Validation of group-wise registration for surface-based functional MRI analysis

Resting-state functional MRI (rsfMRI) provides important information for studying and mapping the activities and functions of the brain. Conventionally, rsfMRIs are often registered to structural images in the Euclidean space without considering cortical surface geometry. Meanwhile, a surface-based representation offers a relaxed coordinate chart, but this still requires surface registration for group-wise data analysis. In this work, we investigate the performance of two existing surface registration methods in a surface-based rsfMRI analysis framework: FreeSurfer and Hierarchical Spherical Deformation (HSD). To minimize registration bias, we establish shape correspondence using both methods in a groupwise manner that estimates the unbiased average of a given cohort. To evaluate their performance, we focus on neuroanatomical alignment as well as the amount of distortion that can potentially bias surface tessellation for secondary level rsfMRI data analyses. In the pilot analysis, we examine a single timepoint of imaging data from 100 subjects out of an aging cohort. Overall, HSD establishes improved shape correspondence with reduced mean curvature deviation (10.94% less on average per subject, paired t-test: p <10-10) and reduced registration distortion (FreeSurfer: average 41.91% distortion per subject, HSD: 18.63%, paired t-test: p <10-10). Furthermore, HSD introduces less distortion than FreeSurfer in the areas identified in the individual components that were extracted by surface-based independent component analysis (ICA) after spatial smoothing and time series normalization. Consequently, we show that FreeSurfer capture individual components with globally similar but locally different patterns in ICA in visual inspection.

[1]  G. Busatto,et al.  Resting-state functional connectivity in normal brain aging , 2013, Neuroscience & Biobehavioral Reviews.

[2]  Martin Styner,et al.  Group-Wise Cortical Correspondence via Sulcal Curve-Constrained Entropy Minimization , 2013, IPMI.

[3]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[4]  Daniel A. Handwerker,et al.  Periodic changes in fMRI connectivity , 2012, NeuroImage.

[5]  Jesse A. Brown,et al.  Altered functional and structural brain network organization in autism☆ , 2012, NeuroImage: Clinical.

[6]  Guido Gerig,et al.  Development of cortical shape in the human brain from 6 to 24months of age via a novel measure of shape complexity , 2016, NeuroImage.

[7]  Emily L. Dennis,et al.  Functional Brain Connectivity Using fMRI in Aging and Alzheimer’s Disease , 2014, Neuropsychology Review.

[8]  Bradley C. Love,et al.  Variability in the analysis of a single neuroimaging dataset by many teams , 2019, Nature.

[9]  John G. Csernansky,et al.  Comparing surface-based and volume-based analyses of functional neuroimaging data in patients with schizophrenia , 2008, NeuroImage.

[10]  Christos Davatzikos,et al.  Predictors of neurodegeneration differ between cognitively normal and subsequently impaired older adults , 2019, Neurobiology of Aging.

[11]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[12]  Aaron Carass,et al.  Consistent cortical reconstruction and multi-atlas brain segmentation , 2016, NeuroImage.

[13]  Ilwoo Lyu,et al.  Hierarchical spherical deformation for cortical surface registration , 2019, Medical Image Anal..

[14]  Nicholas Ayache,et al.  Spherical Demons: Fast Diffeomorphic Landmark-Free Surface Registration , 2010, IEEE Transactions on Medical Imaging.

[15]  Jerry L. Prince,et al.  Using a statistical shape model to extract sulcal curves on the outer cortex of the human brain , 2002, IEEE Transactions on Medical Imaging.

[16]  Timothy O. Laumann,et al.  An approach for parcellating human cortical areas using resting-state correlations , 2014, NeuroImage.

[17]  Paul M. Thompson,et al.  Increased local gyrification mapped in Williams syndrome , 2006, NeuroImage.

[18]  Stefan Brodoehl,et al.  Surface-based analysis increases the specificity of cortical activation patterns and connectivity results , 2020, Scientific Reports.

[19]  Aapo Hyvärinen,et al.  Group-PCA for very large fMRI datasets , 2014, NeuroImage.

[20]  Michael I. Miller,et al.  Landmark Matching via Large Deformation Diffeomorphisms on the Sphere , 2004, Journal of Mathematical Imaging and Vision.

[21]  Steven Robbins,et al.  An unbiased iterative group registration template for cortical surface analysis , 2007, NeuroImage.

[22]  Ilwoo Lyu,et al.  Robust estimation of group-wise cortical correspondence with an application to macaque and human neuroimaging studies , 2015, Front. Neurosci..

[23]  John H. Gilmore,et al.  A cortical shape‐adaptive approach to local gyrification index , 2018, Medical Image Anal..

[24]  Lok Ming Lui,et al.  FLASH: Fast Landmark Aligned Spherical Harmonic Parameterization for Genus-0 Closed Brain Surfaces , 2015, SIAM J. Imaging Sci..

[25]  D. Louis Collins,et al.  Tuning and Comparing Spatial Normalization Methods , 2003, MICCAI.

[26]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[27]  Eileen Luders,et al.  Gender differences in cortical complexity , 2004, Nature Neuroscience.

[28]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[29]  Wiro J Niessen,et al.  Groupwise image registration based on a total correlation dissimilarity measure for quantitative MRI and dynamic imaging data , 2018, Scientific Reports.

[30]  S. Resnick,et al.  Longitudinal Magnetic Resonance Imaging Studies of Older Adults: A Shrinking Brain , 2003, The Journal of Neuroscience.

[31]  Hang Joon Jo,et al.  Volume- and Surface-Based fMRI Analysis; Geometric Influence of Smoothing Kernel , 2007, 2007 3rd International IEEE/EMBS Conference on Neural Engineering.

[32]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[33]  Daniel Rueckert,et al.  Multimodal surface matching with higher-order smoothness constraints , 2017, NeuroImage.