfalls of functional MRI using conventional gradient‐recalled echo techniques , 1994, NMR in biomedicine.

[78]  L Bolinger,et al.  Quantitative magnetic resonance imaging of human brain perfusion at 1.5 T using steady-state inversion of arterial water. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[79]  J. Mugler,et al.  Rapid three‐dimensional T1‐weighted MR imaging with the MP‐RAGE sequence , 1991, Journal of magnetic resonance imaging : JMRI.

[80]  G. Ghose,et al.  Featural and temporal attention selectively enhance task-appropriate representations in human primary visual cortex , 2014 .