Organization and detailed parcellation of human hippocampal head and body regions based on a combined analysis of Cyto- and chemoarchitecture

Journal of Comparative Neurology

Volumn 523, Issue 15, 2015, Pages 2233-2253

  Ding, Song Lin ^a   Van Hoesen, Gary W ^b,c  

^a ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c NONE

Author keywords

AB_10000343; AB_10000347; AB_2314904; Calbindin; Hippocampal subfield; Immunohistochemistry; Medial temporal lobe; Neurofilament protein; Neuronal nuclear antigen; Parvalbumin; Pes hippocampi; RRIDs: AB_10048713; Subicular cortex; Uncus

Indexed keywords

AGED; ANATOMIC LANDMARK; ARTICLE; BRAIN MAPPING; BRAIN REGION; CYTOARCHITECTURE; DENTATE GYRUS; FEMALE; FUNCTIONAL ANATOMY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPOAMYGDALAR TRANSITION AREA; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PARASUBICULUM; PRESUBICULUM; PRIORITY JOURNAL; PROSUBICULUM; STAINING; SUBICULUM; TOPOGRAPHY; VERY ELDERLY; ANATOMY AND HISTOLOGY; BOOK; CYTOLOGY; HEAD; HIPPOCAMPUS; METABOLISM; MICROPHOTOGRAPHY;

CELL NUCLEUS ANTIGEN; NERVE PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN;

AGED; AGED, 80 AND OVER; ANTIGENS, NUCLEAR; ATLASES AS TOPIC; FEMALE; HEAD; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MALE; NERVE TISSUE PROTEINS; PHOTOMICROGRAPHY;

EID: 84939264227     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23786     Document Type: Article

References (65)

1. Adler DH, Pluta J, Kadivar S, Craige C, Gee JC, Avants BB, Yushkevich PA. 2014. Histology-derived volumetric annotation of the human hippocampal subfields in postmortem MRI. Neuroimage 84:505-523.
2. Adriano F, Caltagirone C, Spalletta G. 2012. Hippocampal volume reduction in first-episode and chronic schizophrenia: a review and meta-analysis. Neuroscientist 18:180-200.
3. Amaral DG, Insausti R. 1990. Hippocampal formation. In: Paxinos G, editor. The human nervous system. New York: Academic Press. p 711-755.
4. Augustinack JC, Helmer K, Huber KE, Kakunoori S, Zöllei L, Fischl B. 2010. Direct visualization of the perforant pathway in the human brain with ex vivo diffusion tensor imaging. Front Hum Neurosci 4:1-13.
5. Bakker A, Kirwan CB, Miller M, Stark CEL. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319:1640-1642.
6. Bird CM, Burgess N. 2008. The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9:182-194.
7. Bobinski M, de Leon MJ, Tarnawski M, Wegiel J, Bobinski M, Reisberg B, Miller DC, Wisniewski HM. 1998. Neuronal and volume loss in CA1 of the hippocampal formation uniquely predicts duration and severity of Alzheimer disease. Brain Res 805:267-269.
8. Bonnici HM, Chadwick MJ, Kumaran D, Hassabis D, Weiskopf N, Maguire EA. 2012. Multi-voxel pattern analysis in human hippocampal subfields. Front Hum Neurosci 6:290.
9. Braak H. 1980. Architectonics of the human telencephalic cortex. New York: Springer.
10. Breyer T, Wanke I, Maderwald S, Woermann FG, Kraff O, Theysohn JM, Ebner A, Forsting M, Ladd ME, Schlamann M. 2010. Imaging of patients with hippocampal sclerosis at 7 Tesla: initial results. Acad Radiol 17:421-426.
11. Campbell MJ, Morrison JH. 1989. Monoclonal antibody to neurofilament protein (NPNFP) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191-205.
12. Coras R, Pauli E, Li J, Schwarz M, Rössler K, Buchfelder M, Hamer H, Stefan H, Blumcke I. 2014a. Differential influence of hippocampal subfields to memory formation: insights from patients with temporal lobe epilepsy. Brain 137:1945-1957.
13. Coras R, Milesi G, Zucca I, Mastropietro A, Scotti A, Figini M, Mühlebner A, Hess A, Graf W, Tringali G, Blümcke I, Villani F, Didato G, Frassoni C, Spreafico R, Garbelli R. 2014b. 7T MRI features in control human hippocampus and hippocampal sclerosis: an ex vivo study with histologic correlations. Epilepsia 55:2003-2016.
14. Ding SL. 2013. Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. J Comp Neurol 521:4145-4162.
15. Ding SL, Van Hoesen GW. 2010. Borders, extent, and topography of human perirhinal cortex as revealed using multiple modern neuroanatomical and pathological markers. Hum Brain Mapp 31:1359-1379.
16. Ding SL, Morecraft RJ, Van Hoesen GW. 2003. Topography, cytoarchitecture, and cellular phenotypes of cortical areas that form the cingulo-parahippocampal isthmus and adjoining retrocalcarine areas in the monkey. J Comp Neurol 456:184-201.
17. Ding SL, Van Hoesen GW, Cassell MD, Poremba A. 2009. Parcellation of human temporal polar cortex: a combined analysis of multiple cytoarchitectonic, chemoarchitectonic, and pathological markers. J Comp Neurol 514:595-623.
18. Ding SL, Haber SN, Van Hoesen GW. 2010. Stratum radiatum of CA2 is an additional target of the perforant path in humans and monkeys. NeuroReport 21:245-249.
19. Duvernoy H. 2005. The human hippocampus: functional anatomy, vascularization and serial sections with MRI. New York: Springer.
20. Eriksson SH, Thom M, Bartlett PA, Symms MR, McEvoy AW, Sisodiya SM, Duncan JS. 2008. PROPELLER MRI visualizes detailed pathology of hippocampal sclerosis. Epilepsia 49:33-39.
21. Fanselow MS, Dong H-W. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
22. Fatterpekar GM, Naidich TP, Delman BN, Aguinaldo JG, Gultekin SH, Sherwood CC, Hof PR, Drayer BP, Fayad ZA. 2002. Cytoarchitecture of the human cerebral cortex: MR microscopy of excised specimens at 9.4 Tesla. AJNR Am J Neuroradiol 23:1313-1321.
23. Fischl B, Stevens AA, Rajendran N, Yeo BT, Greve DN, Van Leemput K, Polimeni JR, Kakunoori S, Buckner RL, Pacheco J, Salat DH, Melcher J, Frosch MP, Hyman BT, Grant PE, Rosen BR, van der Kouwe AJ, Wiggins GC, Wald LL, Augustinack JC. 2009. Predicting the location of entorhinal cortex from MRI. Neuroimage 47:8-17.
24. Godsil BP, Kiss JP, Spedding M, Jay TM. 2013. The hippocampal-prefrontal pathway: the weak link in psychiatric disorders? Eur Neuropsychopharmacol 23:1165-1181.
25. Goubran M, Rudko DA, Santyr B, Gati J, Szekeres T, Peters TM, Khan AR. 2014. In vivo normative atlas of the hippocampal subfields using multi-echo susceptibility imaging at 7 Tesla. Hum Brain Mapp 35:3588-3601.
26. Hatanpaa KJ, Raisanen JM, Herndon E, Burns DK, Foong C, Habib AA, White CL 3rd. 2014. Hippocampal sclerosis in dementia, epilepsy, and ischemic injury: differential vulnerability of hippocampal subfields. J Neuropathol Exp Neurol 73:136-142.
27. Henry TR, Chupin M, Lehéricy S, Strupp JP, Sikora MA, Zhiyi YS, Ugurbil K, Van de Moortele PF. 2011. Hippocampal sclerosis in temporal lobe epilepsy: findings at 7 T. Radiology 261:199-209.
28. Hitti FL, Siegelbaum SA. 2014. The hippocampal CA2 region is essential for social memory. Nature 508:88-92.
29. Hof PR, Morrison JH. 1991. Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer's disease. Exp Neurol 111:293-301.
30. Hof PR, Morrison JH. 1995. Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161-186.
31. Hof PR, Mufson EJ, Morrison JH. 1995a. Human orbitofrontal cortex: cytoarchitecture and quantitative immunohistochemical parcellation. J Comp Neurol 359:48-68.
32. Hof PR, Nimchinsky EA, Morrison JH. 1995b. Neurochemical phenotype of corticocortical connections in the macaque monkey: quantitative analysis of a subset of neurofilament protein-immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices. J Comp Neurol 362:109-133.
33. Hof PR, Ungerleider LG, Webster MJ, Gattass R, Adams MM, Sailstad CA, Morrison JH. 1996. Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. J Comp Neurol 376:112-127.
34. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV. 1990. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10:267-282.
35. Jones MW, McHugh TJ. 2011. Updating hippocampal representations: CA2 joins the circuit. Trends Neurosci 34:526-535.
36. La Joie R, Perrotin A, de La Sayette V, Egret S, Doeuvre L, Belliard S, Eustache F, Desgranges B, Chételat G. 2013. Hippocampal subfield volumetry in mild cognitive impairment, Alzheimer's disease and semantic dementia. Neuroimage Clin 3:155-162.
37. Leutgeb JK, Leutgeb S, Moser MB, Moser EI. 2007. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
38. Mai JK, Paxinos G, Voss T. 2008. Atlas of the human brain. New York: Elsevier.
39. Mikkonen M, Soininen H, Pitkänen A. 1997. Distribution of parvalbumin-, calretinin-, and calbindin-D28k immunoreactive neurons and fibers in the human entorhinal cortex. J Comp Neurol 388:64-88.
40. Mueller SG, Laxer KD, Barakos J, Cheong I, Garcia P, Weiner MW. 2009. Subfield atrophy pattern in temporal lobe epilepsy with and without mesial sclerosis detected by high-resolution MRI at 4 Tesla: preliminary results. Epilepsia 50:1474-1483.
41. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
42. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR. 1997. Neurofilament and calcium-binding proteins in the human cingulate cortex. J Comp Neurol 384:597-620.
43. O'Mara SM, Sanchez-Vives MV, Brotons-Mas JR, O'Hare E. 2009. Roles for the subiculum in spatial information processing, memory, motivation and the temporal control of behaviour. Prog Neuropsychopharmacol Biol Psychiatry 33:782-790.
44. Pascual B, Masdeu JC, Hollenbeck M, Makris N, Insausti R, Ding SL, Dickerson BC. 2015. Large-scale brain networks of the human left temporal pole: a functional connectivity MRI study. Cereb Cortex 25:680-702.
45. Pluta J, Yushkevich P, Das S, Wolk D. 2012. In vivo analysis of hippocampal subfield atrophy in mild cognitive impairment via semi-automatic segmentation of T2-weighted MRI. J Alzheimers Dis 31:85-99.
46. Poppenk J, Evensmoen HR, Moscovitch M, Nadel L. 2013. Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230-240.
47. Price JL, Ko AI, Wade MJ, Tsou SK, McKeel DW, Morris JC. 2001. Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch Neurol 58:1395-1402.
48. Prudent V, Kumar A, Liu S, Wiggins G, Malaspina D, Gonen O. 2010. Human hippocampal subfields in young adults at 7.0 T: feasibility of imaging. Radiology 254:900-906.
49. Rosene DL, Van Hoesen GW. 1987. The hippocampal formation of the primate brain: a review of some comparative aspects of cytoarchitecture and connections. In: Jones EG, Peters A, editors. Cerebral cortex. New York: Plenum. p 345-456.
50. Shepherd TM, Ozarslan E, Yachnis AT, King MA, Blackband SJ. 2007. Diffusion tensor microscopy indicates the cytoarchitectural basis for diffusion anisotropy in the human hippocampus. AJNR Am J Neuroradiol 28:958-964.
51. Squire LR, Stark CE, Clark RE. 2004. The medial temporal lobe. Annu Rev Neurosci 27:279-306.
52. Suthana NA, Ekstrom AD, Moshirvaziri S, Knowlton B, Bookheimer SY. 2009. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J Neurosci 29:10512-10519.
53. Tabuchi E, Endo S, Ono T, Nishijo H, Kuze S, Kogure K. 1992. Hippocampal neuronal damage after transient forebrain ischemia in monkeys. Brain Res Bull 29:685-690.
54. Thom M. 2014. Hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol 40:520-543.
55. Urbach H, Huppertz HJ, Schwarzwald R, Becker AJ, Wagner J, Bahri MD, Tschampa HJ. 2014. Is the type and extent of hippocampal sclerosis measurable on high-resolution MRI? Neuroradiology 56:731-735.
56. Van Hoesen GW, Hyman BT. 1990. Hippocampal formation: anatomy and the patterns of pathology in Alzheimer's disease. Prog Brain Res 83: 445-457.
57. Van Leemput K, Bakkour A, Benner T, Wiggins G, Wald LL, Augustinack J, Dickerson BC, Golland P, Fischl B. 2009. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 19:549-557.
58. Vogt BA, Vogt LJ, Perl DP, Hof PR. 2001.Cytology of human caudomedial cingulate, retrosplenial, and caudal parahippocampal cortices. J Comp Neurol 438:353-376.
59. West MJ, Coleman PD, Flood DG, Troncoso JC. 1994. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 344:769-772.
60. Winterburn JL, Pruessner JC, Chavez S, Schira M, Lobaugh NJ, Voineskos AN, Chakravarty MM. 2013. A novel in vivo atlas of human hippocampal subfields using high-resolution 3 T magnetic resonance imaging. Neuroimage 74:254-265.
61. Wisse L, Gerritsen L, Zwanenburg J, Kuijf H, Luijten P, Biessels G, Geerlings M. 2012. Subfields of the hippocampal formation at 7 T MRI: in vivo volumetric assessment. Neuroimage 61:1043-1049.
62. Wolbers T, Hegarty M. 2010. What determines our navigational abilities? Trends Cogn Sci 14:138-146.
63. Yushkevich P, Avants B, Pluta J, Das S, Minkoff D, Mechanichamilton D, Glynn S, Pickup S, Liu W, Gee J. 2009. A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4 T. Neuroimage 44:385-398.
64. Yushkevich PA, Wang H, Pluta J, Das SR, Craige C, Avants BB, Weiner MW, Mueller S. 2010. Nearly automatic segmentation of hippocampal subfields in in vivo focal T2-weighted MRI. Neuroimage 53:1208-1224.
65. Zeineh MM, Holdsworth S, Skare S, Atlas SW, Bammer R. 2012. Ultra-high resolution diffusion tensor imaging of the microscopic pathways of the medial temporal lobe. Neuroimage 62:2065-2082.