Simultaneous Multislice Resting-State Functional Magnetic Resonance Imaging at 3 Tesla: Slice-Acceleration-Related Biases in Physiological Effects

Simultaneous multislice echo-planar imaging (SMS-EPI) can enhance the spatiotemporal resolution of resting-state functional MRI (rs-fMRI) by encoding and simultaneously imaging "groups" of slices. However, phenomena, including respiration, cardiac pulsatility, respiration volume per time (RVT), and cardiac rate variation (CRV), referred to as "physiological processes," impact SMS-EPI rs-fMRI in a manner that is yet to be well characterized. In particular, physiological noise may incur aliasing and introduce spurious signals from one slice into another within the "slice group" in rs-fMRI data, resulting in a deleterious effect on resting-state functional connectivity MRI (rs-fcMRI) maps. In the present work, we aimed to quantitatively compare the effects of physiological noise on regular EPI and SMS-EPI in terms of rs-fMRI data and resulting functional connectivity measurements. We compare SMS-EPI and regular EPI data acquired from 11 healthy young adults with matching parameters. The physiological noise characteristics were compared between the two data sets through different combinations of physiological regression steps. We observed that the physiological noise characteristics differed between SMS-EPI and regular EPI, with cardiac pulsatility contributing more to noise in regular EPI data but low-frequency heart rate variability contributing more to SMS-EPI. In addition, a significant slice-group bias was observed in the functional connectivity density maps derived from SMS-EPI data. We conclude that making appropriate corrections for physiological noise is likely more important for SMS-EPI than for regular EPI acquisitions.

[1]  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.

[2]  Peter A. Bandettini,et al.  Integration of motion correction and physiological noise regression in fMRI , 2008, NeuroImage.

[3]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

[4]  Rajesh Nandy,et al.  Characterization and reduction of cardiac- and respiratory-induced noise as a function of the sampling rate (TR) in fMRI , 2014, NeuroImage.

[5]  Simon J. Graham,et al.  Interactions between head motion and coil sensitivity in accelerated fMRI , 2016, Journal of Neuroscience Methods.

[6]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[7]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[8]  Kawin Setsompop,et al.  Interslice leakage artifact reduction technique for simultaneous multislice acquisitions , 2014, Magnetic resonance in medicine.

[9]  Robin M Heidemann,et al.  Controlled aliasing in parallel imaging results in higher acceleration (CAIPIRINHA) for multi‐slice imaging , 2005, Magnetic resonance in medicine.

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

[11]  N. Volkow,et al.  Functional connectivity density mapping , 2010, Proceedings of the National Academy of Sciences.

[12]  Robin M Heidemann,et al.  Generalized autocalibrating partially parallel acquisitions (GRAPPA) , 2002, Magnetic resonance in medicine.

[13]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

[14]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[15]  Donald E. Myers,et al.  Linear and Generalized Linear Mixed Models and Their Applications , 2008, Technometrics.

[16]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

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

[18]  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.

[19]  Alberto Llera,et al.  ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data , 2015, NeuroImage.

[20]  M. Fox,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

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

[22]  Steen Moeller,et al.  Evaluation of slice accelerations using multiband echo planar imaging at 3T , 2013, NeuroImage.

[23]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[24]  Bharat B. Biswal,et al.  Resting state fMRI: A personal history , 2012, NeuroImage.

[25]  Kawin Setsompop,et al.  Ultra-fast MRI of the human brain with simultaneous multi-slice imaging. , 2013, Journal of magnetic resonance.

[26]  J. Weaver Simultaneous multislice acquisition of MR images , 1988, Magnetic resonance in medicine.

[27]  Peter A. Bandettini,et al.  The respiration response function: The temporal dynamics of fMRI signal fluctuations related to changes in respiration , 2008, NeuroImage.

[28]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[29]  Stephen M. Smith,et al.  Advances and Pitfalls in the Analysis and Interpretation of Resting-State FMRI Data , 2010, Front. Syst. Neurosci..

[30]  Peter A. Bandettini,et al.  Physiological noise effects on the flip angle selection in BOLD fMRI , 2011, NeuroImage.

[31]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.