Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease

Journal of Comparative Neurology

Volumn 379, Issue 4, 1997, Pages 482-494

  Šimić, Goran ^a   Kostović, Ivica ^a   Winblad, Bengt ^b   Bogdanović, Nenad ^b  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

cortex; memory; neurobiology; stereology

Indexed keywords

AGING; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HISTOLOGY; HUMAN; HUMAN TISSUE; MALE; MEMORY; NERVE CELL; PATHOGENESIS; PRIORITY JOURNAL; SUBICULUM;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; CASE-CONTROL STUDIES; CELL COUNT; CELL SIZE; HIPPOCAMPUS; HUMANS; MIDDLE AGED; NEURONS; REFERENCE VALUES;

EID: 0031046970     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970324)379:4<482::AID-CNE2>3.0.CO;2-Z     Document Type: Article

References (94)

1. Abercrombie, M. (1946) Estimation of nuclear populations from microtome sections. Anat. Rec. 94:239-247.
2. Agduhr, E. (1941) A contribution to the technique of determining the number of nerve cells per volume unit of tissue. Anat. Rec. 80:191-202.
3. Alafuzoff, I., K. Iqbal, H. Friden, R. Adolfsson, and B. Winblad (1987) Histopathological criteria for progressive dementia disorders: Clinicalpathological correlation and classification by multivariate data analysis. Acta Neuropathol. 74:209-225.
4. American Psychiatric Association (1987) Diagnostic and Statistical Manual of Mental Disorders, Third Edition, Revised. Washington, DC: American Psychiatric Association.
5. Arriagada, P.V., K. Marzloff, and B.T. Hyman (1992) Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology 42:1681-1688.
6. Ball, M.J. (1977) Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. Acta Neuropathol. 37:111-118.
7. Ball, M.J., M. Fisman, V. Hachinski, V. Blume, A. Fox, V.A. Kral, A.J. Kirshen, H. Fox, and H. Merskey (1985) A new definition of Alzheimer's disease: A hippocampal dementia. Lancet 1:14-16.
8. Berg, L. (1985) Does Alzheimer's disease represent an exaggeration of normal aging? Arch. Neurol. 42:737-739.
9. Bobinski, M., J. Weigel, H.M. Wisniewski, M. Tarnawski, B. Reisberg, B. Mlodzik, M.J. de Leon, and D.C. Miller (1995) Atrophy of hippocampal formation subdivisions correlates with stage and duration of Alzheimer's disease. Dementia 6:205-210.
10. Bodganović, N., and J.H. Morris (1995) Diagnostic criteria for Alzheimer's disease in multi-centre brain banking. In F.F. Cruz-Sanchez, R. Ravid, and M.L. Cuzner (eds): Neuropathological Diagnostic Criteria for Brain Banking. Amsterdam: IOS Press, pp. 20-29.
11. Bok, S.T. (1959) Histonomy of the Cerebral Cortex. Amsterdam: Elsevier.
12. Bouras, C., P.R. Hof, and J.H. Morrison (1993) Neurofibrillary tangle densities in the hippocampal formation in a non-demented population define subgroups of patients with differential early pathological changes. Neurosci. Lett. 153:131-135.
13. Braak, H. (1972) Zur pigmentarchitektonik der grosshirnrinde des menschen. II. Subiculum. Z. Zellforsch. 131:235-254.
14. Braak, H. (1974) On the structure of the human archicortex. I. The Cornu ammonis. A Golgi and pigment architectonic study. Cell Tissue Res. 152:349-383.
15. Braak, H. (1980) Architectonics of the Human Telencephalic Cortex. Studies of Brain Function, Vol. 4. Berlin: Springer, p. 147.
16. Braak, H., and E. Braak (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 82:239-259.
17. Brodmann, K. (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: A. Barth.
18. Burke, D.M., and L.L. Light (1981) Memory and aging. Psychol. Bull. 90:513-546.
19. Cavalieri, B. (1966) Geometria Degli Indivisibili. Torino: Unione Tipografico.
20. Coggeshall, R.E. (1992) A consideration of neural counting methods. Trends Neurosci. 15:9-13.
21. Coggeshall, R.E., and H.A. Lekan (1996) Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J. Comp. Neurol. 364:6-15.
22. Coleman, P.D., and D.G. Flood (1987) Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol. Aging 8:521-545.
23. DeLacoste, M.C., and C.L. White (1993) The role of cortical connectivity in Alzheimer's disease pathogenesis: A review and model system. Neurobiol. Aging 14:1-16.
24. De la Monte, S.M. (1989) Quantitation of cerebral atrophy in preclinical and end-stage Alzheimer's disease. Ann. Neurol. 25:450-459.
25. De Leon, M.J., A.E. George, L.A. Stylopoulos, G. Smith, and D.C. Miller (1989) Early marker for Alzheimer's disease: The atrophic hippocampus. Lancet 9:672-673.
26. Duvernoy, H.M. (1988) The Human Hippocampus. An Atlas of Applied Anatomy. München: J.F. Bergman.
27. Erkinjuntti, T., D.H. Lee, F. Gao, R. Steenhuis, M. Eliasziw, R. Fry, H. Merskey, and V.C. Hachinski (1993) Temporal lobe atrophy on magnetic resonance imaging in diagnosis of early Alzheimer's disease. Arch. Neurol. 50:305-310.
28. Floderus, S. (1944) Untersuchungen über den Bau der menschlichen Hypophyse mit besonderer Berücksichtigung der qualitativen mikromorphologischen Verhältnisse. APMIS 53:1-276.
29. Friedland, R.P., E. Koss, J.V. Haxby, C.L. Grady, J. Luxenberg, and M.B. Schapiro (1988) Alzheimer's disease: Clinical and biological heterogeneity. Ann. Intern. Med. 109:298-311.
30. Gertz, H.-J., H. Krüger, S. Patt, and J. Cervos-Navarro (1991) Tangle-bearing neurons show more extensive dendritic trees than tangle-free neurons in area CA1 of the hippocampus in Alzheimer's disease. Brain Res. 548:260-266.
31. Gertz, S.D., R. Lindenberg, and G.W. Piavis (1972) Structural variations in the rostral human hippocampus. Hopkins Med. J. 130:367-376.
32. Giacomini, C.H. (1884) Fascia dentata du grand hippocampe dans le cerveau de l'homme. Arch. Ital. Biol. 5:396-417.
33. Gundersen, H.J.G. (1986) Stereology of arbitrary particles. A review of unbiased number and size estimators and a presentation of some new ones, in memory of William Thompson. J. Microsc. 143:3-45.
34. Gundersen, H.J.G., and E.B. Jensen (1987) The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147:229-263.
35. Gundersen, H.J.G., P. Bagger, T.F. Bendtsen, S.M. Evans, L. Korbo, N. Marcussen, A. Møller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sørensen, A. Vesterby, and M.J. West (1988a) The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
36. Gundersen, H.J.G., T.F. Bendtsen, L. Korbo, N. Marcussen, A. Møller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sørensen, A. Vesterby, and M.J. West (1988b) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379-394.
37. Hardy, J. (1996) Molecular genetics of Alzheimer's disease. Acta Neurol. Scand. 93:13-17.
38. Hodges, J.R., D.P. Salmon, and N. Butters (1992) Semantic memory impairment in Alzheimer's disease: Failure to access or degraded knowledge? Neuropsychologia 4:301-314.
39. Hof, P.R., and J.H. Morrison (1994) The cellular basis of cortical disconnection in Alzheimer's disease and relating dementing conditions. In R.D. Terry, R. Katzman, and K.L. Bick (eds): Alzheimer's Disease. New York: Raven Press, pp. 197-229.
40. Huesgen, C.T., P.C. Burger, B.J. Crain, and G.A. Johnson (1993) In vitro microscopy of the hippocampus in Alzheimer's disease. Neurology 43:145-152.
41. Hyman, B.T., A.R. Damasio, G.W. Van Hoesen, and C.L. Barnes (1984) Alzheimer's disease: Cell specific pathology isolates the hippocampal formation. Science 225:1168-1170.
42. Hyman, B.T., G.W. Van Hoesen, L.J. Kromer, and A.R. Damasio (1986) Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann. Neurol. 20:472-481.
43. Hyman, B.T., L.J. Kromer, and G.W. Van Hoesen (1987) Reinnervation of the hippocampal perforant pathway zone in Alzheimer's disease. Ann. Neurol. 21:259-267.
44. Jarvik, L. (1978) Genetic factors and chromosomal aberrations in Alzheimer's disease, senile dementia, and related disorders. In R. Katzman, R.D. Terry, and K.L. Bick, KL (eds): Alzheimer's Disease. New York: Raven Press, pp. 273-278.
45. Jerison, J. (1973) Evolution of the Brain and Intelligence. New York: Academic Press.
46. Jobst, K.A., A.D. Smith, and M. Szatmari (1994) Rapidly progressing atrophy of medial temporal lobe in Alzheimer's disease. Lancet 343:829-830.
47. Kesslak, J.P., O. Nalcioglu, and C.W. Cotman (1991) Quantification of magnetic resonance scans for hippocampal and parahippocampal atrophy in Alzheimer's disease. Neurology 41:51-54.
48. Khachaturian, Z.S. (1985) Diagnosis of Alzheimer's disease. Arch. Neurol. 42:1097-1105.
49. Killiany, R.J., M.B. Moss, M.S. Albert, T. Sandor, J. Tieman, and F. Jolesz (1993) Temporal lobe regions on magnetic resonance imageing identify patients with early Alzheimer's disease. Arch. Neurol. 50:949-954.
50. Kroustrup, J.P., and H.J.G. Gundersen (1993) Sampling problems in a heterogeneous organ: Quantitaton of relative and total volume of pancreatic islets by light microsopy. J. Microscopy 132:43-55.
51. Lehericy, S., M. Baulac, J. Chiras, L. Pierot, N. Martin, B. Pillon, B. Deweer, B. Dubois B., and C. Marsault (1994) Amygdalohippocampal MR volume measurements in the early stages of Alzheimer's disease. Am. J. Neuroradiol. 15:929-937.
52. Lopes da Silva, F.H., M.P. Witter, P.H. Boeijinga, and A.H.M. Lohman (1990) Anatomical organization and physiology of the limbic cortex. Physiol. Rev. 70:453-511.
53. Lorente de Nó, R. (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46:113-177.
54. Mani, R.B., J.B. Lohr, and D.V. Jeste (1986) Hippocampal pyramidal cells and aging in the human: A quantitative study of neuronal loss in sectors CA1 to CA4. Exp. Neurol. 94:29-40.
55. Mann, D.M.A. (1994) Alzheimer's disease: Progress in pathological and aetiological aspects. Rev. Clin. Gerontol. 4:43-60.
56. Mann, D.M.A., P.O. Yates, and B. Marcyniuk (1984) Alzheimer's presenile dementia, senile dementia of Alzheimer's type and Down's syndrome in middle age form an age related continuum of pathological changes. Neuropathol. Appl. Neurobiol. 10:185-207.
57. McKhann, G., D. Drachman, M. Folstein, R. Katzman, D. Price, and E.M. Stadlan (1984) Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of the Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34:939-944.
58. Mirra, S.S., M.N. Hart, and R.D. Terry (1993) Making the diagnosis of Alzheimer's disease. Arch. Pathol. Lab. Med. 117:132-144.
59. Mizutani, T., and M. Kasakava (1995) Degeneration of the intrahippocampal routes of the perforant and alvear pathways in senile dementia of Alzheimer type. Neurosci. Lett. 184:141-144.
60. Morris, R.G., and M.D. Kopelman (1986) The memory deficits in Alzheimer-type dementia: A review. Q. J. Exp. Psychol. 38:575-602.
61. Pearson, R., and L. Pearson (1976) The Vertebrate Brain. London: Academic Press.
62. Rakic, P. (1985) Limits in neurogenesis in primates. Science 227:1054-1056.
63. Rolls, E.T. (1991) The representation and storage of information in neuronal networks in the primate cerebral cortex and hippocampus. In R. Durbin, C. Miall, and G. Mitchinson (eds): The Computing Neuron. Workingham: Addison-Wesley, pp. 125-159.
64. Rosene, D.L., and G.W. Van Hoesen (1977) Hippocampal efferents reach widespread areas of the cerebral cortex and amygdala in the rhesus monkey. Science 198:315-317.
65. Rosene, D.L., and G.W. Van Hoesen (1987) The hippocampal formation of the primate brain. In E.G. Jones and A. Peters (eds): Cerebral Cortex, Vol. 6: Further Aspects of Cortical Function, Including Hippocampus. New York: Plenum, pp. 345-456.
66. Roth, M. (1986) The association of clinical and neurological findings and its bearing on the classification and aetiology of Alzheimer's disease. Br. Med. Bull. 42:42-50.
67. Sandbrink, R., T. Hartmann, C.L. Masters, and K. Beyreuther (1996) Genes contributing to Alzheimer's disease. Mol. Psychiatr. 1:27-40.
68. Saper, C.B. (1985) The value of alternative morphological approaches to Alzheimer's disease. Neurobiol. Aging 8:576-577.
69. Schwerdtfeger, W.K. (1984) Structure and Fiber Connections of the Hippocampus. A Comparative Study. Berlin: Springer, p. 74.
70. Seab, J.P., W.J. Jagust, T.S. Wong, M.S. Roos, B.R. Reed, and T.F. Budinger (1988) Quantitative NMR measurements of hippocampal atrophy in Alzheimer's disease. Magnet. Reson. Med. 8:200-208.
71. Selkoe, D.J. (1982) Molecular pathology of the aging human brain. Trends Neurosci. 5:332-336.
72. Selkoe, D.J. (1994) Cell biology of the amyloid beta-protein precursor and the mechanism of Alzheimer's disease. Annu. Rev. Cell. Biol. 10:373-403.
73. Stephan, H. (1975) Allocortex. In W. Bargmann (ed): Handbuch der Mikroskopischen Anatomie des Menschen, Bd 4: Nervensystem, Teil 9. Berlin: Springer.
74. Stephan, H. (1983) Evolutionary trends in limbic structures. Neurosci. Biobehav. Rev. 7:367-374.
75. Stephan, H., and J. Manolescu (1980) Comparative investigations on hippocampus in insectivores and primates. Z. Mikrosk. Anat. Forsch. 94:1025-1050.
76. Sterio, D.C. (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J. Microsc. 134:127-136.
77. Swaab, D.F., and H.B.M. Uylings (1987) Density measures: Parameters to avoid. Neurobiol. Aging 8:574-576.
78. Terry, R.D., and R. Katzman (1983) Senile dementia of the Alzheimer's type: Defining a disease. In R. Katzman and R.D. Terry (eds): The Neurology of Aging. New York: FA Davis, pp. 51-84.
79. Terry, R.D., E. Masliah, D.P. Salmon, N. Butters, R. DeTeresa, R. Hill, L. Hansen, and R. Katzman (1991) Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30:572-580.
80. Tomlinson, B.E. (1989) The neuropathology of Alzheimer's disease - Issues in need of resolution. Neuropathol. Appl. Neurobiol. 15:491-512.
81. Tomlinson, B.E., G. Glessed, and M. Roth (1970) Observations on the brains of demented old people. J. Neurol. Sci. 11:205-242.
82. Traub, R.D., and R. Miles (1991) Neuronal Networks of the Hippocampus. Cambridge: University Press.
83. Ulrich, J. (1985) Alzheimer changes in nondemented patients younger than sixty-five: A possible early stage of Alzheimer's disease and senile dementia of Alzheimer's type. Ann. Neurol. 17:273-277.
84. Uylings, H.B.M., C.G. van Eden, and M.A. Hofman (1986) Morphometry of size/volume variables and comparison of their bivariate relations in the nervous system under different conditions. J. Neurosci. Methods 18:19-37.
85. Van Hoesen, G.W. (1982) The parahippocampal gyrus. New observations regarding its cortical connections in the monkey. Trends Neurosci. 5:345-350.
86. Van Hoesen, G.W., B.T. Hyman, and A.R. Damasio (1991) Entorhinal cortex in Alzheimer's disease. Hippocampus 1:1-8.
87. West, M.J. (1993) Regionally specific loss of neurons in the aging human hippocampus. Neurobiol. Aging 14:287-293.
88. West, M.J., and H.J.G. Gundersen (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296:1-22.
89. West, M.J., P.D. Coleman, D.G. Flood, and J.C. Troncoso (1994) Differences in the pattern of hippocampal neuronal loss in normal aging and Alzheimer's disease. Lancet 344:769-772.
90. Winocur, G. (1988) A neuropsychological analysis of memory loss with age. Neurobiol. Aging 9:487-494.
91. Yamazaki, M., M. Hamamoto, M. Yoshimura, Y. Itoh, and T. Miyazaki (1993) An autopsy case with recent memory disturbance, characterized by localized atrophy of parahippocampal gyrus, subiculum and amygdala. Rinsho Shinkeigaku 33:50-55.
92. Zola-Morgan, S., L.R. Squire, and D.G. Amaral (1986) Human amnesia and the temporal lobe region: Enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 6:2950-2967.
93. Zola-Morgan, S., L.R. Squire, N.L. Rempel, R.P. Clower, and D.G. Amaral (1992) Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J. Neurosci. 12:2582-2596.
94. Zuckerkandl, E. (1887) Über das Reichzentrum. Stuttgart: Enke.