A hybrid high-resolution anatomical MRI atlas with sub-parcellation of cortical gyri using resting fMRI

Brain atlases provide reference parcellations of the brain that are essential for population neuroimaging studies. We present a new high-resolution, single-subject atlas labeled into two parcellation schemes: 1) the anatomical BCI-DNI atlas, which was labeled based on known morphological and anatomical features; and 2) the hybrid USCBrain atlas, which used additional functional information to guide the sub-parcellation of cerebral cortex. Particular attention was paid to the image acquisition, processing and labeling methods to capture fine anatomical details, accommodating for the high-quality data common in recent imaging studies. A single-subject, high-resolution T1-weighted image was acquired and was then processed by an expert neuroanatomist using semi-automated methods in BrainSuite. The brain’s features were meticulously extracted with manual corrections to bias-field and masking steps, thereby providing accurate tissue classification and anatomical surface modeling. Guided by sulcal and gyral landmarks, labeled anatomical regions were drawn manually on coronal single-slice images to generate the BCI-DNI atlas, which contains 66 cortical and 29 noncortical regions. The cortical regions were further sub-parcellated based on connectivity analysis of resting fMRI data from multiple subjects in the Human Connectome Project (HCP) database, which were coregistered to the single subject. The resulting USCBrain atlas contains a total of 130 cortical and 29 noncortical regions. In addition to the anatomical and functional parcellations, we also provide a delineation between sulcal valleys and gyral crowns, which offer an additional set of 26 sulcal subregions per hemisphere. The intended use of the USCBrain atlas is to label individual brains through structural coregistration. To assess utility, we computed the adjusted Rand indices between individual sub-parcellations obtained through structural-only coregistration to the USCBrain atlas and sub-parcellations obtained directly from each subject’s resting fMRI data. The gyral sub-parcellations generated by atlas-based registration show variable but generally good overlap with the resting fMRI-based subdivisions. In addition to the crisp parcellations, a probabilistic map is included to provide users a quantitative measure of reliability for each gyral subdivision. Both atlases can be used with the BrainSuite, FreeSurfer, and FSL software packages.

[1]  D. Collins,et al.  The creation of a brain atlas for image guided neurosurgery using serial histological data , 2003, NeuroImage.

[2]  Jitendra Malik,et al.  Normalized Cuts and Image Segmentation , 2000, IEEE Trans. Pattern Anal. Mach. Intell..

[3]  Jessica L. Wisnowski,et al.  Global PDF-based temporal non-local means filtering reveals individual differences in brain connectivity , 2018, 2018 IEEE 15th International Symposium on Biomedical Imaging (ISBI 2018).

[4]  J. Mailo,et al.  Insight into the precuneus: a novel seizure semiology in a child with epilepsy arising from the right posterior precuneus. , 2015, Epileptic disorders : international epilepsy journal with videotape.

[5]  Bruce Fischl,et al.  FreeSurfer , 2012, NeuroImage.

[6]  R. Leahy,et al.  Magnetic Resonance Image Tissue Classification Using a Partial Volume Model , 2001, NeuroImage.

[7]  M. Docarmo Differential geometry of curves and surfaces , 1976 .

[8]  Christian Hennig,et al.  Recovering the number of clusters in data sets with noise features using feature rescaling factors , 2015, Inf. Sci..

[9]  Dietmar Cordes,et al.  Hierarchical clustering to measure connectivity in fMRI resting-state data. , 2002, Magnetic resonance imaging.

[10]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

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

[12]  Matthew F. Glasser,et al.  Trends and Properties of Human Cerebral Cortex: Correlations with Cortical Myelin Content Introduction and Review , 2022 .

[13]  R. Nieuwenhuys The myeloarchitectonic studies on the human cerebral cortex of the Vogt–Vogt school, and their significance for the interpretation of functional neuroimaging data , 2013, Brain Structure and Function.

[14]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[15]  Mathieu Desbrun,et al.  Discrete Differential Geometry , 2008 .

[16]  D. V. van Essen,et al.  Structural and Functional Analyses of Human Cerebral Cortex Using a Surface-Based Atlas , 1997, The Journal of Neuroscience.

[17]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[18]  Harold W. Kuhn,et al.  The Hungarian method for the assignment problem , 1955, 50 Years of Integer Programming.

[19]  Richard M. Leahy,et al.  A Method for Automated Cortical Surface Registration and Labeling , 2012, WBIR.

[20]  R. Buckner,et al.  Parcellating Cortical Functional Networks in Individuals , 2015, Nature Neuroscience.

[21]  Arthur W. Toga,et al.  Sulcal set optimization for cortical surface registration , 2010, NeuroImage.

[22]  Jian Li,et al.  Are you thinking what I’m thinking? Synchronization of resting fMRI time-series across subjects , 2018, NeuroImage.

[23]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[24]  Karl Zilles,et al.  A volumetric comparison of the insular cortex and its subregions in primates. , 2013, Journal of human evolution.

[25]  Jesper Andersson,et al.  A multi-modal parcellation of human cerebral cortex , 2016, Nature.

[26]  M. García-Fiñana,et al.  Sulcal variability, stereological measurement and asymmetry of Broca's area on MR images , 2007, Journal of anatomy.

[27]  William M. Rand,et al.  Objective Criteria for the Evaluation of Clustering Methods , 1971 .

[28]  Stephen M. Smith,et al.  Resting-State FMRI Single Subject Cortical Parcellation Based on Region Growing , 2012, MICCAI.

[29]  John D. Van Horn,et al.  Unique and persistent individual patterns of brain activity across different memory retrieval tasks , 2009, NeuroImage.

[30]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[31]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[32]  M. Jenkinson Non-linear registration aka Spatial normalisation , 2007 .

[33]  Richard M. Leahy,et al.  BrainSuite: An Automated Cortical Surface Identification Tool , 2000, MICCAI.

[34]  Bruce Fischl,et al.  Combined Volumetric and Surface Registration , 2009, IEEE Transactions on Medical Imaging.

[35]  Justin P. Haldar,et al.  Temporal Non-Local Means Filtering Reveals Real-Time Whole-Brain Cortical Interactions in Resting fMRI , 2016, PloS one.

[36]  G. Bruyn Atlas of the Cerebral Sulci, M. Ono, S. Kubik, Chad D. Abernathey (Eds.). Georg Thieme Verlag, Stuttgart, New York (1990), 232, DM 298 , 1990 .

[37]  Joanna M. Wardlaw,et al.  Whole Brain Magnetic Resonance Image Atlases: A Systematic Review of Existing Atlases and Caveats for Use in Population Imaging , 2017, Front. Neuroinform..

[38]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[39]  K. Amunts,et al.  Centenary of Brodmann's Map — Conception and Fate , 2022 .

[40]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[41]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[42]  Richard M. Leahy,et al.  Comparison of landmark-based and automatic methods for cortical surface registration , 2010, NeuroImage.

[43]  Klaus Reinhardt,et al.  Human Brain Anatomy In Computerized Images , 2016 .

[44]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

[45]  G. E. Smith The Human Brain , 1924, Nature.

[46]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[47]  Richard M. Leahy,et al.  Geodesic curvature flow on surfaces for automatic sulcal delineation , 2012, 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI).

[48]  Paul M. Thompson,et al.  Surface-Constrained Volumetric Brain Registration Using Harmonic Mappings , 2007, IEEE Transactions on Medical Imaging.

[49]  S. Choi,et al.  Individual parcellation of resting fMRI with a group functional connectivity prior , 2017, NeuroImage.

[50]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .