Cerebellum and neurodegenerative diseases: Beyond conventional magnetic resonance imaging

The cerebellum plays a key role in movement control and in cognition and cerebellar involvement is described in several neurodegenerative diseases. While conventional magnetic resonance imaging (MRI) is widely used for brain and cerebellar morphologic evaluation, advanced MRI techniques allow the investigation of cerebellar microstructural and functional characteristics. Volumetry, voxel-based morphometry, diffusion MRI based fiber tractography, resting state and task related functional MRI, perfusion, and proton MR spectroscopy are among the most common techniques applied to the study of cerebellum. In the present review, after providing a brief description of each technique’s advantages and limitations, we focus on their application to the study of cerebellar injury in major neurodegenerative diseases, such as multiple sclerosis, Parkinson’s and Alzheimer’s disease and hereditary ataxia. A brief introduction to the pathological substrate of cerebellar involvement is provided for each disease, followed by the review of MRI studies exploring structural and functional cerebellar abnormalities and by a discussion of the clinical relevance of MRI measures of cerebellar damage in terms of both clinical status and cognitive performance.

[1]  D. Ramasamy,et al.  Extent of cerebellum, subcortical and cortical atrophy in patients with MS A case-control study , 2009, Journal of the Neurological Sciences.

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

[3]  Jun Yi Wang,et al.  Robust Machine Learning-Based Correction on Automatic Segmentation of the Cerebellum and Brainstem , 2016, PloS one.

[4]  Mario Mascalchi,et al.  Brain white matter tracts degeneration in Friedreich ataxia. An in vivo MRI study using tract-based spatial statistics and voxel-based morphometry , 2008, NeuroImage.

[5]  Alexandra Borges,et al.  Imaging of the central skull base. , 2009, Neuroimaging clinics of North America.

[6]  A. Anwander,et al.  Validation of tractography: Comparison with manganese tracing , 2015, Human brain mapping.

[7]  C. Yasuda,et al.  A multimodal evaluation of microstructural white matter damage in spinocerebellar ataxia type 3 , 2013, Movement disorders : official journal of the Movement Disorder Society.

[8]  R. A. Zimmerman,et al.  Ataxia-telangiectasia: the pattern of cerebellar atrophy on MRI , 2003, Neuroradiology.

[9]  S. Marino,et al.  Extensive Direct Subcortical Cerebellum-Basal Ganglia Connections in Human Brain as Revealed by Constrained Spherical Deconvolution Tractography , 2016, Front. Neuroanat..

[10]  Cristina Granziera,et al.  Cerebellar Cortical Layers : In Vivo Visualization with Structural High-Field-Strength MR Imaging 1 , 2010 .

[11]  S. S. Kollias,et al.  Morphological differences in Parkinson’s disease with and without rest tremor , 2009, Journal of Neurology.

[12]  Julie S. Snowden,et al.  Choice of reference region in the quantification of single-photon emission tomography in primary degenerative dementia , 1994, European Journal of Nuclear Medicine.

[13]  À. Rovira,et al.  Contribution of the symptomatic lesion in establishing MS diagnosis and prognosis , 2016, Neurology.

[14]  Jens Frahm,et al.  Clinical proton MR spectroscopy in central nervous system disorders. , 2013, Radiology.

[15]  A. Batla,et al.  The role of cerebellum in patients with late onset cervical/segmental dystonia?--evidence from the clinic. , 2015, Parkinsonism & related disorders.

[16]  A. Shmuel,et al.  Imaging brain function in humans at 7 Tesla , 2001, Magnetic resonance in medicine.

[17]  B E Kendall,et al.  The role of NMR imaging in the assessment of multiple sclerosis and isolated neurological lesions. A quantitative study. , 1987, Brain : a journal of neurology.

[18]  M. Kaplan,et al.  Magnetic resonance imaging of the central skull base. , 1999, Topics in magnetic resonance imaging : TMRI.

[19]  S. Blaser,et al.  Diagnostic Approach to Childhood-Onset Cerebellar Atrophy , 2012, Journal of Child Neurology.

[20]  M. R. Theobald,et al.  Cerebral MR venography: normal anatomy and potential diagnostic pitfalls. , 2000, AJNR. American journal of neuroradiology.

[21]  Ajay S. Kurani,et al.  Distinct functional and macrostructural brain changes in Parkinson's disease and multiple system atrophy , 2015, Human brain mapping.

[22]  Mario Quarantelli,et al.  Modifications of resting state networks in spinocerebellar ataxia type 2 , 2015, Movement disorders : official journal of the Movement Disorder Society.

[23]  M. Filippi,et al.  Relationship between damage to the cerebellar peduncles and clinical disability in multiple sclerosis. , 2014, Radiology.

[24]  S. Marino,et al.  A rare case of cerebellar agenesis: a probabilistic Constrained Spherical Deconvolution tractographic study , 2015, Brain Imaging and Behavior.

[25]  Jeroen Hendrikse,et al.  Mapping of cerebral perfusion territories using territorial arterial spin labeling: techniques and clinical application , 2013, NMR in biomedicine.

[26]  Mark E Ladd,et al.  Structural and functional MRI abnormalities of cerebellar cortex and nuclei in SCA3, SCA6 and Friedreich's ataxia. , 2015, Brain : a journal of neurology.

[27]  Jean B. Cormack,et al.  Cranial CT with 64-, 16-, 4- and single-slice CT systems–comparison of image quality and posterior fossa artifacts in routine brain imaging with standard protocols , 2008, European Radiology.

[28]  N. Yozbatiran,et al.  Diffusion tensor imaging of the human cerebellar pathways and their interplay with cerebral macrostructure , 2015, Front. Neuroanat..

[29]  P. Joseph,et al.  A Method for Correcting Bone Induced Artifacts in Computed Tomography Scanners , 1978, Journal of computer assisted tomography.

[30]  H. Richard,et al.  Structural and Molecular Compartmentation in the Cerebellum , 1993, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[31]  L. Garriga-Grimau,et al.  [Cerebellar cognitive affective syndrome]. , 2015, Archivos argentinos de pediatria.

[32]  Peter Bachert,et al.  A Fully Automated Method for Tissue Segmentation and CSF-Correction of Proton MRSI Metabolites Corroborates Abnormal Hippocampal NAA in Schizophrenia , 2002, NeuroImage.

[33]  D. Timmann,et al.  Evaluation of a new approach for semi-automatic segmentation of the cerebellum in patients with multiple sclerosis , 2012, Journal of Neurology.

[34]  M. Castelo‐Branco,et al.  Parametric fMRI of paced motor responses uncovers novel whole‐brain imaging biomarkers in spinocerebellar ataxia type 3 , 2016, Human brain mapping.

[35]  P. Strick,et al.  An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. , 2003, Journal of neurophysiology.

[36]  S. Raskin,et al.  Diffusion tensor imaging and tract-based spatial statistics analysis in Friedreich's ataxia patients. , 2015, Parkinsonism & related disorders.

[37]  Benjamin L Walter,et al.  Fiber tractography of the axonal pathways linking the basal ganglia and cerebellum in Parkinson disease: implications for targeting in deep brain stimulation. , 2014, Journal of neurosurgery.

[38]  I. F. Braun,et al.  CT and MR imaging of the central skull base. Part 2. Pathologic spectrum. , 1990, Radiographics : a review publication of the Radiological Society of North America, Inc.

[39]  L R Schad,et al.  3D MPRAGE evaluation of lesions in the posterior cranial fossa. , 1994, Magnetic resonance imaging.

[40]  L. Kappos,et al.  Cerebellar Abnormalities Contribute to Disability Including Cognitive Impairment in Multiple Sclerosis , 2014, PloS one.

[41]  Pasquale Borrelli,et al.  In vivo dentate nucleus MRI relaxometry correlates with previous administration of Gadolinium-based contrast agents , 2016, European Radiology.

[42]  F. Cendes,et al.  The Clinical Impact of Cerebellar Grey Matter Pathology in Multiple Sclerosis , 2014, PloS one.

[43]  Stefan Maderwald,et al.  Direct visualization of cerebellar nuclei in patients with focal cerebellar lesions and its application for lesion-symptom mapping , 2012, NeuroImage.

[44]  R. Deichmann,et al.  White matter damage is related to ataxia severity in SCA3 , 2014, Journal of Neurology.

[45]  G. Mancardi,et al.  Cranial MRI in ataxia-telangiectasia , 2004, Neuroradiology.

[46]  J. Fernández-Ruiz,et al.  Functional connectivity changes related to cognitive and motor performance in spinocerebellar ataxia type 2 , 2015, Movement disorders : official journal of the Movement Disorder Society.

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

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

[49]  J. Gore Principles and practice of functional MRI of the human brain. , 2003, The Journal of clinical investigation.

[50]  H. Deininger,et al.  Cranial CT artifacts and gantry angulation. , 1991, Journal of computer assisted tomography.

[51]  M. Glickstein,et al.  Corticopontine projection in the rat: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei , 1989, The Journal of comparative neurology.

[52]  L. Yeoman,et al.  Gantry angulation in brain CT: dosage implications, effect on posterior fossa artifacts, and current international practice. , 1992, Radiology.

[53]  F. Cendes,et al.  Infratentorial gray matter atrophy and excess in primary craniocervical dystonia. , 2014, Parkinsonism & related disorders.

[54]  John N Morelli,et al.  An image-based approach to understanding the physics of MR artifacts. , 2011, Radiographics : a review publication of the Radiological Society of North America, Inc.

[55]  Jeremy D. Schmahmann,et al.  The Diagnosis and Natural History of Multiple System Atrophy, Cerebellar Type , 2016, Cerebellum.

[56]  J. Schmahmann From movement to thought: Anatomic substrates of the cerebellar contribution to cognitive processing , 1996, Human brain mapping.

[57]  K. Peck,et al.  Identification of the Corticobulbar Tracts of the Tongue and Face Using Deterministic and Probabilistic DTI Fiber Tracking in Patients with Brain Tumor , 2015, American Journal of Neuroradiology.

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

[59]  S. Maderwald,et al.  Diagnostic value of 3D fluid attenuated inversion recovery sequence in multiple sclerosis , 2015, Acta radiologica.

[60]  Wietske van der Zwaag,et al.  In vivo Structural Imaging of the Cerebellum, the Contribution of Ultra-High Fields , 2010, The Cerebellum.

[61]  Joshua H. Balsters,et al.  Symbolic representations of action in the human cerebellum , 2008, NeuroImage.

[62]  J. Pillai Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[63]  M. Mascalchi The Cerebellum Looks Normal in Friedreich Ataxia , 2013, American Journal of Neuroradiology.

[64]  Oded Gonen,et al.  Metabolite ratios to assumed stable creatine level may confound the quantification of proton brain MR spectroscopy. , 2003, Magnetic resonance imaging.

[65]  M. Bove,et al.  The fatigue-motor performance paradox in multiple sclerosis , 2013, Scientific Reports.

[66]  Richard G. Wise,et al.  The effect of inflammation and its reduction on brain plasticity in multiple sclerosis: MRI evidence , 2016, Human brain mapping.

[67]  H Lechner,et al.  Criteria for an increased specificity of MRI interpretation in elderly subjects with suspected multiple sclerosis , 1988, Neurology.

[68]  G. Egan,et al.  Fronto‐cerebellar dysfunction and dysconnectivity underlying cognition in friedreich ataxia: The IMAGE‐FRDA study , 2016, Human brain mapping.

[69]  Emergency department CT screening of patients with nontraumatic neurological symptoms referred to the posterior fossa: comparison of thin versus thick slice images , 2014, Emergency Radiology.

[70]  L. Reid,et al.  Motor pathway degeneration in young ataxia telangiectasia patients: A diffusion tractography study , 2015, NeuroImage: Clinical.

[71]  Thomas Klockgether,et al.  Update on degenerative ataxias. , 2011, Current opinion in neurology.

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

[73]  A. Gjedde,et al.  A deformation‐based morphometry study of patients with early‐stage Parkinson’s disease , 2010, European journal of neurology.

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

[75]  M. Mascalchi,et al.  Single‐voxel long TE 1H‐MR spectroscopy of the normal brainstem and cerebellum , 2002, Journal of magnetic resonance imaging : JMRI.

[76]  S. Maier,et al.  Diffusion imaging of brain tumors , 2010, NMR in biomedicine.

[77]  D Petersen,et al.  Early onset cerebellar ataxia with retained tendon reflexes. Clinical, electrophysiological and MRI observations in comparison with Friedreich's ataxia. , 1991, Brain : a journal of neurology.

[78]  Sandeep Mittal,et al.  Identification of calcification with MRI using susceptibility‐weighted imaging: A case study , 2009, Journal of magnetic resonance imaging : JMRI.

[79]  F. Tomasello,et al.  MRI Tractography of Corticospinal Tract and Arcuate Fasciculus in High-Grade Gliomas Performed by Constrained Spherical Deconvolution: Qualitative and Quantitative Analysis , 2015, American Journal of Neuroradiology.

[80]  M. Hallett,et al.  Regional homogeneity changes in patients with Parkinson's disease , 2009, Human brain mapping.

[81]  Structural and Functional anatomy of cerebellum. More than a motor conception , 2011 .

[82]  J. Balsters,et al.  Cerebellar atrophy in Parkinson's disease and its implication for network connectivity. , 2016, Brain : a journal of neurology.

[83]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[84]  R. Baker,et al.  A Functional Magnetic Resonance Imaging Study in Patients with Benign Essential Blepharospasm , 2003, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[85]  Mario Manto,et al.  The Cerebellum, Cerebellar Disorders, and Cerebellar Research—Two Centuries of Discoveries , 2008, The Cerebellum.

[86]  D. Ryglewicz,et al.  Correlations between cerebellar and brain volumes, cognitive impairments, ApoE levels, and APOE genotypes in patients with AD and MCI. , 2013, Current Alzheimer research.

[87]  A. Chawla,et al.  Imaging of skull base: Pictorial essay , 2012, Indian Journal of Radiology and Imaging.

[88]  A. Elbaz,et al.  Structural abnormalities in the cerebellum and sensorimotor circuit in writer's cramp , 2007, Neurology.

[89]  H. Lewis-Jones,et al.  Can computed tomography and magnetic resonance imaging differentiate between malignant pathology and osteomyelitis in the central skull base? , 2015, The Journal of Laryngology & Otology.

[90]  Massimo Filippi,et al.  Cerebellar contribution to motor and cognitive performance in multiple sclerosis: An MRI sub-regional volumetric analysis , 2017, Multiple sclerosis.

[91]  Aldo Quattrone,et al.  Diffusivity of cerebellar hemispheres enables discrimination of cerebellar or parkinsonian multiple system atrophy from progressive supranuclear palsy-Richardson syndrome and Parkinson disease. , 2013, Radiology.

[92]  Stefan Maderwald,et al.  Structural and functional MRI abnormalities of cerebellar cortex and nuclei in SCA 3 , SCA 6 and Friedreich ’ s ataxia , 2015 .

[93]  Andreea C. Bostan,et al.  The basal ganglia communicate with the cerebellum , 2010, Proceedings of the National Academy of Sciences.

[94]  A. S. Hall,et al.  The role of NMR imaging in the diagnosis and management of acoustic neuroma. , 1983, AJNR. American journal of neuroradiology.

[95]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[96]  Peter Bauer,et al.  Visualization, quantification and correlation of brain atrophy with clinical symptoms in spinocerebellar ataxia types 1, 3 and 6 , 2010, NeuroImage.

[97]  Denis Le Bihan,et al.  Diffusion MRI: what water tells us about the brain , 2014, EMBO molecular medicine.

[98]  J. Mugler,et al.  Suppression of cerebrospinal fluid and blood flow artifacts in FLAIR MR imaging with a single-slab three-dimensional pulse sequence: initial experience. , 2001, Radiology.

[99]  I. Wilkinson,et al.  Magnetic Resonance Spectroscopy of the Normal Cerebellum: What Degree of Variability Can Be Expected? , 2013, The Cerebellum.

[100]  C Ytterbergh,et al.  Artifacts in Computed Tomography of the Posterior Fossa: A Comparative Phantom Study , 1986, Journal of computer assisted tomography.

[101]  Christine Preibisch,et al.  Cerebral activation patterns in patients with writer's cramp: a functional magnetic resonance imaging study , 2001, Journal of Neurology.

[102]  N. Ramnani,et al.  Cerebellar Plasticity and the Automation of First-Order Rules , 2011, The Journal of Neuroscience.

[103]  R. Reynolds,et al.  Regional Distribution and Evolution of Gray Matter Damage in Different Populations of Multiple Sclerosis Patients , 2015, PloS one.

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

[105]  M. Hallett,et al.  Preclinical and clinical neural network changes in SCA2 parkinsonism. , 2013, Parkinsonism & related disorders.

[106]  F Barkhof,et al.  Multicontrast Mr Imaging at 7 T in Multiple Sclerosis: Highest Lesion Detection in Cortical Gray Matter with 3d-flair 2.2 Multicontrast Mri at 7 T in Ms , 2022 .

[107]  Frauke Zipp,et al.  Evidence for early, non-lesional cerebellar damage in patients with multiple sclerosis: DTI measures correlate with disability, atrophy, and disease duration , 2016, Multiple sclerosis.

[108]  Karen L. Furie,et al.  Comparative sensitivity of computed tomography vs. magnetic resonance imaging for detecting acute posterior fossa infarct. , 2012, The Journal of emergency medicine.

[109]  C Thomsen,et al.  [Diffusion-weighted MR imaging of the brain]. , 2001, Ugeskrift for laeger.

[110]  T. Crawford,et al.  Cerebral Abnormalities in Adults with Ataxia-Telangiectasia , 2014, American Journal of Neuroradiology.

[111]  Ludwig Kappos,et al.  Association of regional gray matter volume loss and progression of white matter lesions in multiple sclerosis — A longitudinal voxel-based morphometry study , 2009, NeuroImage.

[112]  G. Egan,et al.  Cerebral and cerebellar grey matter atrophy in Friedreich ataxia: the IMAGE-FRDA study , 2016, Journal of Neurology.

[113]  I. Toni,et al.  The Cerebral Network of Parkinson's Tremor: An Effective Connectivity fMRI Study. , 2016, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[114]  Chaozhe Zhu,et al.  Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson's disease. , 2011, European journal of radiology.

[115]  Paula Coutinho,et al.  The Global Epidemiology of Hereditary Ataxia and Spastic Paraplegia: A Systematic Review of Prevalence Studies , 2014, Neuroepidemiology.

[116]  Marek Kubicki,et al.  Radial diffusivity in the cerebellar peduncles correlates with clinical severity in Friedreich ataxia , 2013, Neurological Sciences.

[117]  M Filippi,et al.  Altered functional and structural connectivities in patients with MS , 2007, Neurology.

[118]  R C Grimm,et al.  Initial clinical experience in MR imaging of the brain with a fast fluid-attenuated inversion-recovery pulse sequence. , 1994, Radiology.

[119]  J. Voogd,et al.  The human central nervous system , 1978 .

[120]  Christa Neuper,et al.  Abnormalities of Resting State Functional Connectivity Are Related to Sustained Attention Deficits in MS , 2012, PloS one.

[121]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[122]  AJ Thompson,et al.  A comprehensive assessment of cerebellar damage in multiple sclerosis using diffusion tractography and volumetric analysis , 2011, Multiple sclerosis.

[123]  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.

[124]  A. Cherubini,et al.  A Fully Automated, Atlas-Based Approach for Superior Cerebellar Peduncle Evaluation in Progressive Supranuclear Palsy Phenotypes , 2016, American Journal of Neuroradiology.

[125]  M Skalej,et al.  Autosomal dominant cerebellar ataxia type I clinical features and MRI in families with SCA1, SCA2 and SCA3. , 1996, Brain : a journal of neurology.

[126]  P. Strick,et al.  The cerebellum communicates with the basal ganglia , 2005, Nature Neuroscience.

[127]  D. Altmann,et al.  MRI measures show significant cerebellar gray matter volume loss in multiple sclerosis and are associated with cerebellar dysfunction , 2009, Multiple sclerosis.

[128]  Patricia Svolos,et al.  T2 FLAIR artifacts at 3-T brain magnetic resonance imaging. , 2014, Clinical imaging.

[129]  W. Skaggs,et al.  The Cerebellum , 2016 .

[130]  Ponnada A. Narayana,et al.  Proton magnetic resonance spectroscopy in multiple sclerosis , 1990, Neurology.

[131]  C. Pozzilli,et al.  Dentate nucleus connectivity in adult patients with multiple sclerosis: functional changes at rest and correlation with clinical features , 2017, Multiple sclerosis.

[132]  F. Calamante,et al.  Perfusion Magnetic Resonance Imaging: A Comprehensive Update on Principles and Techniques , 2014, Korean journal of radiology.

[133]  R. Díaz,et al.  Cognitive Deficits Correlate with White Matter Deterioration in Spinocerebellar Ataxia Type 2 , 2016, Journal of the International Neuropsychological Society.

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

[135]  N J Pelc,et al.  Nonlinear partial volume artifacts in x-ray computed tomography. , 1980, Medical physics.

[136]  Manuel Desco,et al.  Is the Cerebellum the Optimal Reference Region for Intensity Normalization of Perfusion MR Studies in Early Alzheimer’s Disease? , 2013, PloS one.

[137]  J. Wolff,et al.  Synaptic pathology in the cerebellar dentate nucleus in chronic multiple sclerosis , 2017, Brain pathology.

[138]  M. Ghilardi,et al.  Diffusion tensor imaging parameters’ changes of cerebellar hemispheres in Parkinson’s disease , 2015, Neuroradiology.

[139]  B. Barbiroli,et al.  Brain diffusion‐weighted imaging in Friedreich's ataxia , 2011, Movement disorders : official journal of the Movement Disorder Society.

[140]  R. Gonzalez,et al.  Diffusion-weighted MR imaging of the brain. , 2000, Radiology.

[141]  F. Causin,et al.  MRI-detectable cortical lesions in the cerebellum and their clinical relevance in multiple sclerosis , 2016, Multiple sclerosis.

[142]  N. Toschi,et al.  Progression of Microstructural Damage in Spinocerebellar Ataxia Type 2: A Longitudinal DTI Study , 2015, American Journal of Neuroradiology.

[143]  Michael D. Greicius,et al.  Distinct Cerebellar Contributions to Intrinsic Connectivity Networks , 2009, NeuroImage.

[144]  A. Weber Imaging of the skull base. , 1996, European journal of radiology.

[145]  Marco Catani,et al.  Visualization of the deep cerebellar nuclei using quantitative T 1 and ρ magnetic resonance imaging at 3 Tesla , 2007, NeuroImage.

[146]  H. Lassmann,et al.  Chapter 1 – The story of multiple sclerosis , 2006 .

[147]  L D Blumhardt,et al.  Infratentorial atrophy on magnetic resonance imaging and disability in multiple sclerosis. , 1999, Brain : a journal of neurology.

[148]  B Lane,et al.  Single- versus multi-detector row CT of the brain: quality assessment. , 2001, Radiology.

[149]  L H Kuller,et al.  Age, Alzheimer disease, and brain structure , 2009, Neurology.

[150]  Hugo Alexandre Ferreira,et al.  Exploring the 3D geometry of the diffusion kurtosis tensor—Impact on the development of robust tractography procedures and novel biomarkers , 2015, NeuroImage.

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

[152]  J H Duyn,et al.  Pittfalls of MRI measurement of white matter perfusion based on arterial spin labeling , 2008, Magnetic resonance in medicine.

[153]  L. Tanenbaum,et al.  Clinical 3T MR imaging: mastering the challenges. , 2006, Magnetic resonance imaging clinics of North America.

[154]  E. Achten,et al.  A neuroradiologist’s guide to arterial spin labeling MRI in clinical practice , 2015, Neuroradiology.

[155]  Klaas Nicolay,et al.  1H MR spectroscopy of the brain: absolute quantification of metabolites. , 2006, Radiology.

[156]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[157]  R. Bakshi,et al.  Intraventricular CSF pulsation artifact on fast fluid-attenuated inversion-recovery MR images: analysis of 100 consecutive normal studies. , 2000, AJNR. American journal of neuroradiology.

[158]  Peter Börnert,et al.  Ghost artifact removal using a parallel imaging approach , 2005, Magnetic resonance in medicine.

[159]  Luca Roccatagliata,et al.  Multiple sclerosis: hyperintense dentate nucleus on unenhanced T1-weighted MR images is associated with the secondary progressive subtype. , 2009, Radiology.