Comparing fully automated state-of-the-art cerebellum parcellation from magnetic resonance images

&NA; The human cerebellum plays an essential role in motor control, is involved in cognitive function (i.e., attention, working memory, and language), and helps to regulate emotional responses. Quantitative in‐vivo assessment of the cerebellum is important in the study of several neurological diseases including cerebellar ataxia, autism, and schizophrenia. Different structural subdivisions of the cerebellum have been shown to correlate with differing pathologies. To further understand these pathologies, it is helpful to automatically parcellate the cerebellum at the highest fidelity possible. In this paper, we coordinated with colleagues around the world to evaluate automated cerebellum parcellation algorithms on two clinical cohorts showing that the cerebellum can be parcellated to a high accuracy by newer methods. We characterize these various methods at four hierarchical levels: coarse (i.e., whole cerebellum and gross structures), lobe, subdivisions of the vermis, and the lobules. Due to the number of labels, the hierarchy of labels, the number of algorithms, and the two cohorts, we have restricted our analyses to the Dice measure of overlap. Under these conditions, machine learning based methods provide a collection of strategies that are efficient and deliver parcellations of a high standard across both cohorts, surpassing previous work in the area. In conjunction with the rank‐sum computation, we identified an overall winning method.

[1]  Jerry L. Prince,et al.  Cortical reconstruction using implicit surface evolution: Accuracy and precision analysis , 2006, NeuroImage.

[2]  Aaron Carass,et al.  Topology preserving brain tissue segmentation using graph cuts , 2012, 2012 IEEE Workshop on Mathematical Methods in Biomedical Image Analysis.

[3]  Jennifer L. Cuzzocreo,et al.  Reconstruction of the human cerebral cortex robust to white matter lesions: Method and validation , 2014, Human brain mapping.

[4]  Aaron Carass,et al.  Automatic outlier detection using hidden Markov model for cerebellar lobule segmentation , 2018, Medical Imaging.

[5]  Martin Styner,et al.  Comparison and Evaluation of Methods for Liver Segmentation From CT Datasets , 2009, IEEE Transactions on Medical Imaging.

[6]  S. Torp,et al.  The prevalence of alcoholic cerebellar atrophy A morphometric and histological study of an autopsy material , 1986, Journal of the Neurological Sciences.

[7]  N. Schuff,et al.  Comparison of automated and manual MRI volumetry of hippocampus in normal aging and dementia , 2002, Journal of magnetic resonance imaging : JMRI.

[8]  Colin Studholme,et al.  A Supervised Patch-Based Approach for Human Brain Labeling , 2011, IEEE Transactions on Medical Imaging.

[9]  Peter A. Calabresi,et al.  A topology-preserving approach to the segmentation of brain images with multiple sclerosis lesions , 2010, NeuroImage.

[10]  Snehashis Roy,et al.  Subject-Specific Sparse Dictionary Learning for Atlas-Based Brain MRI Segmentation , 2015, IEEE Journal of Biomedical and Health Informatics.

[11]  Aaron Carass,et al.  Automated cerebellar lobule segmentation with application to cerebellar structural analysis in cerebellar disease , 2016, NeuroImage.

[12]  P. Murali Doraiswamy,et al.  Mapping the effects of ApoE4, age and cognitive status on 18F-florbetapir PET measured regional cortical patterns of beta-amyloid density and growth , 2013, NeuroImage.

[13]  Martin Styner,et al.  Standardized evaluation methodology and reference database for evaluating coronary artery centerline extraction algorithms , 2009, Medical Image Anal..

[14]  D. Louis Collins,et al.  Optimized PatchMatch for Near Real Time and Accurate Label Fusion , 2014, MICCAI.

[15]  N. Andreasen,et al.  The Role of the Cerebellum in Schizophrenia , 2008, Biological Psychiatry.

[16]  D. Caplan,et al.  Cognition, emotion and the cerebellum. , 2006, Brain : a journal of neurology.

[17]  et al.,et al.  ISLES 2015 ‐ A public evaluation benchmark for ischemic stroke lesion segmentation from multispectral MRI , 2017, Medical Image Anal..

[18]  M. Mallar Chakravarty,et al.  Derivation of high-resolution MRI atlases of the human cerebellum at 3T and segmentation using multiple automatically generated templates , 2014, NeuroImage.

[19]  Pierre-Louis Bazin,et al.  Homeomorphic brain image segmentation with topological and statistical atlases , 2008, Medical Image Anal..

[20]  Jose Dolz,et al.  3D fully convolutional networks for subcortical segmentation in MRI: A large-scale study , 2016, NeuroImage.

[21]  Koenraad Van Leemput,et al.  Automated model-based tissue classification of MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[22]  Catherine J. Stoodley,et al.  Cerebellar gray matter and lobular volumes correlate with core autism symptoms , 2015, NeuroImage: Clinical.

[23]  J. Schmahmann Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[24]  Konstantinos Kamnitsas,et al.  Efficient multi‐scale 3D CNN with fully connected CRF for accurate brain lesion segmentation , 2016, Medical Image Anal..

[25]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

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

[27]  Anders M. Dale,et al.  Sequence-independent segmentation of magnetic resonance images , 2004, NeuroImage.

[28]  Jayaram K. Udupa,et al.  New Variants of a Method of MRI Scale Normalization , 1999, IPMI.

[29]  Alejandro F. Frangi,et al.  Is the winner really the best? A critical analysis of common research practice in biomedical image analysis competitions , 2018, ArXiv.

[30]  Michael A Kraut,et al.  Association between serotonin denervation and resting‐state functional connectivity in mild cognitive impairment , 2017, Human brain mapping.

[31]  Adam Finkelstein,et al.  The Generalized PatchMatch Correspondence Algorithm , 2010, ECCV.

[32]  Aaron Carass,et al.  A JOINT REGISTRATION AND SEGMENTATION APPROACH TO SKULL STRIPPING , 2007, 2007 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[33]  Jian Sun,et al.  Delving Deep into Rectifiers: Surpassing Human-Level Performance on ImageNet Classification , 2015, 2015 IEEE International Conference on Computer Vision (ICCV).

[34]  Declan G. M. Murphy,et al.  Altered cerebellar feedback projections in Asperger syndrome , 2008, NeuroImage.

[35]  Amir Alansary,et al.  MRBrainS Challenge: Online Evaluation Framework for Brain Image Segmentation in 3T MRI Scans , 2015, Comput. Intell. Neurosci..

[36]  P. Strick,et al.  Cerebellum and nonmotor function. , 2009, Annual review of neuroscience.

[37]  Karl J. Friston,et al.  Image registration using a symmetric prior—in three dimensions , 1999, Human brain mapping.

[38]  J. O'Brien,et al.  Patterns of cerebellar volume loss in dementia with Lewy bodies and Alzheimer׳s disease: A VBM-DARTEL study , 2014, Psychiatry Research: Neuroimaging.

[39]  F. Rossi,et al.  Handbook of the Cerebellum and Cerebellar Disorders , 2013, Springer Netherlands.

[40]  Thomas Brox,et al.  U-Net: Convolutional Networks for Biomedical Image Segmentation , 2015, MICCAI.

[41]  Ulrich Seidl,et al.  The cerebellum in mild cognitive impairment and Alzheimer's disease - a structural MRI study. , 2008, Journal of psychiatric research.

[42]  Paul A. Yushkevich,et al.  Multi-Atlas Segmentation with Joint Label Fusion , 2013, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[43]  Abraham Z. Snyder,et al.  A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume , 2004, NeuroImage.

[44]  Aaron Carass,et al.  Multi-atlas segmentation of the hydrocephalus brain using an adaptive ventricle atlas , 2018, Medical Imaging.

[45]  Catherine J. Stoodley,et al.  Distinct regions of the cerebellum show gray matter decreases in autism, ADHD, and developmental dyslexia , 2014, Front. Syst. Neurosci..

[46]  Vladimir Fonov,et al.  Contribution of the cerebellum to cognitive performance in children and adolescents with multiple sclerosis , 2016, Multiple sclerosis.

[47]  J. Schmahmann An emerging concept. The cerebellar contribution to higher function. , 1991, Archives of neurology.

[48]  Bruce Fischl,et al.  Avoiding asymmetry-induced bias in longitudinal image processing , 2011, NeuroImage.

[49]  A W Toga,et al.  Pontine and cerebellar atrophy correlate with clinical disability in SCA2 , 2006, Neurology.

[50]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[51]  Daniel P. Kennedy,et al.  The Autism Brain Imaging Data Exchange: Towards Large-Scale Evaluation of the Intrinsic Brain Architecture in Autism , 2013, Molecular Psychiatry.

[52]  Xiaowei Jiang,et al.  Sexual dimorphism of the cerebellar vermis in schizophrenia , 2016, Schizophrenia Research.

[53]  Jessica A Bernard,et al.  Beat and metaphoric gestures are differentially associated with regional cerebellar and cortical volumes , 2015, Human brain mapping.

[54]  Xuemei Huang,et al.  The Role of the Cerebellum in the Pathophysiology of Parkinson's Disease , 2013, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[55]  Jerry L Prince,et al.  An Overview of the Multi-Object Geometric Deformable Model Approach in Biomedical Imaging , 2016 .

[56]  F Fazio,et al.  Regional reductions of gray matter volume in familial dyslexia , 2004, Neurology.

[57]  Jerry L. Prince,et al.  Automated Segmentation of the Cerebellar Lobules Using Boundary Specific Classification and Evolution , 2013, IPMI.

[58]  E. Courchesne,et al.  Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging. , 1994, AJR. American journal of roentgenology.

[59]  George Fein,et al.  Automated MRI cerebellar size measurements using active appearance modeling , 2014, NeuroImage.

[60]  Masao Ito The Cerebellum And Neural Control , 1984 .

[61]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[62]  I. Agartz,et al.  Smaller cerebellar vermis but not hemisphere volumes in patients with chronic schizophrenia. , 2003, The American journal of psychiatry.

[63]  G. M. Halliday,et al.  Neuronal loss in functional zones of the cerebellum of chronic alcoholics with and without Wernicke's encephalopathy , 1999, Neuroscience.

[64]  J. Holton,et al.  Selective damage to the cerebellar vermis in chronic alcoholism: a contribution from neurotoxicology to an old problem of selective vulnerability , 1997, Neuropathology and applied neurobiology.

[65]  Jörn Diedrichsen,et al.  A spatially unbiased atlas template of the human cerebellum , 2006, NeuroImage.

[66]  A L Reiss,et al.  Evaluation of Cerebellar Size in Attention-Deficit Hyperactivity Disorder , 1998, Journal of child neurology.

[67]  Subhashis Banerjee,et al.  A Novel GBM Saliency Detection Model Using Multi-Channel MRI , 2016, PloS one.

[68]  Jennifer L. Cuzzocreo,et al.  Segmentation of Brain Images Using Adaptive Atlases with Application to Ventriculomegaly , 2011, IPMI.

[69]  Jörn Diedrichsen,et al.  A probabilistic MR atlas of the human cerebellum , 2009, NeuroImage.

[70]  Jacob Henle,et al.  Handbuch der Nervenlehre des Menschen , 1871 .

[71]  Stefan Klein,et al.  Cerebellum segmentation in MRI using atlas registration and local multi-scale image descriptors , 2009, 2009 IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[72]  Jerry L. Prince,et al.  A multiple object geometric deformable model for image segmentation , 2013, Comput. Vis. Image Underst..

[73]  Nancy C. Andreasen,et al.  The therapeutic potential of the cerebellum in schizophrenia , 2014, Front. Syst. Neurosci..

[74]  Daniel S. O'Leary,et al.  Manual and Semiautomated Measurement of Cerebellar Subregions on MR Images , 2002, NeuroImage.

[75]  Krzysztof J. Gorgolewski,et al.  MRIQC: Advancing the automatic prediction of image quality in MRI from unseen sites , 2016, bioRxiv.

[76]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[77]  Eric Courchesne,et al.  Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: an fMRI study of autism. , 2003, The American journal of psychiatry.

[78]  D. Amaral,et al.  Neuroanatomy of autism , 2008, Trends in Neurosciences.

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

[80]  M. Mallar Chakravarty,et al.  CERES: A new cerebellum lobule segmentation method , 2017, NeuroImage.

[81]  Pierrick Coupé,et al.  Author manuscript, published in "Journal of Magnetic Resonance Imaging 2010;31(1):192-203" DOI: 10.1002/jmri.22003 Adaptive Non-Local Means Denoising of MR Images with Spatially Varying Noise Levels , 2010 .

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

[83]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[84]  Milan Sonka,et al.  Machine learning in a graph framework for subcortical segmentation , 2017, Medical Imaging.

[85]  Razvan Pascanu,et al.  Theano: A CPU and GPU Math Compiler in Python , 2010, SciPy.

[86]  N. Andreasen,et al.  Selective reduction of the posterior superior vermis in men with chronic schizophrenia , 2002, Schizophrenia Research.

[87]  J M Bland,et al.  Statistical methods for assessing agreement between two methods of clinical measurement , 1986 .

[88]  Sabine Van Huffel,et al.  Hierarchical non‐negative matrix factorization to characterize brain tumor heterogeneity using multi‐parametric MRI , 2015, NMR in biomedicine.

[89]  Brian B. Avants,et al.  The Multimodal Brain Tumor Image Segmentation Benchmark (BRATS) , 2015, IEEE Transactions on Medical Imaging.

[90]  Vladimir Fonov,et al.  Rapid automatic segmentation of the human cerebellum and its lobules (RASCAL)—Implementation and application of the patch‐based label‐fusion technique with a template library to segment the human cerebellum , 2014, Human brain mapping.

[91]  Aaron Carass,et al.  Combining multi-atlas segmentation with brain surface estimation , 2016, SPIE Medical Imaging.

[92]  Aaron Carass,et al.  Simple paradigm for extra-cerebral tissue removal: Algorithm and analysis , 2011, NeuroImage.

[93]  Aaron Carass,et al.  Deep Learning for Cerebellar Ataxia Classification and Functional Score Regression , 2014, MLMI.

[94]  Peter A. Calabresi,et al.  Longitudinal multiple sclerosis lesion segmentation data resource , 2017, Data in brief.

[95]  R. Adams,et al.  A Restricted Form of Cerebellar Cortical Degeneration Occurring in Alcoholic Patients , 1959 .

[96]  Snehashis Roy,et al.  Longitudinal multiple sclerosis lesion segmentation: Resource and challenge , 2017, NeuroImage.

[97]  Pierrick Coupé,et al.  HIST: HyperIntensity Segmentation Tool , 2016, Patch-MI@MICCAI.

[98]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

[99]  A L Reiss,et al.  Decreased cerebellar posterior vermis size in fragile X syndrome , 1998, Neurology.

[100]  J. Bower,et al.  Consensus Paper: The Role of the Cerebellum in Perceptual Processes , 2014, The Cerebellum.

[101]  S. Heim,et al.  Cognitive subtypes of dyslexia are characterized by distinct patterns of grey matter volume , 2013, Brain Structure and Function.

[102]  Aaron Carass,et al.  Quality assurance using outlier detection on an automatic segmentation method for the cerebellar peduncles , 2016, SPIE Medical Imaging.

[103]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[104]  D. Louis Collins,et al.  Unbiased average age-appropriate atlases for pediatric studies , 2011, NeuroImage.

[105]  Erin D Bigler,et al.  Quantitative magnetic resonance image analysis of the cerebellum in macrocephalic and normocephalic children and adults with autism , 2008, Journal of the International Neuropsychological Society.

[106]  Peter A. Calabresi,et al.  Towards Topological Correct Segmentation of Macular OCT from Cascaded FCNs , 2017, FIFI/OMIA@MICCAI.

[107]  Frederik Barkhof,et al.  Different patterns of gray matter atrophy in early- and late-onset Alzheimer’s disease , 2013, Neurobiology of Aging.

[108]  Hao Chen,et al.  DCAN: Deep Contour-Aware Networks for Accurate Gland Segmentation , 2016, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[109]  D. Louis Collins,et al.  An Optimized PatchMatch for multi-scale and multi-feature label fusion , 2016, NeuroImage.

[110]  Geraldine Dawson,et al.  Cerebellar vermal volumes and behavioral correlates in children with autism spectrum disorder , 2009, Psychiatry Research: Neuroimaging.

[111]  Jyrki Lötjönen,et al.  Robust whole-brain segmentation: Application to traumatic brain injury , 2015, Medical Image Anal..

[112]  Simon K. Warfield,et al.  A Model of Population and Subject (MOPS) Intensities With Application to Multiple Sclerosis Lesion Segmentation , 2015, IEEE Transactions on Medical Imaging.

[113]  Dennis J. L. G. Schutter,et al.  The cerebellum on the rise in human emotion , 2008, The Cerebellum.

[114]  Aaron Carass,et al.  Whole Brain Segmentation and Labeling from CT Using Synthetic MR Images , 2017, MLMI@MICCAI.

[115]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[116]  Jan K Buitelaar,et al.  Magnetic resonance imaging of boys with attention-deficit/hyperactivity disorder and their unaffected siblings. , 2004, Journal of the American Academy of Child and Adolescent Psychiatry.

[117]  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.

[118]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[119]  D. Louis Collins,et al.  Patch-based segmentation using expert priors: Application to hippocampus and ventricle segmentation , 2011, NeuroImage.

[120]  H. Mehdorn,et al.  Evidence for distinct cognitive deficits after focal cerebellar lesions , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[121]  Jerry L. Prince,et al.  Approaching expert results using a hierarchical cerebellum parcellation protocol for multiple inexpert human raters , 2013, NeuroImage.

[122]  Stephanie Powell,et al.  Registration and machine learning-based automated segmentation of subcortical and cerebellar brain structures , 2008, NeuroImage.

[123]  Stephen M. Smith,et al.  A Bayesian model of shape and appearance for subcortical brain segmentation , 2011, NeuroImage.

[124]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[125]  Jimmy Ba,et al.  Adam: A Method for Stochastic Optimization , 2014, ICLR.

[126]  Thomas Brox,et al.  3D U-Net: Learning Dense Volumetric Segmentation from Sparse Annotation , 2016, MICCAI.

[127]  D. Altman,et al.  STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT , 1986, The Lancet.

[128]  Emma J. Burton,et al.  A comprehensive study of gray matter loss in patients with Alzheimer’s disease using optimized voxel-based morphometry , 2003, NeuroImage.

[129]  L G Nyúl,et al.  On standardizing the MR image intensity scale , 1999, Magnetic resonance in medicine.

[130]  Nancy C Andreasen,et al.  An MRI study of cerebellar vermis morphology in patients with schizophrenia: evidence in support of the cognitive dysmetria concept , 1999, Biological Psychiatry.

[131]  Snehashis Roy,et al.  System for Integrated Neuroimaging Analysis and Processing of Structure , 2012, Neuroinformatics.

[132]  Jerry L Prince,et al.  Structural cerebellar correlates of cognitive and motor dysfunctions in cerebellar degeneration , 2017, Brain : a journal of neurology.

[133]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.

[134]  Xiang Li,et al.  Whole Brain Parcellation with Pathology: Validation on Ventriculomegaly Patients , 2017, Patch-MI@MICCAI.

[135]  M. Molinari,et al.  The cerebellum contributes to linguistic production , 1994, Neurology.

[136]  J. Desmond,et al.  Neuroimaging studies of the cerebellum: language, learning and memory , 1998, Trends in Cognitive Sciences.

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

[138]  F. Wilcoxon Individual Comparisons by Ranking Methods , 1945 .

[139]  O. Larsell,et al.  The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat , 1952, The Journal of comparative neurology.

[140]  Jerry L. Prince,et al.  Improving cerebellar segmentation with statistical fusion , 2016, SPIE Medical Imaging.

[141]  Ulrich Seidl,et al.  Morphological cerebral correlates of CERAD test performance in mild cognitive impairment and Alzheimer's disease. , 2011, Journal of Alzheimer's disease : JAD.

[142]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[143]  S. Crowe,et al.  The relationship between alcoholic cerebellar degeneration and cognitive and emotional functioning , 2008, Neuroscience & Biobehavioral Reviews.

[144]  T. Bourgeron,et al.  Cerebellar Volume in Autism: Literature Meta-analysis and Analysis of the Autism Brain Imaging Data Exchange Cohort , 2017, Biological Psychiatry.