Histology-derived volumetric annotation of the human hippocampal subfields in postmortem MRI

NeuroImage

Volumn 84, Issue , 2014, Pages 505-523

  Adler, Daniel H ^a,b   Pluta, John ^a,c   Kadivar, Salmon ^a   Craige, Caryne ^a   Gee, James C ^a   Avants, Brian B ^a   Yushkevich, Paul A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Hippocampus; Histology; MRI; Postmortem; Reconstruction; Subfields

Indexed keywords

AGED; ARTICLE; AUTOPSY; BRAIN MAPPING; CYTOARCHITECTURE; FEMALE; HIPPOCAMPUS; HISTOLOGY; HUMAN; HUMAN TISSUE; IMAGE PROCESSING; IMAGE RECONSTRUCTION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; ALGORITHM; COMPUTER ASSISTED DIAGNOSIS; IMAGE ENHANCEMENT; PATHOLOGY; POSTMORTEM CHANGE; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; THREE DIMENSIONAL IMAGING; VERY ELDERLY;

AGED, 80 AND OVER; ALGORITHMS; AUTOPSY; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; POSTMORTEM CHANGES; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84884962740     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.08.067     Document Type: Article

References (117)

1. Amaral D., Lavenex P. The Hippocampus Book 2007, Oxford University Press, Cambridge.
2. Amunts K., Kedo O., Kindler M., Pieperhoff P., Mohlberg H., Shah N., Habel U., Schneider F., Zilles K. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat. Embryol. 2005, 210(5-6):343-352.
3. Amunts K., Lepage C., Borgeat L., Mohlberg H., Dickscheid T., Rousseau M.-T., Bludau S., Bazin P.-L., Lewis L.B., Oros-Peusquens A.-M. BigBrain: an ultrahigh-resolution 3D human brain model. Science 2013, 340(6139):14721475.
4. Apostolova L.G., Dinov I.D., Dutton R.A., Hayashi K.M., Toga A.W., Cummings J.L., Thompson P.M. 3D comparison of hippocampal atrophy in amnestic mild cognitive impairment and Alzheimer's disease. Brain 2006, 129(11):2867-2873.
5. Arganda-Carreras I., Sorzano C.O.S., Thévenaz P., Muñoz Barrutia A., Kybic J., Marabini R., Carazo J.M., Ortiz-de Solorzano C. Non-rigid consistent registration of 2D image sequences. Phys. Med. Biol. 2010, 55(20):6215-6242.
6. 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):1-13.
7. Avants B., Epstein C., Grossman M., Gee J. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 2008, 12(1):26-41.
8. Avants B., Tustison N., Wu J., Cook P., Gee J. An Open Source Multivariate Framework for n-Tissue Segmentation with Evaluation on Public Data 2011, University of Pennsylvania Image Computing and Science Laboratory, (Whitepaper).
9. Bakker A., Kirwan C.B., Miller M., Stark C.E.L. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319(5870):1640-1642.
10. Bardinet E., Bhattacharjee M., Dormont D., Pidoux B., Malandain G., Schpbach M., Ayache N., Cornu P., Agid Y., Yelnik J. A three-dimensional histological atlas of the human basal ganglia. II. Atlas deformation strategy and evaluation in deep brain stimulation for Parkinson disease. J. Neurosurg. 2009, 110(2):208-219.
11. Barnes J., Bartlett J.W., van de Pol L.A., Loy C.T., Scahill R.I., Frost C., Thompson P., Fox N.C. A meta-analysis of hippocampal atrophy rates in Alzheimer's disease. Neurobiol. Aging 2009, 30(11):1711-1723.
12. Beare R., Richards K., Murphy S., Petrou S., Reutens D. An assessment of methods for aligning two-dimensional microscope sections to create image volumes. J. Neurosci. Methods 2008, 170(2):332-344.
13. Bird C.M., Burgess N. The hippocampus and memory: insights from spatial processing. Nat. Rev. Neurosci. 2008, 9(3):182-194.
14. Blamire A.M., Rowe J.G., Styles P., McDonald B. Optimising imaging parameters for post mortem MR imaging of the human brain. Acta Radiol. 1999, 40(6):593-597.
15. Bobinski M., de Leon M.J., Tarnawski M., Wegiel J., Bobinski M., Reisberg B., Miller D.C., Wisniewski H.M. Neuronal and volume loss in CA1 of the hippocampal formation uniquely predicts duration and severity of Alzheimer disease. Brain Res. 1998, 805(1):267-269.
16. Boccardi M., Ganzola R., Bocchetta M., Pievani M., Redolfi A., Bartzokis G., Camicioli R., Csernansky J.G., de Leon M.J., deToledo-Morrell L. Survey of protocols for the manual segmentation of the hippocampus: preparatory steps towards a joint EADC-ADNI harmonized protocol. J. Alzheimers Dis. 2011, 26:61-75.
17. Bonnici H.M., Chadwick M.J., Kumaran D., Hassabis D., Weiskopf N., Maguire E.A. Multi-voxel pattern analysis in human hippocampal subfields. Front. Hum. Neurosci. 2012, 6.
18. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82(4):239-259.
19. Braak H., Alafuzoff I., Arzberger T., Kretzschmar H., Tredici K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006, 112(4):389-404.
20. Breen M.S., Lancaster T.L., Wilson D.L. Correcting spatial distortion in histological images. Comput. Med. Imaging Graph. 2005, 29(6):405-417.
21. Breen M.S., Lazebnik R.S., Wilson D.L. Three-dimensional registration of magnetic resonance image data to histological sections with model-based evaluation. Ann. Biomed. Eng. 2005, 33(8):1100-1112.
22. Bürgel U., Schormann T., Schleicher A., Zilles K. Mapping of histologically identified long fiber tracts in human cerebral hemispheres to the MRI volume of a reference brain: position and spatial variability of the optic radiation. Neuroimage 1999, 10(5):489-499.
23. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002, 35(4):625-642.
24. Cannestra A.F., Santori E.M., Holmes C.J., Toga A.W. A three-dimensional multimodality brain map of the nemestrina monkey. Brain Res. Bull. 1997, 43(2):141-148.
25. Ceritoglu C., Wang L., Selemon L.D., Csernansky J.G., Miller M.I., Ratnanather J.T. Large deformation diffeomorphic metric mapping registration of reconstructed 3D histological section images and in vivo MR images. Front. Hum. Neurosci. 2010, 4.
26. Chakeres D.W., Whitaker C.D., Dashner R.A., Scharre D.W., Beversdorf D.Q., Raychaudhury A., Schmalbrock P. High-resolution 8Tesla imaging of the formalin-fixed normal human hippocampus. Clin. Anat. 2005, 18(2):88-91.
27. Chakravarty M.M., Bertrand G., Hodge C.P., Sadikot A.F., Collins D.L. The creation of a brain atlas for image guided neurosurgery using serial histological data. Neuroimage 2006, 30(2):359-376.
28. Choe A.S., Gao Y., Li X., Compton K.B., Stepniewska I., Anderson A.W. Accuracy of image registration between MRI and light microscopy in the ex vivo brain. Magn. Reson. Imaging 2011, 29(5):683-692.
29. Cifor A., Pridmore T., Pitiot A. Smooth 3-D reconstruction for 2-D histological images. Lect. Notes Comput. Sci 2009, 5636:350-361.
30. Das S.R., Mechanic-Hamilton D., Pluta J., Korczykowski M., Detre J.A., Yushkevich P.A. Heterogeneity of functional activation during memory encoding across hippocampal subfields in temporal lobe epilepsy. Neuroimage 2011, 58(4):1121-1130.
31. Dauguet J., Delzescaux T., Cond F., Mangin J.F., Ayache N., Hantraye P., Frouin V. Three-dimensional reconstruction of stained histological slices and 3D non-linear registration with in-vivo MRI for whole baboon brain. J. Neurosci. Methods 2007, 164(1):191-204.
32. 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(2):530-538.
33. Dawe R.J., Bennett D.A., Schneider J.A., Vasireddi S.K., Arfanakis K. Postmortem MRI of human brain hemispheres: T2 relaxation times during formaldehyde fixation. Magn. Reson. Med. 2009, 61(4):810-818.
34. Duvernoy H. The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI 2005, Springer.
35. Ekstrom A.D., Bazih A.J., Suthana N.A., Al-Hakim R., Ogura K., Zeineh M., Burggren A.C., Bookheimer S.Y. Advances in high-resolution imaging and computational unfolding of the human hippocampus. Neuroimage 2009, 47(1):42-49.
36. Fanselow M.S., Dong H.-W. Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron 2010, 65(1):7-19.
37. Fatterpekar G.M., Naidich T.P., Delman B.N., Aguinaldo J.G., Gultekin S.H., Sherwood C.C., Hof P.R., Drayer B.P., Fayad Z.A. Cytoarchitecture of the human cerebral cortex: MR microscopy of excised specimens at 9.4Tesla. Am. J. Neuroradiol. 2002, 23(8):1313-1321.
38. Feuerstein M., Heibel H., Gardiazabal J., Navab N., Groher M. Reconstruction of 3-D histology images by simultaneous deformable registration. Med. Image Comput. Comput. Assist. Interv. 2011, 14(2):582-589.
39. Fischl B., Stevens A.A., Rajendran N., Yeo B.T., Greve D.N., Van Leemput K., Polimeni J.R., Kakunoori S., Buckner R.L., Pacheco J., Salat D.H., Melcher J., Frosch M.P., Hyman B.T., Grant P.E., Rosen B.R., van der Kouwe A.J., Wiggins G.C., Wald L.L., Augustinack J.C. Predicting the location of entorhinal cortex from MRI. Neuroimage 2009, 47(1):8-17.
40. Frisoni G.B., Jack C.R. Harmonization of magnetic resonance-based manual hippocampal segmentation: a mandatory step for wide clinical use. Alzheimers Dement. 2011, 7(2):171-174.
41. Gefen S., Tretiak O., Nissanov J. Elastic 3-D alignment of rat brain histological images. IEEE Trans. Med. Imaging 2003, 22(11):1480-1489.
42. Geuze E., Vermetten E., Bremner J.D. MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Mol. Psychiatry 2004, 10(2):160-184.
43. 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(14):4491-4500.
44. Groen H.C., van Walsum T., Rozie S., Klein S., van Gaalen K., Gijsen F.J.H., Wielopolski P.A., van Beusekom H.M.M., de Crom R., Verhagen H.J.M. Three-dimensional registration of histology of human atherosclerotic carotid plaques to in-vivo imaging. J. Biomech. 2010, 43(11):2087-2092.
45. Guest E., Baldock R. Automatic reconstruction of serial sections using the finite element method. Bioimaging 1995, 3(4):154-167.
46. Hanseeuw B.J., Van Leemput K., Kavec M., Grandin C., Seron X., Ivanoiu A. Mild cognitive impairment: differential atrophy in the hippocampal subfields. Am. J. Neuroradiol. 2011, 32(9):1658-1661.
47. Harding A., Halliday G., Kril J. Variation in hippocampal neuron number with age and brain volume. Cereb. Cortex 1998, 8(8):710-718.
48. Henry T.R., Chupin M., Lehéricy S., Strupp J.P., Sikora M.A., Zhiyi Y.S., Ugurbil K., Van de Moortele P.F. Hippocampal sclerosis in temporal lobe epilepsy: findings at 7T. Radiology 2011, 261(1):199-209.
49. Hess A., Lohmann K., Gundelfinger E.D., Scheich H. A new method for reliable and efficient reconstruction of 3-dimensional images from autoradiographs of brain sections. J. Neurosci. Methods 1998, 84(1):77-86.
50. Jack C.R., Barkhof F., Bernstein M.A., Cantillon M., Cole P.E., DeCarli C., Dubois B., Duchesne S., Fox N.C., Frisoni G.B., Hampel H., Hill D.L., Johnson K., Mangin J.-F., Scheltens P., Schwarz A.J., Sperling R., Suhy J., Thompson P.M., Weiner M., Foster N.L. Steps to standardization and validation of hippocampal volumetry as a biomarker in clinical trials and diagnostic criterion for Alzheimer's disease. Alzheimers Dement. 2011, 7(4):474-485. (e4).
51. Ju T., Warren J., Carson J., Bello M., Kakadiaris I., Chiu W., Thaller C., Eichele G. 3D volume reconstruction of a mouse brain from histological sections using warp filtering. J. Neurosci. Methods 2006, 156(1):84-100.
52. Kirwan C.B., Jones C.K., Miller M.I., Stark C.E. High-resolution fMRI investigation of the medial temporal lobe. Hum. Brain Mapp. 2007, 28(10):959-966.
53. Kluver H., Barrera E. A method for the combined staining of cells and fibers in the nervous system. J. Neuropathol. Exp. Neurol. 1953, 12(4):400-403.
54. Krauth A., Blanc R., Poveda A., Jeanmonod D., Morel A., Székely G. A mean three-dimensional atlas of the human thalamus: generation from multiple histological data. Neuroimage 2010, 49(3):2053-2062.
55. Krinidis S., Nikou C., Pitas I. Reconstruction of serially acquired slices using physics-based modeling. IEEE Trans. Inf. Technol. Biomed. 2003, 7(4):394-403.
56. La Joie R., Fouquet M., Mézenge F., Landeau B., Villain N., Mevel K., Pélerin A., Eustache F., Desgranges B., Chételat G. Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage 2010, 53(2):506-514.
57. Lebenberg J., Hérard A.S., Dubois A., Dauguet J., Frouin V., Dhenain M., Hantraye P., Delzescaux T. Validation of MRI-based 3D digital atlas registration with histological and autoradiographic volumes: an anatomofunctional transgenic mouse brain imaging study. Neuroimage 2010, 51(3):1037.
58. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2006, 445(7124):168-176.
59. Leutgeb J.K., Leutgeb S., Moser M.B., Moser E.I. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 2007, 315(5814):961-966.
60. Li X., Yankeelov T.E., Rosen G.D., Gore J.C., Dawant B.M. Enhancement of histological volumes through averaging and their use for the analysis of magnetic resonance images. Magn. Reson. Imaging 2009, 27(3):401-416.
61. Lisman J.E., Otmakhova N.A. Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 2001, 11(5):551-568.
62. Lorente de Nó R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 1934, 46:113-177.
63. MacKenzie-Graham A., Lee E.F., Dinov I.D., Bota M., Shattuck D.W., Ruffins S., Yuan H., Konstantinidis F., Pitiot A., Ding Y. A multimodal, multidimensional atlas of the C57BL/6J mouse brain. J. Anat. 2004, 204(2):93-102.
64. Mai J.K., Paxinos G. The Human Nervous System 2011, Academic Press.
65. Malandain G., Bardinet E., Nelissen K., Vanduffel W. Fusion of autoradiographs with an MR volume using 2-D and 3-D linear transformations. Neuroimage 2004, 23(1):111-127.
66. Malykhin N., Lebel R., Coupland N., Wilman A., Carter R. In vivo quantification of hippocampal subfields using 4.7T fast spin echo imaging. Neuroimage 2010, 49(2):1224-1230.
67. McLaren D.G., Kosmatka K.J., Oakes T.R., Kroenke C.D., Kohama S.G., Matochik J.A., Ingram D.K., Johnson S.C. A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage 2009, 45(1):52-59.
68. Meyer C.R., Moffat B.A., Kuszpit K., Bland P.L., Chenevert T.L., Rehemtulla A., Ross B.D. A methodology for registration of a histological slide and in vivo MRI volume based on optimizing mutual information. Mol. Imaging 2006, 5(1):16.
69. Milner B., Johnsrude I., Crane J. Right medial temporal-lobe contribution to object-location memory. Philos. Trans. R. Soc. B 1997, 352(1360):1469-1474.
70. Mueller S.G., Weiner M.W. Selective effect of age, apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus 2009, 19(6):558-564.
71. Mueller S., Stables L., Du A., Schuff N., Truran D., Cashdollar N., Weiner M. Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol. Aging 2007, 28(5):719-726.
72. Newman J.D., Kenkel W.M., Aronoff E.C., Bock N.A., Zametkin M.R., Silva A.C. A combined histological and MRI brain atlas of the common marmoset monkey, Callithrix jacchus. Brain Res. Rev. 2009, 62(1):1-18.
73. Nikou C., Heitz F., Nehlig A., Namer I.J., Armspach J.P. A robust statistics-based global energy function for the alignment of serially acquired autoradiographic sections. J. Neurosci. Methods 2003, 124(1):93-102.
74. Nunn J.A., Graydon F.J.X., Polkey C.E., Morris R.G. Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration. Brain 1999, 122(1):47-59.
75. Ourselin S., Bardinet E., Dormont D., Malandain G., Roche A., Ayache N., Tande D., Parain K., Yelnik J. Fusion of histological sections and MR images: towards the construction of an atlas of the human basal ganglia. Lect. Notes Comput. Sci. 2001, 2208:743-751.
76. Ourselin S., Roche A., Subsol G., Pennec X., Ayache N. Reconstructing a 3D structure from serial histological sections. Image Vision Comput. 2001, 19(1):25-31.
77. Park H., Piert M.R., Khan A., Shah R., Hussain H., Siddiqui J., Meyer C.R. Registration methodology for histological sections and in-vivo imaging of human prostate. Acad. Radiol. 2008, 15(8):1027.
78. Pfefferbaum A., Sullivan E.V., Adalsteinsson E., Garrick T., Harper C. Postmortem MR imaging of formalin-fixed human brain. Neuroimage 2004, 21(4):1585-1595.
79. Pitiot A., Bardinet E., Thompson P., Malandain G. Piecewise affine registration of biological images for volume reconstruction. Med. Image Anal. 2006, 10(3):465-483.
80. Pluta J., Yushkevich P., Das S., Wolk D. In vivo analysis of hippocampal subfield atrophy in mild cognitive impairment via semi-automatic segmentation of T2-weighted MRI. J. Alzheimers Dis. 2012, 31(1):85-99.
81. Poppenk J., Moscovitch M. A hippocampal marker of recollection memory ability among healthy young adults: contributions of posterior and anterior segments. Neuron 2011, 72(6):931-937.
82. Price J.L., Ko A.I., Wade M.J., Tsou S.K., McKeel D.W., Morris J.C. Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch. Neurol. 2001, 58:1395-1402.
83. Purger D., McNutt T., Achanta P., Quiones-Hinojosa A., Wong J., Ford E. A histology-based atlas of the C57BL/6J mouse brain deformably registered to in vivo MRI for localized radiation and surgical targeting. Phys. Med. Biol. 2009, 54(24):7315.
84. Rangarajan A., Chui H., Mjolsness E., Pappu S., Davachi L., Goldman-Rakic P., Duncan J. A robust point-matching algorithm for autoradiograph alignment. Med. Image Anal. 1997, 1(4):379-398.
85. Rosazza C., Minati L., Ghielmetti F., Maccagnano E., Erbetta A., Villani F., Epifani F., Spreafico R., Bruzzone M. Engagement of the medial temporal lobe in verbal and nonverbal memory: assessment with functional MR imaging in healthy subjects. Am. J. Neuroradiol. 2009, 30(6):1134-1141.
86. Saleem K., Logothetis N. A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates 2012, Academic Press.
87. Schormann T., Dabringhaus A., Zilles K. Statistics of deformations in histology and application to improved alignment with MRI. IEEE Trans. Med. Imaging 1995, 14(1):25-35.
88. Shepherd T.M., Zarslan E., Yachnis A.T., King M.A., Blackband S.J. Diffusion tensor microscopy indicates the cytoarchitectural basis for diffusion anisotropy in the human hippocampus. Am. J. Neuroradiol. 2007, 28(5):958-964.
89. Shing Y.L., Rodrigue K.M., Kennedy K.M., Fandakova Y., Bodammer N., Werkle-Bergner M., Lindenberger U., Raz N. Hippocampal subfield volumes: age, vascular risk, and correlation with associative memory. Front. Aging Neurosci. 2011, 3.
90. Simic G., Kostovic I., Winblad B., Bogdanovic N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 1997, 379(4):482-494.
91. Simmons D.M., Swanson L.W. Comparing histological data from different brains: sources of error and strategies for minimizing them. Brain Res. Rev. 2009, 60(2):349.
92. Small S.A., Nava A.S., Perera G.M., DeLaPaz R., Mayeux R., Stern Y. Circuit mechanisms underlying memory encoding and retrieval in the long axis of the hippocampal formation. Nat. Neurosci. 2001, 4(4):442.
93. Small S.A., Schobel S.A., Buxton R.B., Witter M.P., Barnes C.A. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 2011, 12(10):585-601.
94. Squire L.R., Stark C.E., Clark R.E. The medial temporal lobe. Annu. Rev. Neurosci. 2004, 27(1):279-306.
95. Strange B.A., Fletcher P.C., Henson R.N.A., Friston K.J., Dolan R.J. Segregating the functions of human hippocampus. Proc. Natl. Acad. Sci. 1999, 96(7):4034-4039.
96. Suthana N.A., Ekstrom A.D., Moshirvaziri S., Knowlton B., Bookheimer S.Y. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J. Neurosci. 2009, 29(34):10512-10519.
97. Thomas B.P., Welch E.B., Niederhauser B.D., Whetsell W.O., Anderson A.W., Gore J.C., Avison M.J., Creasy J.L. High-resolution 7T MRI of the human hippocampus in vivo. J. Magn. Reson. Imaging 2008, 28(5):1266-1272.
98. Toga A.W., Goldkorn A., Ambach K., Chao K., Quinn B.C., Yao P. Postmortem cryosectioning as an anatomic reference for human brain mapping. Comput. Med. Imaging Graph. 1997, 21(2):131-141.
99. 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(6):549-557.
100. van Strien N.M., Widere M., van de Berg W.D.J., Uylings H.B.M. Imaging hippocampal subregions with in vivo MRI: advances and limitations. Nat. Rev. Neurosci. 2011, 13(1):70-70.
101. Wang L., Swank J.S., Glick I.E., Gado M.H., Miller M.I., Morris J.C., Csernansky J.G. Changes in hippocampal volume and shape across time distinguish dementia of the Alzheimer type from healthy aging. Neuroimage 2003, 200(2):667-682.
102. West M.J., Gundersen H.J.G. Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 1990, 296(1):1-22.
103. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344(8925):769-772.
104. Wieshmann U.C., Symms M.R., Mottershead J.P., MacManus D.G., Barker G.J., Tofts P.S., Revesz T., Stevens J.M., Shorvon S.D. Hippocampal layers on high resolution magnetic resonance images: real or imaginary?. J. Anat. 1999, 195(1):131-135.
105. Winterburn J.L., Pruessner J.C., Chavez S., Schira M., Lobaugh N.J., Voineskos A.N., Chakravarty M.M. A novel in vivo atlas of human hippocampal subfields using high-resolution 3T magnetic resonance imaging. Neuroimage 2013, 254-265.
106. Wisse L., Gerritsen L., Zwanenburg J., Kuijf H., Luijten P., Biessels G., Geerlings M. Subfields of the hippocampal formation at 7T MRI: in vivo volumetric assessment. Neuroimage 2012, 61(4):1043-1049.
107. Xiao G., Bloch B.N., Chappelow J., Genega E.M., Rofsky N.M., Lenkinski R.E., Tomaszewski J., Feldman M.D., Rosen M., Madabhushi A. Determining histology-MRI slice correspondences for defining MRI-based disease signatures of prostate cancer. Comput. Med. Imaging Graph. 2011, 35(7):568-578.
108. Yassa M.A., Stark S.M., Bakker A., Albert M.S., Gallagher M., Stark C.E. High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic mild cognitive impairment. Neuroimage 2010, 51(3):1242-1252.
109. Yelnik J., Bardinet E., Dormont D., Malandain G., Ourselin S., Tandé D., Karachi C., Ayache N., Cornu P., Agid Y. A three-dimensional, histological and deformable atlas of the human basal ganglia. I. Atlas construction based on immunohistochemical and MRI data. Neuroimage 2007, 34(2):618-638.
110. Yong-Hing C.J., Obenaus A., Stryker R., Tong K., Sarty G.E. Magnetic resonance imaging and mathematical modeling of progressive formalin fixation of the human brain. Magn. Reson. Med. 2005, 54(2):324-332.
111. Yushkevich P., Avants B., Ng L., Hawrylycz M., Burstein P., Zhang H., Gee J. 3D mouse brain reconstruction from histology using a coarse-to-fine approach. Lect. Notes Comput. Sci. 2006, 4057:230-237.
112. Yushkevich P.A., Piven J., Cody Hazlett H., Gimpel Smith R., Ho S., Gee J.C., Gerig G. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006, 31(3):1116-1128.
113. Yushkevich P., Avants B., Pluta J., Das S., Minkoff D., Mechanichamilton D., Glynn S., Pickup S., Liu W., Gee J. A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4T. Neuroimage 2009, 44(2):385-398.
114. 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(4):1208-1224.
115. Zeineh M.M., Engel S.A., Bookheimer S.Y. Application of cortical unfolding techniques to functional MRI of the human hippocampal region. Neuroimage 2000, 11(6):668-683.
116. Zeineh M.M., Holdsworth S., Skare S., Atlas S.W., Bammer R. Ultra-high resolution diffusion tensor imaging of the microscopic pathways of the medial temporal lobe. Neuroimage 2012, 62(3):2065-2082.
117. Zola-Morgan S., Squire L.R. Neuroanatomy of memory. Annu. Rev. Neurosci. 1993, 16:547-563.