MR diffusion histology and micro-tractography reveal mesoscale features of the human cerebellum

Cerebellum

Volumn 12, Issue 6, 2013, Pages 923-931

  Dell'Acqua, Flavio ^a   Bodi, Istvan ^b   Slater, David ^a   Catani, Marco ^a   Modo, Michel ^a,c,d,e  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

^e University of Pittsburgh   (United States)

Author keywords

Cerebellum; Connectome; Diffusion tensor imaging; Human; Micro tractography; MR diffusion histology; Multi scale; Post mortem; Tractography

Indexed keywords

ARTICLE; BRAIN REGION; CELL COMPOSITION; CEREBELLUM; CEREBELLUM CORTEX; CHILD; CONNECTOME; DIFFUSION TENSOR IMAGING; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MICROTRACTOGRAPHY; MR DIFFUSION HISTOLOGY; NERVE CELL NETWORK; NEUROANATOMY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SCHOOL CHILD; THREE DIMENSIONAL IMAGING; TISSUE STRUCTURE; TRACTOGRAPHY;

ANISOTROPY; CEREBELLUM; CHILD; DIFFUSION TENSOR IMAGING; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MYELIN BASIC PROTEIN; NEURAL PATHWAYS; NEURONS; POSTMORTEM CHANGES;

EID: 84892433914     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-013-0503-x     Document Type: Article

References (68)

1. Golgi C. Sulla struttura della sostanza grigia del cervello. Gazzetta Med Ital Lombardia. 1873;6:244-6.
2. Pannese E. The Golgi stain: invention, diffusion and impact on neurosciences. J Hist Neurosci. 1999;8(2):132-40.
3. Ramon y Cajal S. The Croonian Lecture. La fine structure des centres nerveux. Proc R Soc Lond. 1894;55:444-67.
4. Glickstein M, Strata P, Voogd J. Cerebellum: history. Neuroscience. 2009;162(3):549-59.
5. Dow RS, Moruzzi G. The physiology and pathology of the cerebellum. Minneapolis: University of Minnesota Press; 1958.
6. Marr D. A theory of the cerebellar cortex. J Physiol. 1969;202:437-70.
7. Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25-61.
8. Manto M, Bower JM, Conforto AB, Delgado-García JM, da Guarda SN F, Gerwig M, et al. Consensus paper: roles of the cerebellum in motor control-the diversity of ideas on cerebellar involvement in movement. Cerebellum. 2012;11(3):352-65.
9. Strata P. David Marr's theory of cerebellar learning: 40 years later. J Physiol. 2009;587(23):5519-20.
10. Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89:634-9.
11. Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432-44.
12. Schmahmann J, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121:561-79.
13. Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum-insights from the clinic. Cerebellum. 2007;6:254-67.
14. Deoni SCL, Catani M. Visualization of the deep cerebellar nuclei using quantitative T1 and rho magnetic resonance imaging at 3 Tesla. NeuroImage. 2007;37(4):1260-6.
15. Marques JP, van der Zwaag W, Granziera C, Krueger G, Gruetter R. Cerebellar cortical layers: in vivo visualization with structural highfield-strength MR imaging. Radiology. 2010;254(3):942-8.
16. Granziera C, Schmahmann JD, Hadjikhani N, Meyer H, Meuli R, Wedeen VJ, et al. Diffusion spectrum imaging shows the structural basis of functional cerebellar circuits in the human cerebellum in vivo. PLoS One. 2009;4:e5101.
17. Catani M, Jones DK, Daly E, Embiricos N, Deeley Q, Pugliese L, et al. Altered cerebellar feedback projections in Asperger syndrome. NeuroImage. 2008;41(4):1184-91.
18. Lee S-K, Kim DI, Kim J, Kim DJ, Kim HD, Kim DS, et al. Diffusion-tensor MR imaging and fiber tractography: a new method of describing aberrant fiber connections in developmental CNS anomalies. Radiographics. 2005;25:53-65.
19. Okugawa G, Nobuhara K, Minami T, Takase K, Sugimoto T, Saito Y, et al. Neural disorganization in the superior cerebellar peduncle and cognitive abnormality in patients with schizophrenia: a diffusion tensor imaging study. Prog Neuro-Psychopharmacol Biol Psychiatry. 2006;30:1408-12.
20. Taoka T, Kin T, Nakagawa H, Hirano M, Sakamoto M, Wada T, et al. Diffusivity and diffusion anisotropy of cerebellar peduncles in cases of spinocerebellar degenerative disease. NeuroImage. 2007;37:387-93.
21. Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, Blatt GJ, et al. Consensus paper: pathological role of the cerebellum in autism. Cerebellum. 2012;11(3):777-807.
22. DeFelipe J. From the connectome to the synaptome: an epic love story. Science. 2010;330:1198-201.
23. Lichtman JW, Denk W. The big and the small: challenges of imaging the brain's circuits. Science. 2011;334:618-23.
24. Sporns O, Tononi G, Kotter R. The human connectome: a structural description of the human brain. PLoS Comput Biol. 2005;1:e42.
25. Kobbert C, Apps R, Bechmann I, Lanciego JL, Mey J, Thanos S. Current concepts in neuroanatomical tracing. Prog Neurobiol. 2000;62:327-51.
26. Boldogkoi Z, Sik A, Denes A, Reichart A, Toldi J, Gerendai I, et al. Novel tracing paradigms-genetically engineered herpesviruses as tools for mapping functional circuits within the CNS: present status and future prospects. Prog Neurobiol. 2004;72:417-45.
27. Wouterlood FG, Vinkenoog M, van den Oever M. Tracing tools to resolve neural circuits. Network. 2002;13:327-42.
28. Pautler RG, Koretsky AP. Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. NeuroImage. 2002;16:441-8.
29. Racette BA, Aschner M, Guilarte TR, Dydak U, Criswell SR, Zheng W. Pathophysiology of manganese-associated neurotoxicity. Neurotoxicology. 2012;33(4):881-6.
30. Balsters JH, Cussans E, Diedrichsen J, Phillips KA, Preuss TM, Rilling JK, et al. Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules. NeuroImage. 2010;49:2045-52.
31. Rathelot JA, Strick PL. Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci U S A. 2009;106:918-23.
32. Mesulam M. The evolving landscape of human cortical connectivity: facts and inferences. NeuroImage. 2012;62(4):2182-9.
33. Swanson LW. Mapping the human brain: past, present, and future. Trends Neurosci. 1995;18:471-4.
34. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. NeuroImage. 2009;44:489-501.
35. Peterburs J, Bellebaum C, Koch B, Schwarz M, Daum I. Working memory and verbal fluency deficits following cerebellar lesions: relation to interindividual differences in patient variables. Cerebellum. 2010;9(3):375-83.
36. Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352-65.
37. Jones DK. Studying connections in the living human brain with diffusion MRI. Cortex. 2008;44:936-52.
38. Basser PJ, Mattiello J, Le Bihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994;66:259-67.
39. Mori S, van Zijl PCM. Fiber tracking: principles and strategies-a technical review. NMR Biomed. 2002;15:468-80.
40. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn Reson Med. 2000;44:625-32.
41. Catani M, Howard RJ, Pajevic S, Jones DK. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage. 2002;17(1):77-94.
42. Thiebaut de Schotten M, Dell'Acqua F, Forkel S, Simmons A, Vergani F, Murphy D, et al. A lateralized brain network for visuospatial attention. Nat Neurosci. 2011;14(10):1245-6.
43. Wiegell MR, Larsson HBW, Wedeen VJ. Fiber crossing in human brain depicted with diffusion tensor MR imaging. Radiology. 2000;217:897-903.
44. Seehaus AK, Roebroeck A, Chiry O, Kim DS, Ronen I, Bratzke H, et al. Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex. 2013;23(2):442-50.
45. Leergaard TB, White NS, de Crespigny AJ, Bolstad I, D'Arceuil HE, Bjaalie JG, et al. Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PLoS One. 2010;e8595(1).
46. Flint JJ, Hansen B, Fey M, Schmidig D, King MA, Vestergaard-Poulsen P, et al. Cellular-level diffusion tensor microscopy and fiber tracking in mammalian nervous tissue with direct histological correlation. NeuroImage. 2010;52:556-61.
47. Mcnab JA, Jbabdi S, Deoni SCL, Douaud G, Behrens TEJ, Miller KL. High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. NeuroImage. 2009;46(3):775-85.
48. Miller KL, Stagg CJ, Douaud G, Jbabdi S, Smith SM, Behrens TEJ, et al. Diffusion imaging of whole, post-mortem human brains on a clinical MRI scanner. NeuroImage. 2011;57(1):167-81.
49. Shepherd TM, Ozarslan E, Yachnis AT, King MA, Blackband SJ. Diffusion tensor microscopy indicates the cytoarchitectural basis for diffusion anisotropy in the human hippocampus. Am J Neuroradiol. 2007;28:958-64.
50. Jones DK, Basser PJ. Squashing peanuts and smashing pumpkins: how noise distorts diffusion-weighted MR data. Magn Reson Med. 2004;52(5):979-93.
51. Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci. 2005;6:297-311.
52. Dell'Acqua F, Catani M. Structural human brain networks: hot topics in diffusion tractography. Curr Opin Neurol. 2011;25(4):375-83.
53. Assaf Y, Basser PJ. Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. NeuroImage. 2005;27:48-58.
54. Alexander DC. A general framework for experiment design in diffusion MRI and its application in measuring direct tissuemicrostructure features. Magn Reson Med. 2008;60(2):439-48.
55. Jespersen SN, Kroenke CD, Ostergaard L, Ackerman JJ, Yablonskiy DA. Modeling dendrite density from magnetic resonance diffusion measurements. NeuroImage. 2007;34:1473-86.
56. Wedeen VJ, Hagmann P, Tseng WYI, Reese TG, Weisskoff RM. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med. 2005;54(6):1377-86.
57. Tournier JD, Calamante F, Gadian DG, Connelly A. Direct estimation of the fiber orientation density function from diffusionweighted MRI using spherical deconvolution. NeuroImage. 2004;23:1176-85.
58. Dell'Acqua F, Scifo P, Rizzo G, Catani M, Simmons A, Scotti G, et al. A modified damped Richardson-Lucy algorithm to reduce isotropic background effects in spherical deconvolution. NeuroImage. 2010;49(2):1446-58.
59. Shepherd TM, Flint JJ, Thelwall PE, Stanisz GJ, Mareci TH, Yachnis AT, et al. Postmortem interval alters the water relaxation and diffusion properties of rat nervous tissue-implications forMRI studies of human autopsy samples. NeuroImage. 2009;44:820-6.
60. D'Arceuil HE, Crespigny AJ. The effects of brain tissue decomposition on diffusion tensor imaging and tractography. NeuroImage. 2007;36:64-8.
61. D'Arceuil HE, Westmoreland S, de Crespigny AJ. An approach to high resolution diffusion tensor imaging in fixed primate brain. NeuroImage. 2007;35:553-65.
62. Dyrby TB, Baare WFC, Alexander DC, Jelsing J, Garde E, Søgaard LV. An ex vivo imaging pipeline for producing high-quality and high-resolution diffusion-weighted imaging datasets. Hum Brain Mapp. 2011;32:544-63.
63. Ramnani N. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 2006;7:511-22.
64. Sultan F, Augath M, Hamodeh S, Murayama Y, Oeltermann A, Rauch A, et al. Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks. Nature Commun. 2012;3:924.
65. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. NeuroImage. 2009;46:39-46.
66. Saksena S, Husain N, Das V, Pradhan M, Trivedi R, Srivastava S, et al. Diffusion tensor imaging in the developing human cerebellum with histologic correlation. Int J Dev Neurosci. 2008;26:705-11.
67. Annese J. The importance of combining MRI and large-scale digital histology in neuroimaging studies of brain connectivity and disease. Front Neuroinformatics. 2012;6:13.
68. Catani M, Thiebaut de Schotten M, Slater D, Dell'Acqua F. Connectomic approaches before the connectome. Neuroimage. 2013. doi:10.1016/j.neuroimage. 2013.05.109.