Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol

NeuroImage

Volumn 111, Issue , 2015, Pages 526-541

  Yushkevich, Paul A ^a   Amaral, Robert S C ^b   Augustinack, Jean C ^c   Bender, Andrew R ^d   Bernstein, Jeffrey D ^e,f   Boccardi, Marina ^g   Bocchetta, Martina ^g,h   Burggren, Alison C ⁱ   Carr, Valerie A ^j   Chakravarty, M Mallar ^b,k   Chételat, Gaël ^l   Daugherty, Ana M ^d   Davachi, Lila ^m   Ding, Song Lin ⁿ   Ekstrom, Arne ^o   Geerlings, Mirjam I ^p   Hassan, Abdul ^o   Huang, Yushan ^q   Iglesias, J Eugenio ^c,r   La Joie, Renaud ^l   Kerchner, Geoffrey A ^e,f   LaRocque, Karen F ^j   Libby, Laura A ^o   Malykhin, Nikolai ^q   Mueller, Susanne G ^s,t   Olsen, Rosanna K ^u   Palombo, Daniela J ^v   Parekh, Mansi B ^j   Pluta, John B ^a   Preston, Alison R ^w   Pruessner, Jens C ^k,x   Ranganath, Charan ^o   Raz, Naftali ^d   Schlichting, Margaret L ^w   Schoemaker, Dorothee ^k,x   Singh, Sachi ^y   Stark, Craig E L ^z   Suthana, Nanthia ⁱ   Tompary, Alexa ^m   Turowski, Marta M ^m   Van Leemput, Koen ^c,aa   Wagner, Anthony D ^j   Wang, Lei ^y   Winterburn, Julie L ^b   Wisse, Laura E M ^p   Yassa, Michael A ^z   Zeineh, Michael M ^j   more..

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d WAYNE STATE UNIVERSITY   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Stanford Center for Memory Disorders   (United States)

^g IRCCS Centro S Giovanni di Dio Fatebenefratelli   (Italy)

^h UNIVERSITY OF BRESCIA   (Italy)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j STANFORD UNIVERSITY   (United States)

^k MCGILL UNIVERSITY   (Canada)

^l UNIVERSITÉ DE CAEN   (France)

^m NEW YORK UNIVERSITY   (United States)

ⁿ ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^o UNIVERSITY OF CALIFORNIA   (United States)

^p UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^q UNIVERSITY OF ALBERTA   (Canada)

^r BASQUE CENTER ON COGNITION   (Spain)

^s UNIVERSITY OF CALIFORNIA   (United States)

^t VETERANS AFFAIRS MEDICAL CENTER   (United States)

^u ROTMAN RESEARCH INSTITUTE   (Canada)

^v VA BOSTON HEALTHCARE SYSTEM   (United States)

^w UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^x MCGILL UNIVERSITY   (Canada)

^y NORTHWESTERN UNIVERSITY   (United States)

^z UNIVERSITY OF CALIFORNIA   (United States)

^aa TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

more..

Author keywords

CA1; CA2; CA3; Dentate gyrus; Entorhinal cortex; Hippocampal subfields; Hippocampus; Magnetic resonance imaging; Medial temporal lobe; Parahippocampal gyrus; Perirhinal cortex; Segmentation; Subiculum; Unified protocol

Indexed keywords

ADULT; ANATOMY AND HISTOLOGY; CLINICAL PROTOCOL; CLINICAL TRIAL; COMPARATIVE STUDY; HIPPOCAMPUS; HUMAN; IMAGE PROCESSING; MULTICENTER STUDY; NUCLEAR MAGNETIC RESONANCE IMAGING; PARAHIPPOCAMPAL GYRUS; PROCEDURES; STANDARDS;

ADULT; CLINICAL PROTOCOLS; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; PARAHIPPOCAMPAL GYRUS;

EID: 84939468449     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.01.004     Document Type: Article

References (81)

1. Amaral D.G., Insausti R. The hippocampal formation. The Human Nervous System 1990, Academic Press, San Diego, CA. G. Paxinos (Ed.).
2. Amaral D., Lavenex P. Hippocampal Neuroanatomy 2007, 37-114. Oxford University Press. P. Anderson (Ed.).
3. 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, 129:2867-2873.
4. Arnold S.E., Franz B.R., Gur R.C., Gur R.E., Shapiro R.M., Moberg P.J., Trojanowski J.Q. Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am. J. Psychiatry 1995, 152:738-748.
5. Augustinack J.C., Huber K.E., Stevens A.A., Roy M., Frosch M.P., van der Kouwe A.J.W., Wald L.L., Van Leemput K., McKee A.C., Fischl B. Predicting the location of human perirhinal cortex, Brodmann's area 35, from MRI. Neuroimage 2013, 64:32-42. Alzheimer's Disease Neuroimaging Initiative.
6. Bakker A., Kirwan C.B., Miller M., Stark C.E.L. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319:1640-1642.
7. Bender A.R., Daugherty A.M., Raz N. Vascular risk moderates associations between hippocampal subfield volumes and memory. J. Cogn. Neurosci. 2013, 25:1851-1862.
8. Boccardi M., Ganzola R., Bocchetta M., Pievani M., Redolfi A., Bartzokis G., Camicioli R., Csernansky J.G., de Leon M.J., deToledo Morrell L., Killiany R.J., Lehéricy S., Pantel J., Pruessner J.C., Soininen H., Watson C., Duchesne S., Jack C.R., Frisoni G.B. Survey of protocols for the manual segmentation of the hippocampus: preparatory steps towards a joint EADC-ADNI harmonized protocol. J. Alzheimers Dis. 2011, 26(Suppl. 3):61-75.
9. Boccardi M., Bocchetta M., Ganzola R., Robitaille N., Redolfi A., Duchesne S., Jack C.R., Frisoni G.B., EADC-ADNI Working Group on The Harmonized Protocol for Hippocampal Volumetry Operationalizing protocol differences for EADC-ADNI manual hippocampal segmentation. Alzheimers Dement. 2013, for the Alzheimer's Disease Neuroimaging Initiative. 10.1016/j.jalz.2013.03.001.
10. Boccardi M., Bocchetta M., Apostolova L., Barnes J., Bartzokis G., Corbetta G., DeCarli C., deToledo Morrell L., Firbank M., Ganzola R., Gerritsen L., Henneman W., Killiany R., Malykhin N., Pasqualetti P., Pruessner J., Redolfi A., Robitaille N., Soininen H., Tolomeo D., Wang L., Watson C., Wolf H., Duvernoy H., Duchesne S., Jack C., GB Frisoni for the EADC-ADNI Working Group on the Harmonized Protocol for Manual Hippocampal Segmentation Delphi definition of the EADC-ADNI harmonized protocol for hippocampal segmentation on magnetic resonance. Alzheimers Dement. 2014, 10.1016/j.jalz.2014.02.009.
11. Bocchetta M., Boccardi M., Ganzola R., Apostolova L.G., Preboske G., Wolf D., Ferrari C., Pasqualetti P., Robitaille N., Duchesne S., Jack C.R., Frisoni G.B. Harmonized benchmark labels of the hippocampus on magnetic resonance: the EADC-ADNI project. Alzheimers Dement. 2014, EADC-ADNI Working Group on The Harmonized Protocol for Manual Hippocampal Segmentation, the Alzheimer's Disease Neuroimaging Initiative, EADC-ADNI Working Group on The Harmonized Protocol for Manual Hippocampal Segmentation, the Alzheimer's Disease Neuroimaging Initiative. 10.1016/j.jalz.2013.12.019.
12. 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, 6:290.
13. Braak H., Braak E. Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol. Aging 1995, 16:271-278. (discussion 278-84).
14. Danielsson P. Euclidean distance mapping. Comput. Vision Graph 1980, 14:227-248.
15. de Lanerolle N.C., Kim J.H., Williamson A., Spencer S.S., Zaveri H.P., Eid T., Spencer D.D., Eid T. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 2003, 44:677-687.
16. Dice L.R. Measures of the amount of ecologic association between species. Ecology 1945, 26:297-302.
17. Duncan K., Tompary A., Davachi L. Associative encoding and retrieval are predicted by functional connectivity in distinct hippocampal area ca1 pathways. J. Neurosci. 2014, 34:11188-11198.
18. Duvernoy H.M. The Human Hippocampus, Functional Anatomy, Vascularization and Serial Sections With MRI 1998, Springer.
19. Duvernoy H. The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections With MRI 2005, Springer, Berlin, Germany.
20. 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, 47:42-49.
21. Fischl B., Stevens A.A., Rajendran N., Yeo B.T.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.W., Wiggins G.C., Wald L.L., Augustinack J.C. Predicting the location of entorhinal cortex from MRI. Neuroimage 2009, 47:8-17.
22. Frisoni G.B., Jack C.R. Harmonization of magnetic resonance-based manual hippocampal segmentation: a mandatory step for wide clinical use. Alzheimers Dement. 2011, 7:171-174.
23. Gloor P. The temporal lobe and limbic system. Chapter 5: The Hippocampal System 1997, 325-589. Oxford Univ. Press.
24. Goncharova I.I., Dickerson B.C., Stoub T.R., deToledo Morrell L. MRI of human entorhinal cortex: a reliable protocol for volumetric measurement. Neurobiol. Aging 2001, 22:737-745.
25. Grinstead J.W., Speck O., Paul D., Silbert L., Perkins L., Rooney W. Whole-brain FLAIR Using 3D TSE With Variable Flip Angle Readouts Optimized for 7 Tesla 2010, 3034. ISMRM, Stockholm, Sweden.
26. Hanseeuw B.J., Van Leemput K., Kavec M., Grandin C., Seron X., Ivanoiu A. Mild cognitive impairment: differential atrophy in the hippocampal subfields. AJNR Am. J. Neuroradiol. 2011, 32:1658-1661.
27. Harding A.J., Halliday G.M., Kril J.J. Variation in hippocampal neuron number with age and brain volume. Cereb. Cortex 1998, 8:710-718.
28. Henry T.R., Chupin M., Lehéricy S., Strupp J.P., Sikora M.A., Sha Z.Y., Ugurbil K., Van de Moortele P.F. Hippocampal sclerosis in temporal lobe epilepsy: findings at 7T. Radiology 2011, 261:199-209.
29. Insausti R., Amaral D.G. Hippocampal formation. The Human Nervous System 2004, 871-914. Elsevier Academic Press, Amsterdam. Second ed. G. Paxinos, J.K. Mai (Eds.).
30. Insausti R., Amaral D.G. Hippocampal formation. The Human Nervous System 2012, Elsevier Academic Press, London. Third ed. J.K. Mai, G. Paxinos (Eds.).
31. 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.
32. 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.
33. Kerchner G., Hess C., Hammond-Rosenbluth K., Xu D., Rabinovici G., Kelley D., Vigneron D., Nelson S., Miller B. Hippocampal CA1 apical neuropil atrophy in mild Alzheimer disease visualized with 7-T MRI. Neurology 2010, 75:1381-1387.
34. Kerchner G.A., Deutsch G.K., Zeineh M., Dougherty R.F., Saranathan M., Rutt B.K. Hippocampal ca1 apical neuropil atrophy and memory performance in Alzheimer's disease. Neuroimage 2012, 63:194-202.
35. Kirov I.I., Hardy C.J., Matsuda K., Messinger J., Cankurtaran C.Z., Warren M., Wiggins G.C., Perry N.N., Babb J.S., Goetz R.R., George A., Malaspina D., Gonen O. In vivo 7 tesla imaging of the dentate granule cell layer in schizophrenia. Schizophr. Res. 2013, 147(2-3):362-367.
36. Kirwan C.B., Jones C.K., Miller M.I., Stark C.E.L. High-resolution fMRI investigation of the medial temporal lobe. Hum. Brain Mapp. 2007, 28:959-966.
37. 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, 53:506-514.
38. La Joie R., Perrotin A., de La Sayette V., Egret S., Doeuvre L., Belliard S., Eustache F., Desgranges B., Chételat G. Hippocampal subfield volumetry in mild cognitive impairment, Alzheimer's disease and semantic dementia. NeuroImage 2013, 3:155-162.
39. Libby L.A., Ekstrom A.D., Ragland J.D., Ranganath C. Differential connectivity of perirhinal and parahippocampal cortices within human hippocampal subregions revealed by high-resolution functional imaging. J. Neurosci. 2012, 32:6550-6560.
40. 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.
41. Lucassen P.J., Heine V.M., Muller M.B., van der Beek E.M., Wiegant V.M., De Kloet E.R., Joels M., Fuchs E., Swaab D.F., Czeh B. Stress, depression and hippocampal apoptosis. CNS Neurol. Disord. Drug Targets 2006, 5:531-546.
42. Mai J., Paxinos G., Voss T. Atlas of the Human Brain 2008, Elsevier, New York, NY, USA.
43. Malykhin N.V., Bouchard T.P., Ogilvie C.J., Coupland N.J., Seres P., Camicioli R. Three-dimensional volumetric analysis and reconstruction of amygdala and hippocampal head, body and tail. Psychiatry Res. 2007, 155:155-165.
44. Malykhin N.V., Lebel R.M., Coupland N.J., Wilman A.H., Carter R. In vivo quantification of hippocampal subfields using 4.7T fast spin echo imaging. Neuroimage 2010, 49:1224-1230.
45. Moscovitch M., Nadel L., Winocur G., Gilboa A., Rosenbaum R.S. The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr. Opin. Neurobiol. 2006, 16:179-190.
46. Mueller S.G., Weiner M.W. Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus 2009, 19:558-564.
47. Mueller S.G., Stables L., Du A.T., Schuff N., Truran D., Cashdollar N., Weiner M.W. Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol. Aging 2007, 28:719-726.
48. Olsen R.K., Nichols E.A., Chen J., Hunt J.F., Glover G.H., Gabrieli J.D.E., Wagner A.D. Performance-related sustained and anticipatory activity in human medial temporal lobe during delayed match-to-sample. J. Neurosci. 2009, 29:11880-11890.
49. Olsen R.K., Palombo D.J., Rabin J.S., Levine B., Ryan J.D., Rosenbaum R.S. Volumetric analysis of medial temporal lobe subregions in developmental amnesia using high-resolution magnetic resonance imaging. Hippocampus 2013, 23(10):855-860.
50. Palombo D.J., Amaral R.S.C., Olsen R.K., Müller D.J., Todd R.M., Anderson A.K., Levine B. Kibra polymorphism is associated with individual differences in hippocampal subregions: evidence from anatomical segmentation using high-resolution MRI. J. Neurosci. 2013, 33:13088-13093.
51. Pereira J.B., Valls-Pedret C., Ros E., Palacios E., Falcón C., Bargalló N., Bartrés-Faz D., Wahlund L.O., Westman E., Junque C. Regional vulnerability of hippocampal subfields to aging measured by structural and diffusion MRI. Hippocampus 2013, 24(4):403-414.
52. Pipitone J., Park M.T.M., Winterburn J., Lett T.A., Lerch J.P., Pruessner J.C., Lepage M., Voineskos A.N., Chakravarty M.M., the Alzheimer's Disease Neuroimaging Initiative Multi-atlas segmentation of the whole hippocampus and subfields using multiple automatically generated templates. Neuroimage 2014, 101:494-512.
53. 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, 29:1-15.
54. Preston A.R., Bornstein A.M., Hutchinson J.B., Gaare M.E., Glover G.H., Wagner A.D. High-resolution fmri of content-sensitive subsequent memory responses in human medial temporal lobe. J. Cogn. Neurosci. 2010, 22:156-173.
55. Prudent V., Kumar A., Liu S., Wiggins G., Malaspina D., Gonen O. Human hippocampal subfields in young adults at 7.0T: feasibility of imaging. Radiology 2010, 254:900-906.
56. Pruessner J.C., Li L.M., Serles W., Pruessner M., Collins D.L., Kabani N., Lupien S., Evans A.C. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb. Cortex 2000, 10:433-442.
57. Pruessner J.C., Köhler S., Crane J., Pruessner M., Lord C., Byrne A., Kabani N., Collins D.L., Evans A.C. Volumetry of temporopolar, perirhinal, entorhinal and parahippocampal cortex from high-resolution MR images: considering the variability of the collateral sulcus. Cereb. Cortex 2002, 12:1342-1353.
58. Rosene D., Van Hoesen G.W. The hippocampal formation of the primate brain. A review of some comparative aspects of cytoarchitecture and connections. Cereb. Cortex 1987, 345-456.
59. Shrout P., Fleiss J. Intraclass correlations: uses in assessing rater reliability. Psychol. Bull. 1979, 86:420-428.
60. Simić G., Kostović I., Winblad B., Bogdanović N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 1997, 379:482-494.
61. Small S.A., Nava A.S., Perera G.M., Delapaz R., Stern Y. Evaluating the function of hippocampal subregions with high-resolution MRI in Alzheimer's disease and aging. Microsc. Res. Tech. 2000, 51:101-108.
62. Small S., Schobel S., Buxton R., Witter M., Barnes C. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 2011, 12:585-601.
63. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
64. Squire L.R., Stark C.E.L., Clarkx R.E. The medial temporal lobe. Annu. Rev. Neurosci. 2004, 27:279-306.
65. Teicher M.H., Anderson C.M., Polcari A. Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E563-E572.
66. 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.
67. van Strien N.M., Widerøe M., van de Berg W.D.J., Uylings H.B.M. Imaging hippocampal subregions with in vivo MRI: advances and limitations. Nat. Rev. Neurosci. 2012, 13:70.
68. 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, 20:667-682.
69. Wang L., Miller J.P., Gado M.H., McKeel D.W., Rothermich M., Miller M.I., Morris J.C., Csernansky J.G. Abnormalities of hippocampal surface structure in very mild dementia of the Alzheimer type. Neuroimage 2006, 30:52-60.
70. Wang Z., Neylan T.C., Mueller S.G., Lenoci M., Truran D., Marmar C.R., Weiner M.W., Schuff N. Magnetic resonance imaging of hippocampal subfields in posttraumatic stress disorder. Arch. Gen. Psychiatry 2010, 67:296-303.
71. Watson C., Andermann F., Gloor P., Jones-Gotman M., Peters T., Evans A., Olivier A., Melanson D., Leroux G. Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 1992, 42:1743-1750.
72. West M.J., Kawas C.H., Stewart W.F., Rudow G.L., Troncoso J.C. Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol. Aging 2004, 25:1205-1212.
73. Winterburn J.L., Pruessner J.C., Chavez S., Schira M.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, 74:254-265.
74. Wisse L.E.M., Gerritsen L., Zwanenburg J.J.M., Kuijf H.J., Luijten P.R., Biessels G.J., Geerlings M.I. Subfields of the hippocampal formation at 7T MRI: in vivo volumetric assessment. Neuroimage 2012, 61:1043-1049.
75. Wolk D.A., Dunfee K.L., Dickerson B.C., Aizenstein H.J., DeKosky S.T. A medial temporal lobe division of labor: insights from memory in aging and early Alzheimer disease. Hippocampus 2011, 21:461-466.
76. Yassa M.A., Stark S.M., Bakker A., Albert M.S., Gallagher M., Stark C.E.L. 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.
77. Yushkevich P.A., Pluta J.B., Wang H., Xie L., Ding S.L., Gertje E.C., Mancuso L., Kliot D., Das S.R., Wolk D.A. Automated volumetry and regional thickness analysis of hippocampal subfields and medial temporal cortical structures in mild cognitive impairment. Hum. Brain Mapp. 2015, 36(1):258-287.
78. Zeineh M.M., Engel S.A., Bookheimer S.Y. Application of cortical unfolding techniques to functional MRI of the human hippocampal region. Neuroimage 2000, 11:668-683.
79. Zeineh M.M., Engel S.A., Thompson P.M., Bookheimer S.Y. Unfolding the human hippocampus with high resolution structural and functional MRI. Anat. Rec. 2001, 265:111-120.
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. Ultra-high resolution diffusion tensor imaging of the microscopic pathways of the medial temporal lobe. Neuroimage 2012, 62:2065-2082.