Mapping remodeling of thalamocortical projections in the living reeler mouse brain by diffusion tractography

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 19, 2013, Pages

  Harsan, Laura Adela ^a   Dávid, Csaba ^b   Reisert, Marco ^a   Schnell, Susanne ^a,c   Hennig, Jürgen ^a   Von Elverfeldt, Dominik ^a   Staiger, Jochen F ^d  

^a UNIVERSITY OF FREIBURG   (Germany)

^b SEMMELWEIS UNIVERSITY   (Hungary)

^c NORTHWESTERN UNIVERSITY   (United States)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Brain developmental plasticity; Fiber tracking validation

Indexed keywords

ANISOTROPY; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FORNIX; BRAIN MAPPING; CONNECTOME; CORPUS CALLOSUM; DIFFUSION TRACTOGRAPHY; FEMALE; GRAY MATTER; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; SIGNAL NOISE RATIO; THALAMUS; TRACTOGRAPHY; WHITE MATTER; WILD TYPE;

BRAIN DEVELOPMENTAL PLASTICITY; FIBER TRACKING VALIDATION;

ANIMALS; AXONS; BRAIN; BRAIN MAPPING; CEREBRAL CORTEX; DIFFUSION TENSOR IMAGING; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; MICE, NEUROLOGIC MUTANTS; NEURAL PATHWAYS; NEURONS; PROBABILITY; THALAMUS;

EID: 84877322570     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1218330110     Document Type: Article

References (60)

1. Johansen-Berg H, et al. (2005) Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex 15(1): 31-39.
2. Nauta WJ (1993) Some early travails of tracing axonal pathways in the brain. J Neurosci 13(4): 1337-1345.
3. Vercelli A, Repici M, Garbossa D, Grimaldi A (2000) Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51(1): 11-28.
4. Lichtman JW, Livet J, Sanes JR (2008) A technicolour approach to the connectome. Nat Rev 9(6): 417-422.
5. Bock DD, et al. (2011) Network anatomy and in vivo physiology of visual cortical neurons. Nature 471(7337): 177-182.
6. O'Leary DD, Chou SJ, Sahara S (2007) Area patterning of the mammalian cortex. Neuron 56(2): 252-269.
7. Lopez-Bendito G, Molnar Z (2003) Thalamocortical development: How are we going to get there? Nat Rev 4(4): 276-289.
8. Behrens TE, et al. (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6(7): 750-757.
9. Yu X, et al. (2012) Thalamocortical inputs show post-critical-period plasticity. Neuron 74(4): 731-742.
10. Garel S, Yun K, Grosschedl R, Rubenstein JL (2002) The early topography of thalamocortical projections is shifted in Ebf1 and Dlx1/2 mutant mice. Development 129(24): 5621-5634.
11. Mallamaci A, Muzio L, Chan CH, Parnavelas J, Boncinelli E (2000) Area identity shifts in the early cerebral cortex of Emx2-/- mutant mice. Nat Neurosci 3(7): 679-686.
12. Bishop KM, Goudreau G, O'Leary DD (2000) Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288(5464): 344-349.
13. Le Bihan D (2003) Looking into the functional architecture of the brain with diffusion MRI. Nat Rev 4(6): 469-480.
14. Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51(5): 527-539.
15. Jbabdi S, Johansen-Berg H (2011) Tractography: Where do we go from here? Brain Connect 1(3): 169-183.
16. Jones DK (2008) Studying connections in the living human brain with diffusion MRI. Cortex 44(8): 936-952.
17. Parker GJ, et al. (2002) Initial demonstration of in vivo tracing of axonal projections in the macaque brain and comparison with the human brain using diffusion tensor imaging and fast marching tractography. Neuroimage 15(4): 797-809.
18. Parker GJ, Haroon HA, Wheeler-Kingshott CA (2003) A framework for a streamlinebased probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. J Magn Reson Imaging 18(2): 242-254.
19. Kreher BW, et al. (2008) Connecting and merging fibres: Pathway extraction by combining probability maps. Neuroimage 43(1): 81-89.
20. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2): 265-269.
21. Reisert M, et al. (2011) Global fiber reconstruction becomes practical. Neuroimage 54(2): 955-962.
22. Li L, et al. (2012) Quantitative assessment of a framework for creating anatomical brain networks via global tractography. Neuroimage 61(4): 1017-1030.
23. Jbabdi S, Woolrich MW, Andersson JL, Behrens TE (2007) A Bayesian framework for global tractography. Neuroimage 37(1): 116-129.
24. Jiang Y, Johnson GA (2010) Microscopic diffusion tensor imaging of the mouse brain. Neuroimage 50(2): 465-471.
25. Aggarwal M, Mori S, Shimogori T, Blackshaw S, Zhang J (2010) Three-dimensional diffusion tensor microimaging for anatomical characterization of the mouse brain. Magn Reson Med 64(1): 249-261.
26. Moldrich RX, et al. (2010) Comparative mouse brain tractography of diffusion magnetic resonance imaging. Neuroimage 51(3): 1027-1036.
27. Calamante F, et al. (2012) Super-resolution track-density imaging studies of mouse brain: comparison to histology. Neuroimage 59(1): 286-296.
28. Kim YB, Kalthoff D, Po C, Wiedermann D, Hoehn M (2012) Connectivity of thalamocortical pathway in rat brain: Combined diffusion spectrum imaging and functional MRI at 11.7 T. NMR Biomed 25(7): 943-952.
29. Diamond ME, et al. (2008) 'Where' and 'what' in the whisker sensorimotor system. Nat Rev 9(8): 601-612.
30. D'Arcangelo G (2005) The reeler mouse: Anatomy of a mutant. Int Rev Neurobiol 71: 383-417.
31. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4(6): 496-505.
32. Wagener RJ, Dávid C, Zhao S, Haas CA, Staiger JF (2010) The somatosensory cortex of reeler mutant mice shows absent layering but intact formation and behavioral activation of columnar somatotopic maps. J Neurosci 30(46): 15700-15709.
33. Caviness VS, Jr., Frost DO (1983) Thalamocortical projections in the reeler mutant mouse. J Comp Neurol 219(2): 182-202.
34. Jones DK (2003) Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI. Magn Reson Med 49(1): 7-12.
35. Leergaard TB, Hilgetag CC, Sporns O (2012) Mapping the connectome: Multi-level analysis of brain connectivity. Front Neuroinform 6:14.
36. Axer M, et al. (2011) A novel approach to the human connectome: Ultra-high resolution mapping of fiber tracts in the brain. Neuroimage 54(2): 1091-1101.
37. Bohland JW, et al. (2009) A proposal for a coordinated effort for the determination of brainwide neuroanatomical connectivity in model organisms at a mesoscopic scale. PLOS Comput Biol 5(3):e1000334.
38. Ren T, Zhang J, Plachez C, Mori S, Richards LJ (2007) Diffusion tensor magnetic resonance imaging and tract-tracing analysis of Probst bundle structure in Netrin1- and DCC-deficient mice. J Neurosci 27(39): 10345-10349.
39. Fillard P, et al. (2011) Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. Neuroimage 56(1): 220-234.
40. Budde MD, Janes L, Gold E, Turtzo LC, Frank JA (2011) The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: Validation in the rat using Fourier analysis of stained tissue sections. Brain 134(Pt 8): 2248-2260.
41. Mochida GH (2009) Genetics and biology of microcephaly and lissencephaly. Semin Pediatr Neurol 16(3): 120-126.
42. Leemhuis J, et al. (2010) Reelin signals through apolipoprotein E receptor 2 and Cdc42 to increase growth cone motility and filopodia formation. J Neurosci 30(44): 14759-14772.
43. Harsan LA, et al. (2010) In vivo diffusion tensor magnetic resonance imaging and fiber tracking of the mouse brain. NMR Biomed 23(7): 884-896.
44. Clatworthy PL, et al. (2010) Probabilistic tractography of the optic radiations - an automated method and anatomical validation. Neuroimage 49(3): 2001-2012.
45. Lawes IN, et al. (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39(1): 62-79.
46. Hansen B, et al. (2011) Diffusion tensor microscopy in human nervous tissue with quantitative correlation based on direct histological comparison. Neuroimage 57(4): 1458-1465.
47. Dauguet J, et al. (2007) Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 37(2): 530-538.
48. Dauguet J, et al. (2007) Three-dimensional reconstruction of stained histological slices and 3D non-linear registration with in-vivo MRI for whole baboon brain. J Neurosci Methods 164(1): 191-204.
49. Dyrby TB, et al. (2007) Validation of in vitro probabilistic tractography. Neuroimage 37(4): 1267-1277.
50. Leergaard TB, et al. (2010) Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PLoS ONE 5(1):e8595.
51. Flint JJ, et al. (2010) Cellular-level diffusion tensor microscopy and fiber tracking in mammalian nervous tissue with direct histological correlation. Neuroimage 52(2): 556-561.
52. Bastiani M, Shah NJ, Goebel R, Roebroeck A (2012) Human cortical connectome reconstruction from diffusion weighted MRI: The effect of tractography algorithm. Neuroimage 62(3): 1732-1749.
53. Maruyama T, Matsuura M, Suzuki K, Yamamoto N (2008) Cooperative activity of multiple upper layer proteins for thalamocortical axon growth. Dev Neurobiol 68(3): 317-331.
54. Higashi S, Hioki K, Kurotani T, Kasim N, Molnár Z (2005) Functional thalamocortical synapse reorganization from subplate to layer IV during postnatal development in the reeler-like mutant rat (shaking rat Kawasaki). J Neurosci 25(6): 1395-1406.
55. Paxinos G, Franklin K (2001) The Mouse Brain in Stereotaxic Coordinates (Academic, London).
56. Wong-Riley MT, Welt C (1980) Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci USA 77(4): 2333-2337.
57. Calhoun ME, Mouton PR (2001) Length measurement: New developments in neurostereology and 3D imagery. J Chem Neuroanat 21(3): 257-265.
58. Schmitz C, Hof PR (2005) Design-based stereology in neuroscience. Neuroscience 130(4): 813-831.
59. Budde MD, Xie M, Cross AH, Song SK (2009) Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: A quantitative pixelwise analysis. J Neurosci 29(9): 2805-2813.
60. Manders EM, Verbeek FJ, Aten JA (1993) Measurement of co-localization of object in dual-colour confocal images. J Microsc 169: 375-382.