Atypical form of Alzheimer's disease with prominent posterior cortical atrophy: A review of lesion distribution and circuit disconnect in cortical visual pathways

Vision Research

Volumn 37, Issue 24, 1997, Pages 3609-3625

  Hof, Patrick R ^a   Vogt, Brent A ^b   Bouras, Constantin ^a,c   Morrison, John H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Corticocortical projections; Dementia; Human vision; Occipitoparietal; Occipitotemporal

Indexed keywords

ALZHEIMER DISEASE; ARTICLE; CINGULATE GYRUS; DEMENTIA; HUMAN; HUMAN TISSUE; NEUROFIBRILLARY TANGLE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SENILE PLAQUE; SYMPTOMATOLOGY; TEMPORAL LOBE; VISUAL CORTEX; VISUAL SYSTEM;

NASA DISCIPLINE NEUROSCIENCE; NON-NASA CENTER;

AGED; ALZHEIMER DISEASE; ATROPHY; HUMANS; PARIETAL LOBE; SENILE PLAQUES; VISION DISORDERS; VISUAL CORTEX;

EID: 0030784929     PISSN: 00426989     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6989(96)00240-4     Document Type: Article

References (105)

1. Arnold, S. E., Hyman, B. T., Flory, J., Damasio, A. R. & Van Hoesen, G. W. (1991). The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cerebral Cortex, 1, 103-116.
2. Baizer, J. S., Ungerleider, L. G. & Desimone, R. (1991). Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. Journal of Neuroscience, 11, 168-190.
3. Baleydier, C. & Mauguière, F. (1987). Network organization of the connectivity between parietal area 7, posterior cingulate cortex and medial pulvinar nucleus: a double fluorescent tracer study in monkey. Experimental Brain Research, 66, 385-393.
4. Bálint, R. (1909). Seelenlähmung des "Schauens", optische Ataxie, räumliche Störung der Aufmerksamkeit. Monatsschrift für Psychia-trie und Neurologie, 25, 51-81.
5. Ball, J. A., Lantos, P. L., Jackson, M, Marsden, C. D., Scadding, J. W. & Rossor, M. N. (1993). Alien hand sign in association with Alzheimer's histopathology. Journal of Neurology, Neurosurgery, and Psychiatry, 56, 1020-1023.
6. Beach, T. G. & McGeer, E. G. (1988). Lamina-specific arrangement of astrocytic gliosis and senile plaques in Alzheimer's disease visual cortex. Brain Research, 463, 357-361.
7. Beach, T. G. & McGeer, E. G. (1992). Senile plaques, amyloid βprotein, and acetylcholinesterase fibres: laminar distributions in Alzheimer's disease striate cortex. Acta Neuropathologica, 83, 292-299.
8. Benson, D. F., Davis, R. J. & Snyder, B. D. (1988). Posterior cortical atrophy. Archives of Neurology, 45, 789-793.
9. Berthier, M. L., Leiguarda, R., Starkstein, S. E , Sevlever, G. & Taratuto, A. L. (1991). Alzheimer's disease in a patient with posterior cortical atrophy. Journal of Neurology, Neurosurgery, and Psychiatry, 54, 1110-1111.
10. Blanks, J. C., Schmidt, S. I., Torigoe, Y., Porrello, K. V., Hinton, D. R. & Blanks, R. H. I. (1996a) Retinal pathology in Alzheimer's disease. II. Regional neuron loss and glial changes in GCL. Neurobiology of Aging, 17, 385-395.
11. Blanks, J. C., Torigoe, Y., Hinton, D. R. & Blanks, R. H. I. (1996b) Retinal pathology in Alzheimer's disease. I. Ganglion cell loss in foveal/parafoveal retina. Neurobiology of Aging, 17, 377-384.
12. Braak, H., Braak, E. & Kalus, P. (1989). Alzheimer's disease: areal and laminar pathology in the occipital isocortex. Acta Neuropathologica, 77, 494-506.
13. Brodmann, K. (1909). Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellen-baues. Leipzig: Barth. [Translated version: Garey, L. J. (1994). Brodmann's "Localisation in the cerebral cortex". London: Smith Gordon].
14. Brun, A. & Englund, E. (1981). Regional pattern of degeneration in Alzheimer's disease: neuronal loss and histopathological grading. Histopathology, 5, 549-564.
15. Buée-Scherrer, V., Condamines, O., Mourton-Gilles, C., Jakes, R., Goedert, M., Pau, B. & Delacourte, A. (1996). AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Molecular Brain Research, 39, 79-88.
16. Ceccaldi, M., Poncet, M., Gambarelli, D., Guinot, H. & Billé, J. (1995). Apraxie unilatérale gauche d'aggravation progressive dans deux cas de maladie d'Alzheimer. Revue Neurologique (Paris), 151, 240-246.
17. Clarke, S. (1993). Callosal connections and functional subdivision of the human occipital cortex. In Gulyas, B., Ottoson, D. & Roland, P. E. (Eds), Functional organisation of the human visual cortex (pp. 137-150). Oxford: Pergamon Press.
18. Clarke, S. (1994). Modular organization of human extrastriate visual cortex: evidence from cytochrome oxidase pattern in normal and macular degeneration cases. European Journal of Neuroscience, 6, 725-736.
19. Clarke, S. (1995). Association and intrinsic connections of human extrastriate visual cortex. Proceedings of the Royal Society of London B, 257, 87-92.
20. Clarke, S. & Miklossy, J. (1990). Occipital cortex in man: organization of callosal connections, related myelo-and cytoarchitecture, and putative boundaries of functional visual areas. Journal of Comparative Neurology, 298, 188-214.
21. Cogan, D. G. (1985). Visual disturbances with focal progressive dementing diseae. American Journal of Ophthalmology, 100, 68-72.
22. Croisile, B., Trillet, M., Hibert, O., Cinotti, L., Le Bars, D., Mauguière, F. & Aimard, G. (1991). Désordres visuo-constructifs et alexieagraphie associés à une atrophie corticale postérieure. Revue Neurologique (Paris), 147, 138-143.
23. Cronin-Golomb, A., Suguira, R., Corkin, S. & Growdon, J. H. (1993). Incomplete achromatopsia in Alzheimer's disease. Neurobiology of Aging, 74, 471-477.
24. Crystal, H. A., Horoupian, D. S., Katzman, R. & Jotkowitz, S. (1982). Biopsy-proved Alzheimer disease presenting as a right parietal lobe syndrome. Annals of Neurology, 12, 186-188.
25. Curcio, C. A. & Drucker, D. N. (1993). Retinal ganglion cells in Alzheimer's disease and aging. Annals of Neurology, 33, 248-257.
26. Damasio, A. R. (1985). Disorders of complex visual processing: agnosias, achromatopsias, Balint's syndrome and related difficulties of orientation and construction. In Mesulam, M. M. (Ed.), Principles of behavioral neurology (pp. 259-288). Philadelphia: F.A. Davis.
27. Delacourte, A., Flament, S., Dibe, E. M., Hublau, P., Sablonnière, B., Hémon, B., Scherrer, V. & Défossez, A. (1990). Pathological proteins tau 64 and 69 are specifically expressed in the somatodendritic domain of the degenerating cortical neurons during Alzheimer's disease: demonstration with a panel of antibodies against tau proteins. Acta Neuropathologica, 80, 111-117.
28. DeYoe, E. A., Carman, G. J., Bandettini, P., Glickman, S., Wieser, J., Cox, R., Miller, D. & Neitz, J. (1996). Mapping striate and extrastriate visual areas in human cerebral cortex. Proceedings of the National Academy of Sciences USA, 93, 2382-2386.
29. DeYoe, E. A. & Van Essen, D. C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neurosciences, 11, 219-225.
30. Felleman, D. J. & Van Essen, D. C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex, 1, 1-41.
31. Flechsig, P. (1920). Anatomie des menschlichen Gehirns und Rückenmarks. Leipzig: Thieme.
32. Fletcher, W. A. (1994). Ophthalmological aspects of Alzheimer's disease. Current Opinion in Ophthalmology, 5, 38-44.
33. Fletcher, W. A. & Sharpe, J. A. (1988). Smooth pursuit dysfunction in Alzheimer's disease. Neurology, 38, 272-277.
34. Fries, W., Keizer, K. & Kuypers, H. G. J. M. (1985). Large layer VI cells in macaque striate cortex project to both superior colliculus and prestriate area V5. Experimental Brain Research, 58, 613-616.
35. Gaspar, P., Duyckaerts, C., Febvret, A., Benoit, R., Beck, R. & Berger, B. (1989). Subpopulations of somatostatin 28-immunoreactive neurons display different vulnerability in senile dementia of the Alzheimer type. Brain Research, 490, 1-13.
36. Golaz, J., Bouras, C. & Hof, P. R. (1992). Motor cortex involvement in presenile dementia: report of a case. Journal of Geriatric Psychiatry and Neurology, 5, 85-92.
37. Graff-Radford, N. R., Boiling, J. P., Earnest IV, F., Shuster, E. A., Caselli, R. J. & Brazis, P. W. (1993). Simultanagnosia as the initial sign of degenerative dementia. Mayo Clinic Proceedings, 68, 955-964.
38. Grünthal, E. (1928). Zur Hirnpathologischen Analyse der Alzheimerschen Krankheit. Psychiatrisch-Neurologische Wochenschrift, 36, 401-407.
39. Hinton, D. R., Sadun, A. A., Blanks, J. C. & Miller, C. A. (1986). Optic-nerve degeneration in Alzheimer's disease. New England Journal of Medicine, 315, 485-187.
40. Hof, P. R., Archin, N., Osmand, A. P., Dougherty, J. H., Wells, C., Bouras, C. & Morrison, J. H. (1993). Posterior cortical atrophy in Alzheimer's disease: analysis of a new case and re-evaluation of an historical report. Acta Neuropathologica, 86, 215-223.
41. Hof, P. R. & Bouras, C. (1991). Object recognition deficit in Alzheimer's disease: possible disconnection of the occipitotemporal component of the visual system. Neuroscience Letters, 122, 53-56.
42. Hof, P. R., Bouras, C., Constantinidis, J. & Morrison, J. H. (1989). Balint's syndrome in Alzheimer's disease: specific disruption of the occipito-parietal visual pathway. Brain Research, 493, 368-375.
43. Hof, P. R., Bouras, C., Constantinidis, J. & Morrison, J. H. (1990a) Selective disconnection of specific visual association pathways in cases of Alzheimer's disease presenting with Balint's syndrome. Journal of Neuropathology and Experimental Neurology, 49, 168-184.
44. Hof, P. R., Cox, K. & Morrison, J. H. (1990b) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease. I. Superior frontal and inferior temporal cortex. Journal of Comparative Neurology, 301, 44-54.
45. Hof. P. R. & Morrison, J. H. (1990). Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease. II. Primary and secondary visual cortex. Journal of Comparative Neurology, 301, 55-64.
46. Hof, P. R. & Morrison, J. H. (1991). Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer's disease. Experimental Neurology, 111, 293-301.
47. Hof, P. R. & Morrison J. H. (1994). The cellular basis of cortical disconnection in Alzheimer disease and related dementing conditions. In Terry, R. D., Katzman, R. & Bick, K. L. (Eds), Alzheimer disease (pp. 197-229). New York: Raven Press.
48. Hof, P. R. & Morrison, J. H. (1995). Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. Journal of Comparative Neurology, 352. 161-186.
49. Hyman, B. T., Van Hoesen, G. W., Kromer, L. J. & Damasio, A. R. (1986). Perforant pathway changes and the memory impairment of Alzheimer's disease. Annals of Neurology, 20, 472-481.
50. Jacquet, M. F., Boucquey, D., Theaux, R., Smidts, M., Callewaerts, A., Brucher, J. M. & Kevers, L. (1990). L'atrophie corticale postérieure: variante anatomo-clinique de la maladie d'Alzheimer. Acta Neurologica Belgica, 90, 265-273.
51. Jagust, W. J., Davies, P., Tiller-Borcich, J. K. & Reed, B. R. (1990). Focal Alzheimer's disease. Neurology, 40, 14-19.
52. Katz, B. & Rimmer, S. (1989). Ophthalmologic manifestations of Alzheimer's disease. Survey of Ophthalmology, 34, 31-34.
53. Kiyosawa, M., Bosley, T. M., Chawluk, J., Jamieson, D., Schatz, N. J., Savino, P. J., Sergott, R. C., Reivich, M. & Alavi, A. (1989). Alzheimer's disease with prominent visual symptoms. Ophthalmology, 96, 1077-1086.
54. Kowall, N. W. & Beal, M. F. (1988). Cortical somatostatin, neuropeptide Y, and NADPH diaphorase neurons: normal anatomy and alterations in Alzheimer's disease. Annals of Neurology, 23, 105-114.
55. Kuljis, R. O. (1994). Lesions in the pulvinar in patients with Alzheimer's disease. Journal of Neuropathology and Experimental Neurology, 53, 202-211.
56. Kuncl, R. W., Crawford, T. O., Rothstein, J. D. & Drachman, D. B. (1992). Motor neuron disease. In Asbury, A. K., McKhann, G. M. & McDonald, W. I. (Eds), Diseases of the nervous system, Clinical neurobiology, 2nd edition (pp. 1179-1208). Philadelphia: W.B. Saunders.
57. Kurylo, D. D., Corkin, S., Dolan, R. P., Rizzo III, J. F., Parker, S. W. & Growdon, J. H. (1994). Broad-band visual capacities are not selectively impaired in Alzheimer's disease. Neurobiology of Aging, 75, 305-311.
58. Kuskowski, M. A., Malone, S. M., Mortimer, J. A. & Dysken, M. W. (1989). Smooth pursuit eye movements in dementia of the Alzheimer type. Alzheimer Disease and Associated Disorders, 3, 157-171.
59. Leuba, G. & Saini, K. (1995). Pathology of subcortical visual centres in relation to cortical degeneration in Alzheimer's disease. Neuropathology and Applied Neurobiology, 21, 410-422.
60. Levine, D. N., Lee, J. M. & Fisher, C. M. (1993). The visual variant of Alzheimer's disease: a clinicopathologic case study. Neurology, 43, 305-313.
61. Levy, M. H., Hart, W. M.Jr, Sonstein, F. M. & Ballinger, W. E. Jr (1995). The incredible shrinking brain [Comments by Sadun, A]. Survey of Ophthalmology, 39, 315-322.
62. Lewis, D. A., Campbell, M. J., Terry, R. D. & Morrison, J. H. (1987). Laminar and regional distribution of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices. Journal of Neuroscience, 7,1799-1808.
63. Magnani, G., Bettoni, L. & Mazzuchi, A. (1982). Lesioni atrofiche bioccipitali di incerta natura all'origine di una agnosia visiva. Rivista di Neurologia, 52, 137-148.
64. McCarthy, G., Spicer, M., Adrignolo, A., Luby, M., Gore, J. & Allison, T. (1995). Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans. Human Brain Mapping, 2, 234-243.
65. Markesbery, W. (1992). Alzheimer's disease. In Asbury, A. K., McKhann, G. M. & McDonald, W. I. (Eds), Diseases of the nervous system, Clinical neurobiology, 2nd edition (pp. 795-803). Philadelphia: W.B. Saunders.
66. Mendez, M. F., Mendez, M. A., Martin, R., Smyth, K. A. & Whitehouse, P. J. (1990a) Complex visual disturbances in Alzheimer's disease. Neurology, 40, 439-443.
67. Mendez, M. F., Tomsak, R. L. & Render, B. (1990b) Disorders of the visual system in Alzheimer's disease. Journal of Clinical Neuro-ophthalmology, 10, 62-69.
68. Mendez, M. F., Turner, J., Gilmore, G. C., Remler, B. & Tomsak, R. L. (1990c) Bálint's syndrome in Alzheimer's disease: visuospatial functions. International Journal of Neuroscience, 54, 339-346.
69. Miklossy, J. (1993). The geniculocalcarine pathway in man, and some putative rostral visual areas involved in visuo-spatial attention. In Gulyas, B., Ottoson, D. & Roland, P. E. (Eds), Functional organisation of the human visual cortex (pp. 123-136). Oxford: Pergamon Press.
70. Minoshima, S., Foster, N. L. & Kuhl, D. E. (1994). Posterior cingulate cortex in Alzheimer's disease. The Lancet, 344, 895.
71. Mirra, S. S., Hart, M. N. & Terry, R. D. (1993). Making the diagnosis of Alzheimer's disease. A primer for practicing pathologists. Archives of Pathology and Laboratory Medicine, 117, 132-144.
72. Mishkin, M., Ungerleider, L. G. & Macko, K. A. (1983). Object vision and spatial vision: two cortical pathways. Trends in Neurosciences, 6, 414-417.
73. Morel, F. (1945). Les aires striée, parastriée et péristriée dans les troubles de la fonction visuelle au cours de la maladie d'Alzheimer. Confinia Neurologica, 6, 238-242.
74. Moss, M. B. & Albert, M. S. (1988). Alzheimer's disease and other dementing disorders. In Albert, M. S. & Moss, M. B. (Eds), Geriatric neuropsychology (pp. 145-178). New York: The Guilford Press.
75. Murray, E. A., Davidson, M., Gaffan, D., Olton, D S. & Suomi, S. (1989). Effects of fornix transection and cingulate cortical ablation on spatial memory in rhesus monkeys. Experimental Brain Research, 74, 173-186.
76. Nakamura, H., Gattass, R., Desimone, R. & Ungerleider, L. G. (1993). The modular organization of projections from areas VI and V2 to areas V4 and TEO in macaques. Journal of Neuroscience, 13, 3681-3691.
77. Nissen, M. J., Corkin, S., Buonanno, F. S., Growdon, J. H., Wray, S. H. & Bauer, J. (1985). Spatial vision in Alzheimer's disease - general findings and a case report. Archives of Neurology, 42, 667-671.
78. Olson, C. R. & Musil, S. Y. (1992a) Posterior cingulate cortex: sensory and oculomotor properties of single neurons in behaving cat. Cerebral Cortex, 2, 485-502.
79. Olson, C. R. & Musil, S. Y. (1992b) Topographic organization of cortical and subcortical projections to posterior cingulate cortex in the cat: evidence for somatic, ocular and complex subrogions. Journal of Comparative Neurology, 323, 1-24.
80. Olson, C. R., Musil, S. Y. & Goldberg, M. E. (1993). Neurophysiology of posterior cingulate cortex in the behaving monkey. In Vogt, B. A. & Gabriel, M. (Eds), The neurobiology of cingulate cortex and limbic thalamus (pp. 366-380). Boston: Birkhäuser.
81. Orban, G. A., Dupont, P., De Bruyn, B., Vogels, R., Vandenberghe, R. & Mortelmans, L. (1995). A motion area in human visual cortex. Proceedings of the National Academy of Sciences USA, 92, 993-997.
82. Pearson, R. C. A., Esiri, M. M., Hiorns, R. W., Wilcock, G. K. & Powell, T. P. S. (1985). Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. Proceedings of the National Academy of Sciences USA, 82, 4531-4534.
83. Permanne, B., Buée, L., David, J. P., Fallet-Bianco, C., Di Menza, C. & Delacourte, A. (1995). Quantitation of Alzheimer's amyloid peptide and identification of related amyloid proteins by dot-blot immunoassay. Brain Research, 685, 154-162.
84. Reiman, E. M., Caselli, R. J., Yun, L. S., Chen, K., Bandy, D., Minoshima, S., Thibodeau, S. N. & Osborne, D. (1996). Preclinical evidence of Alzheimer's disease in persons homozygous for the ε4 allele for apolipoprotein E. New England Journal of Medicine, 334, 752-758.
85. Rockland, K. S. & Pandya, D. N. (1979). Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Research, 179, 3-20.
86. Rogers, J. & Morrison, J. H. (1985). Quantitative morphology and regional and laminar distributions of senile plaques in Alzheimer's disease. Journal of Neuroscience, 5, 2801-2808.
87. Sereno, M. I., Dale, A. M., Reppas, J. B., Kwong, K. K., Belliveau, J. W., Brady, T. J., Rosen, B. R. & Tootell, R. B. H. (1995). Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science, 268, 889-893.
88. Sikes, R. W., Vogt, B. A. & Swadlow, H. A. (1988). Neuronal responses in rabbit cingulate cortex linked to quick-phase eye movements during nystagmus. Journal of Neurophysiology, 59, 922-936.
89. Silverman, S. E., Tran, D. B., Zimmermann, K. M. & Feidon, S. E. (1994). Dissociation between the detection and perception of motion in Alzheimer's disease. Neurology, 44, 1814-1818.
90. Terry, R. D., Peck, A., DeTeresa, R., Schlechter, R. & Horoupian, D. S. (1981). Some morphometric aspects of the brain in senile dementia of the Alzheimer type. Annals of Neurology, 10, 184-192.
91. Tootell, R. B. H., Reppas, J. B., Kwong, K. K., Malach, R., Born, R. T., Brady, T. J., Rosen, B. R. & Belliveau, J. W. (1995). Functional analysis of human area MT and related visual cortical areas using magnetic resonance imaging. Journal of Neuroscience, 15, 3215-3230.
92. Tootell, R. B. H. & Taylor, J. B. (1995). Anatomical evidence for MT and additional cortical visual areas in humans. Cerebral Cortex, 5, 39-55.
93. Vallet, P. G., Guntern, R., Hof, P. R., Golaz, J., Delacourte, A., Robakis, N. K. & Bouras, C. (1992). A comparative study of histological and immunohistochemical methods for neurofibrillary tangles and senile plaques in Alzheimer's disease. Acta Neuropathologica, 83, 170-178.
94. Vickers, J. C., Chin, D., Edwards, A. M., Sampson, V., Harper, C. & Morrison, J. H. (1996). Dystrophie neunte formation associated with age-related amyloid deposition in the neocortex: clues to the genesis of neurofibrillary pathology. Experimental Neurology, 141, 1-11.
95. Victoroff, J., ROSS, W., Benson, D. F., Verity, M. A. & Vinters, H. V. (1994). Posterior cortical atrophy - neuropathologic correlations. Archives of Neurology, 51, 269-274.
96. Vogt, B. A., Crino, P. B. & Vogt, L. J. (1992). Reorganization of cingulate cortex in Alzheimer's disease: neuron loss, neuritic plaques, and muscarinic receptor binding. Cerebral Cortex, 2, 526-535.
97. Vogt, B. A. & Miller, M. W. (1983). Cortical connections between rat cingulate cortex and visual, motor and postsubicular cortices. Journal of Comparative Neurology, 216, 192-210.
98. Vogt, B. A. & Pandya, D. N. (1987). Cingulate cortex of rhesus monkey: II. Cortical afferents. Journal of Comparative Neurology, 262, 271-289.
99. Vogt, B. A., Rosene, D. L. & Pandya, D. N. (1979). Thalamic and cortical afferents differentiate anterior from posterior cingulate cortex in the monkey. Science, 204, 205-207.
100. Vogt, B. A., Sikes, R. W., Swadlow, H. A. & Weyand, T. G. (1986). Rabbit cingulate cortex: cytoarchitecture, physiological border with visual cortex, and afferent cortical connections of visual, motor, postsubicular and intracingulate origin. Journal of Comparative Neurology, 248, 74-94.
101. Vogt, B. A., Van Hoesen, G. W. & Vogt, L. J. (1990). Laminar distribution of neuron degeneration in posterior cingulate cortex in Alzheimer's disease. Acta Neuropathologica, 80, 581-589.
102. Watson, J. D. G., Myers, R., Frackowiak, R. S. J., Hajnal, J. V., Woods, R. P., Mazziotta, J. C., Shipp, S. & Zeki, S. (1993). Area V5 of the human brain: evidence from a combined study using positron emmision tomography and magnetic resonance imaging. Cerebral Cortex, 3, 79-94.
103. Wilson, F. A. W., ÓScalaidhe, S. P. & Goldman-Rakic, P. S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science, 260, 1955-1958.
104. Young, W. G., Nimchinsky, E. A., Hof, P. R., Bloom, F. E. & Morrison, J. H. (1995). NeuroZoom: computer software for quantitative neuroanatomic mapping and stereology. Society for Neuroscience Abstracts, 21, 1078.
105. Zeki, S. M. & Shipp, S. (1988). The functional logic of cortical connections. Nature, 335, 311-317.