Ultra-high resolution diffusion tensor imaging of the microscopic pathways of the medial temporal lobe

NeuroImage

Volumn 62, Issue 3, 2012, Pages 2065-2082

  Zeineh, Michael M ^a   Holdsworth, Samantha ^a   Skare, Stefan ^b   Atlas, Scott W ^a   Bammer, Roland ^a  

^a STANFORD UNIVERSITY   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

DTI; Hippocampus; Medial temporal lobe; MRI; Perforant pathway; Tractography

Indexed keywords

ACCURACY; ARTICLE; DIFFUSION TENSOR IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; MEDIAL TEMPORAL LOBE; NOISE REDUCTION; NORMAL HUMAN; OPTICAL RESOLUTION; PERFORANT NERVE TRACT; PRIORITY JOURNAL; SIGNAL NOISE RATIO; TEMPORAL LOBE; TRACTOGRAPHY;

BRAIN MAPPING; DIFFUSION TENSOR IMAGING; HUMANS; NEURAL PATHWAYS; TEMPORAL LOBE;

EID: 84863769222     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.05.065     Document Type: Article

References (81)

1. Aggleton J.P., Brown M.W. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 1999, 22:425-444. (discussion 444-489).
2. Alexander D.C., Barker G.J. Optimal imaging parameters for fiber-orientation estimation in diffusion MRI. Neuroimage 2005, 27:357-367.
3. Amaral D.G., Dolorfo C., Alvarez-Royo P. Organization of CA1 projections to the subiculum: a PHA-L analysis in the rat. Hippocampus 1991, 1:415-435.
4. Andersson J.L.R., Skare S. A model-based method for retrospective correction of geometric distortions in diffusion-weighted EPI. Neuroimage 2002, 16:177-199.
5. Augustinack J.C., Helmer K., Huber K.E., Kakunoori S., Zöllei L., Fischl B. Direct visualization of the perforant pathway in the human brain with ex vivo diffusion tensor imaging. Front. Hum. Neurosci. 2010, 4:42.
6. Bammer R. Basic principles of diffusion-weighted imaging. Eur. J. Radiol. 2003, 45:169-184.
7. Basser P.J., Mattiello J., LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B 1994, 103:247-254.
8. Basser P.J., Pajevic S., Pierpaoli C., Duda J., Aldroubi A. In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 2000, 44:625-632.
9. Benes F.M. Myelination of cortical-hippocampal relays during late adolescence. Schizophr. Bull. 1989, 15:585-593.
10. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
11. Burggren A.C., Zeineh M.M., Ekstrom A.D., Braskie M.N., Thompson P.M., Small G.W., Bookheimer S.Y. Reduced cortical thickness in hippocampal subregions among cognitively normal apolipoprotein E e4 carriers. Neuroimage 2008, 41:1177-1183.
12. Cook P., Bai Y., Nedjati-Gilani S., Seunarine K., Hall M., Parker G., Alexander D. Camino: open-source diffusion-MRI reconstruction and processing. 14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine 2006.
13. Dauguet J., Peled S., Berezovskii V., Delzescaux T., Warfield S.K., Born R., Westin C.-F. Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 2007, 37:530-538.
14. Dice L.R. Measures of the amount of ecologic association between species. Ecology 1945, 26:297-302.
15. Dietrich O., Raya J.G., Reeder S.B., Reiser M.F., Schoenberg S.O. Measurement of signal-to-noise ratios in MR images: influence of multichannel coils, parallel imaging, and reconstruction filters. J. Magn. Reson. Imaging 2007, 26:375-385.
16. Duvernoy H.M. The Human Hippocampus: Functional Anatomy, Vascularization, and Serial Sections with MRI 2005, Springer Verlag, Berlin.
17. Dyrby T.B., Søgaard L.V., Parker G.J., Alexander D.C., Lind N.M., Baaré W.F.C., Hay-Schmidt A., Eriksen N., Pakkenberg B., Paulson O.B., Jelsing J. Validation of in vitro probabilistic tractography. Neuroimage 2007, 37:1267-1277.
18. Embleton K.V., Haroon H.A., Morris D.M., Ralph M.A.L., Parker G.J.M. Distortion correction for diffusion-weighted MRI tractography and fMRI in the temporal lobes. Hum. Brain Mapp. 2010, 31:1570-1587.
19. Giannakopoulos P., Kövari E., Gold G., von Gunten A., Hof P.R., Bouras C. Pathological substrates of cognitive decline in Alzheimer's disease. Front. Neurol. Neurosci. 2009, 24:20-29.
20. Goldman-Rakic P.S., Selemon L.D., Schwartz M.L. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience 1984, 12:719-743.
21. Gómez-Isla T., Price J.L., McKeel D.W., Morris J.C., Growdon J.H., Hyman B.T. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 1996, 16:4491-4500.
22. Gómez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 1997, 41:17-24.
23. Griswold M.A., Jakob P.M., Heidemann R.M., Nittka M., Jellus V., Wang J., Kiefer B., Haase A. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn. Reson. Med. 2002, 47:1202-1210.
24. Haselgrove J.C., Moore J.R. Correction for distortion of echo-planar images used to calculate the apparent diffusion coefficient. Magn. Reson. Med. 1996, 36:960-964.
25. Hevner R.F., Kinney H.C. Reciprocal entorhinal-hippocampal connections established by human fetal midgestation. J. Comp. Neurol. 1996, 372:384-394.
26. Holdsworth S., Skare S., Bammer R. On the application of phase correction and use of k-space entropy in partial Fourier diffusion-weighted EPI. Proceedings 17th Scientific Meeting, International Society for Magnetic Resonance in Medicine, Honolulu 2009, 4617.
27. Holdsworth S.J., Skare S., Newbould R.D., Bammer R. Robust GRAPPA-accelerated diffusion-weighted readout-segmented (RS)-EPI. Magn. Reson. Med. 2009, 62:1629-1640.
28. Hyman B.T., Van Hoesen G.W., Damasio A.R., Barnes C.L. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 1984, 225:1168-1170.
29. Insausti R., Amaral D.G. The Human Nervous System 2004, 871-914. Academic Press, London. second edition.
30. Insausti R., Juottonen K., Soininen H., Insausti A.M., Partanen K., Vainio P., Laakso M.P., Pitkänen A. MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. AJNR Am. J. Neuroradiol. 1998, 19:659-671.
31. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
32. Jezzard P., Barnett A.S., Pierpaoli C. Characterization of and correction for eddy current artifacts in echo planar diffusion imaging. Magn. Reson. Med. 1998, 39:801-812.
33. Jones D.K. Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI. Magn. Reson. Med. 2003, 49:7-12.
34. Jones D.K., Basser P.J. "Squashing peanuts and smashing pumpkins": how noise distorts diffusion-weighted MR data. Magn. Reson. Med. 2004, 52:979-993.
35. Jones D.K., Leemans A. Diffusion tensor imaging. Methods Mol. Biol. 2011, 711:127-144.
36. Kalus P., Slotboom J., Gallinat J., Mahlberg R., Cattapan-Ludewig K., Wiest R., Nyffeler T., Buri C., Federspiel A., Kunz D., Schroth G., Kiefer C. Examining the gateway to the limbic system with diffusion tensor imaging: the perforant pathway in dementia. Neuroimage 2006, 30:713-720.
37. Kerchner G.A., Hess C.P., Hammond-Rosenbluth K.E., Xu D., Rabinovici G.D., Kelley D.A.C., Vigneron D.B., Nelson S.J., Miller B.L. Hippocampal CA1 apical neuropil atrophy in mild Alzheimer disease visualized with 7-T MRI. Neurology 2010, 75:1381-1387.
38. Köhler C. Morphological details of the projection from the presubiculum to the entorhinal area as shown with the novel PHA-L immunohistochemical tracing method in the rat. Neurosci. Lett. 1984, 45:285-290.
39. Leemans A., Jones D.K. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn. Reson. Med. 2009, 61:1336-1349.
40. Lim C., Blume H.W., Madsen J.R., Saper C.B. Connections of the hippocampal formation in humans: I. The mossy fiber pathway. J. Comp. Neurol. 1997, 385:325-351.
41. Lim C., Mufson E.J., Kordower J.H., Blume H.W., Madsen J.R., Saper C.B. Connections of the hippocampal formation in humans: II. The endfolial fiber pathway. J. Comp. Neurol. 1997, 385:352-371.
42. Malykhin N., Concha L., Seres P., Beaulieu C., Coupland N.J. Diffusion tensor imaging tractography and reliability analysis for limbic and paralimbic white matter tracts. Psychiatry Res. 2008, 164:132-142.
43. Mirra S.S., Heyman A., McKeel D., Sumi S.M., Crain B.J., Brownlee L.M., Vogel F.S., Hughes J.P., van Belle G., Berg L. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991, 41:479-486.
44. Mufson E.J., Pandya D.N. Some observations on the course and composition of the cingulum bundle in the rhesus monkey. J. Comp. Neurol. 1984, 225:31-43.
45. Mufson E.J., Brady D.R., Kordower J.H. Tracing neuronal connections in postmortem human hippocampal complex with the carbocyanine dye DiI. Neurobiol. Aging 1990, 11:649-653.
46. Müller M.J., Mazanek M., Weibrich C., Dellani P.R., Stoeter P., Fellgiebel A. Distribution characteristics, reproducibility, and precision of region of interest-based hippocampal diffusion tensor imaging measures. AJNR Am. J. Neuroradiol. 2006, 27:440-446.
47. Nieuwenhuys R., Voogd J., Van Huijzen C., Van Huijzen C. The Human Central Nervous System 2008, Springer Verlag.
48. O'Mara S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. J. Anat. 2005, 207:271-282.
49. Ozarslan E., Koay C., Shepherd T., Blackband S., Basser P. Simple harmonic oscillator based reconstruction and estimation for three-dimensional q-space MRI. Proceedings 17th Scientific Meeting, International Society for Magnetic Resonance in Medicine, Honolulu 2009, 1396.
50. Parker G.J.M., Haroon H.A., Wheeler-Kingshott C.A.M. A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. J. Magn. Reson. Imaging 2003, 18:242-254.
51. Pipe J.G., Farthing V.G., Forbes K.P. Multishot diffusion-weighted FSE using PROPELLER MRI. Magn. Reson. Med. 2002, 47:42-52.
52. Powell H.W.R., Guye M., Parker G.J.M., Symms M.R., Boulby P., Koepp M.J., Barker G.J., Duncan J.S. Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus. Neuroimage 2004, 22:740-747.
53. Qu P., Shen G.X., Wang C., Wu B., Yuan J. Tailored utilization of acquired k-space points for GRAPPA reconstruction. J. Magn. Reson. 2005, 174:60-67.
54. Reeder S.B., Atalar E., Faranesh A.Z., McVeigh E.R. Referenceless interleaved echo-planar imaging. Magn. Reson. Med. 1999, 41:87-94.
55. Reese T.G., Heid O., Weisskoff R.M., Wedeen V.J. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn. Reson. Med. 2003, 49:177-182.
56. Rohde G.K., Barnett A.S., Basser P.J., Marenco S., Pierpaoli C. Comprehensive approach for correction of motion and distortion in diffusion-weighted MRI. Magn. Reson. Med. 2004, 51:103-114.
57. Rose S.E., McMahon K.L., Janke A.L., O'Dowd B., de Zubicaray G., Strudwick M.W., Chalk J.B. Diffusion indices on magnetic resonance imaging and neuropsychological performance in amnestic mild cognitive impairment. J. Neurol. Neurosurg. Psychiatry 2006, 77:1122-1128.
58. Rosene D.L., Van Hoesen G.W. Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 1977, 198:315-317.
59. Salmenpera T.M., Simister R.J., Bartlett P., Symms M.R., Boulby P.A., Free S.L., Barker G.J., Duncan J.S. High-resolution diffusion tensor imaging of the hippocampus in temporal lobe epilepsy. Epilepsy Res. 2006, 71:102-106.
60. Shepherd T.M., Ozarslan E., Yachnis A.T., King M.A., Blackband S.J. Diffusion tensor microscopy indicates the cytoarchitectural basis for diffusion anisotropy in the human hippocampus. AJNR Am. J. Neuroradiol. 2007, 28:958-964.
61. Skare S., Newbould R.D., Clayton D.B., Albers G.W., Nagle S., Bammer R. Clinical multishot DW-EPI through parallel imaging with considerations of susceptibility, motion, and noise. Magn. Reson. Med. 2007, 57:881-890.
62. Skare S., Holdsworth S., Newbould R., Bammer R. On the battle between Rician noise and phase-interferences in DWI. Proceedings 17th Scientific Meeting, International Society for Magnetic Resonance in Medicine, Honolulu 2009, 1409.
63. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
64. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl. 1):S208-S219.
65. Suzuki W.A., Amaral D.G. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J. Neurosci. 1994, 14:1856-1877.
66. Swanson L.W., Cowan W.M. Hippocampo-hypothalamic connections: origin in subicular cortex, not ammon's horn. Science 1975, 189:303-304.
67. Swanson L.W., Cowan W.M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 1977, 172:49-84.
68. Swanson L.W., Wyss J.M., Cowan W.M. An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J. Comp. Neurol. 1978, 181:681-715.
69. Trojanowski J.Q., Lee V.M.Y. The role of tau in Alzheimer's disease. Med. Clin. North Am. 2002, 86:615-627.
70. Van Hoesen G.W., Pandya D.N. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res. 1975, 95:39-59.
71. Van Hoesen G.W., Hyman B.T., Damasio A.R. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus 1991, 1:1-8.
72. Van Leemput K., Bakkour A., Benner T., Wiggins G., Wald L.L., Augustinack J., Dickerson B.C., Golland P., Fischl B. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 2009, 19:549-557.
73. Witter M.P., Van Hoesen G.W., Amaral D.G. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J. Neurosci. 1989, 9:216-228.
74. Woolrich M.W., Jbabdi S., Patenaude B., Chappell M., Makni S., Behrens T., Beckmann C., Jenkinson M., Smith S.M. Bayesian analysis of neuroimaging data in FSL. Neuroimage 2009, 45:S173-S186.
75. Xu D. Correcting high order eddy current induced distortion for diffusion weighted echo planar imaging. Proceedings 19th Scientific Meeting, International Society for Magnetic Resonance in Medicine, Montreal 2011, 4564.
76. Yassa M.A., Muftuler L.T., Stark C.E.L. Ultrahigh-resolution microstructural diffusion tensor imaging reveals perforant path degradation in aged humans in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:12687-12691.
77. Yushkevich P.A., Piven J., Hazlett H.C., Smith R.G., Ho S., Gee J.C., Gerig G. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006, 31:1116-1128.
78. Yushkevich P.A., Avants B.B., Pluta J., Das S., Minkoff D., Mechanic-Hamilton D., Glynn S., Pickup S., Liu W., Gee J.C., Grossman M., Detre J.A. A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4T. Neuroimage 2009, 44:385-398.
79. Yushkevich P.A., Wang H., Pluta J., Das S.R., Craige C., Avants B.B., Weiner M.W., Mueller S. Nearly automatic segmentation of hippocampal subfields in in vivo focal T2-weighted MRI. Neuroimage 2010, 53:1208-1224.
80. Zeineh M.M., Engel S.A., Thompson P.M., Bookheimer S.Y. Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 2003, 299:577-580.
81. Zeineh M.M., Holdsworth S., Skare S., Atlas S.W., Bammer R. Challenges of high-resolution diffusion imaging of the human medial temporal lobe in Alzheimer disease. Top. Magn. Reson. Imaging 2010, 21:355-365.