Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices

The number of Thioflavine S-positive neurofibrillary tangles (NFT) and neuritic plaques (NP) was determined in visual and auditory cortical regions of 8 patients with Alzheimer's disease. On both a regional and laminar basis, NFT exhibited very distinctive and consistent distribution patterns. The mean (+/- SEM) number of NFT in a 250-micron- wide cortical traverse was very low in area 17, primary visual cortex (0.9 +/- 1.0), increased 20-fold in the immediately adjacent visual association cortex of area 18 (19.7 +/- 3.6), and showed a further doubling in area 20, the higher-order visual association cortex of the inferior temporal gyrus (35.5 +/- 8.8). Similar differences in NFT number were present between primary auditory (1.6 +/- 0.5) and auditory association (18.9 +/- 5.4) regions. On a laminar basis, NFT were predominantly present in layers III and V, although there were striking regional differences in the proportion of NFT in these 2 layers. Layer III contained 79% of the NFT in layers III and V in area 18, 41% in area 20, and only 27% in area 22. In contrast, NP showed different, and less specific, regional and laminar distribution patterns. Total NP number was similar in the 3 visual areas, although there were marked regional differences in the type of NP present. Nearly 80% of the NP in area 17 was of the NPc type (i.e., contained a dense, brightly fluorescent core), whereas over 70% of the NP in both areas 18 and 21 was of the NPnc type (i.e., lacked a dense, brightly fluorescent core). NP were present in every cortical layer but were most numerous in layers III and IV. The distinctive distribution patterns of NFT are very similar to the regional and laminar locations of long corticocortical projection neurons in homologous regions of monkey neocortex. This association suggests that NFT reside in the cell bodies of a subpopulation of pyramidal neurons, namely, those that furnish long corticocortical projections. In contrast, the distribution patterns of NP suggest that multiple neuronal systems contribute to their formation.

[1]  R. Terry,et al.  Somatostatin-like immunoreactivity within neuritic plaques , 1985, Brain Research.

[2]  B. Seltzer,et al.  A comparison of clinical features in early- and late-onset primary degenerative dementia. One entity or two? , 1983, Archives of neurology.

[3]  I. Ferrier,et al.  Elevation of neuropeptide Y (NPY) in substantia innominata in Alzheimer's type dementia , 1984, Journal of the Neurological Sciences.

[4]  S. Zeki Representation of central visual fields in prestriate cortex of monkey. , 1969, Brain research.

[5]  R. Perry Recent advances in neuropathology. , 1986, British medical bulletin.

[6]  B. Cragg The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. , 1969, Vision research.

[7]  R. Katzman.,et al.  Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa , 1980, Nature.

[8]  V. Chan‐Palay,et al.  II. Cortical neurons immunoreactive with antisera against neuropeptide Y are altered in Alzheimer's‐type dementia , 1985, The Journal of comparative neurology.

[9]  P. Emson,et al.  Morphology, distribution, and synaptic relations of somatostatin- and neuropeptide Y-immunoreactive neurons in rat and monkey neocortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  G K Wilcock,et al.  Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[11]  P. Somogyi,et al.  Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin- immunoreactive material , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  G. V. Van Hoesen,et al.  Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. , 1984, Science.

[13]  T. Powell,et al.  The cortex of the primary auditory area in Alzheimer's disease , 1986, Brain Research.

[14]  J. Penney,et al.  Alterations in L-glutamate binding in Alzheimer's and Huntington's diseases. , 1985, Science.

[15]  A. Nappi,et al.  Alzheimer ' s Disease : Cell-Specific Pathology Isolates the Hippocampal Formation , 2022 .

[16]  C D Gilbert,et al.  Aspartate and glutamate as possible neurotransmitters in the visual cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  E. Perry,et al.  Intralaminar Neurochemical Distributions in Human Midtemporal Cortex: Comparison Between Alzheimer's Disease and the Normal , 1984, Journal of neurochemistry.

[18]  J. Tigges,et al.  Areal and laminar distribution of neurons interconnecting the central visual cortical areas 17, 18, 19, and MT in squirrel monkey (Saimiri) , 1981, The Journal of comparative neurology.

[19]  H. Barbas Pattern in the laminar origin of corticocortical connections , 1986, The Journal of comparative neurology.

[20]  M. Beal,et al.  Reduced numbers of somatostatin receptors in the cerebral cortex in Alzheimer's disease. , 1985, Science.

[21]  M Hallett,et al.  Intra- and interhemispheric connections of the neocortical auditory system in the rhesus monkey. , 1969, Brain research.

[22]  R. Benoit,et al.  Regional heterogeneity in the distribution of somatostatin-28- and somatostatin-28(1-12)-immunoreactive profiles in monkey neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  A. Procter,et al.  Excitatory amino acid-releasing and cholinergic neurones in Alzheimer's disease , 1986, Neuroscience Letters.

[24]  S. Vincent,et al.  Somatostatin- and Neuropeptide Y-immunoreactive neurons in the neocortex in senile dementia of alzheimer's type , 1986, Brain Research.

[25]  H. Swadlow Efferent systems of primary visual cortex: A review of structure and function , 1983, Brain Research Reviews.

[26]  D. Price,et al.  Catecholaminergic neurites in senile plaques in prefrontal cortex of aged nonhuman primates , 1985, Neuroscience.

[27]  M J Campbell,et al.  An immunohistochemical characterization of somatostatin‐28 and somatostatin‐281–12 in monkey prefrontal cortex , 1986, The Journal of comparative neurology.

[28]  H. Barbas,et al.  Organization of afferent input to subdivisions of area 8 in the rhesus monkey , 1981, The Journal of comparative neurology.

[29]  R. DeTeresa,et al.  Some morphometric aspects of the brain in senile dementia of the alzheimer type , 1981, Annals of neurology.

[30]  D. Dawbarn,et al.  Neuropeptide Y-like immunoreactivity in neuritic plaques of Alzheimer's disease. , 1985, Biochemical and biophysical research communications.

[31]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[32]  L. Hersh,et al.  Choline acetyltransferase immunoreactivity in neuritic plaques of Alzheimer brain , 1986, Neuroscience Letters.

[33]  R. Desimone,et al.  Prestriate afferents to inferior temporal cortex: an HRP study , 1980, Brain Research.

[34]  John H. R. Maunsell,et al.  Hierarchical organization and functional streams in the visual cortex , 1983, Trends in Neurosciences.

[35]  P. Emson,et al.  Decreased somatostatin immunoreactivity but not neuropeptide Y immunoreactivity in cerebral cortex in senile dementia of Alzheimer type , 1986, Neuroscience Letters.

[36]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[37]  P. Schwartz Amyloid degeneration and tuberculosis in the aged. , 1972, Gerontologia.

[38]  D. Price,et al.  Evidence for cholinergic neurites in senile plaques. , 1984, Science.

[39]  D. Kleinbaum,et al.  Applied Regression Analysis and Other Multivariate Methods , 1978 .

[40]  M. Roth,et al.  Cortical neuronal counts in normal elderly controls and demented patients , 1983, Neurobiology of Aging.

[41]  D. Neary,et al.  Amino acid release from biopsy samples of temporal neocortex from patients with Alzheimer's disease , 1983, Brain Research.

[42]  E. Perentes [Senile dementia of the Alzheimer type]. , 1981, Revue medicale de la Suisse romande.

[43]  E G Jones,et al.  Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[44]  T. Hicks,et al.  Synaptic transmission in suprasylvian visual cortex is reduced by excitatory amino acid antagonists. , 1981, Canadian journal of physiology and pharmacology.

[45]  G. K. Wilcock,et al.  Plaques, tangles and dementia A quantitative study , 1982, Journal of the Neurological Sciences.

[46]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[47]  R. Terry,et al.  Substance P immunoreactivity within neuritic plaques , 1985, Neuroscience Letters.

[48]  D. Mann,et al.  Correlation between senile plaque and neurofibrillary tangle counts in cerebral cortex and neuronal counts in cortex and subcortical structures in Alzheimer's disease , 1985, Neuroscience Letters.

[49]  T. Crow,et al.  Location of neuronal tangles in somatostatin neurones in Alzheimer's disease , 1985, Nature.

[50]  F. Fonnum,et al.  Glutamate in cortical fibers. , 1981, Advances in biochemical psychopharmacology.

[51]  J. Morrison,et al.  Quantitative morphology and regional and laminar distributions of senile plaques in Alzheimer's disease , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  L. Iversen,et al.  Reduced amounts of immunoreactive somatostatin in the temporal cortex in senile dementia of Alzheimer type , 1980, Neuroscience Letters.

[53]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[54]  A M Galaburda,et al.  The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey , 1983, The Journal of comparative neurology.

[55]  F. Bloom,et al.  Somatostatin immunoreactivity in neuritic plaques of Alzheimer's patients , 1985, Nature.