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Senile plaques, amyloid β-protein, and acetylcholinesterase fibres: laminar distributions in Alzheimer's disease striate cortex

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Summary

The laminar distributions of senile plaques and amyloid β-protein (AβP) within the striate cortex of patients with Alzheimer's disease (AD) were studied with enhanced Bielschowsky (roughly equivalent to the Campbell technique) and immunohistochemical methods. The laminar distribution of acetylcholinesterase (AChE) fibres within the striate cortex of both AD patients and control patients was studied with an enzyme histochemical method. Quantification of Bielschowsky-stained plaque numbers along intersect lines drawn parallel to laminar boundaries revealed a significant aggregation of plaques at the interface of layers IVc and V. Lines drawn through layer VI intersected significantly fewer plaques than lines through other laminae. Immunoperoxidase staining for AβP revealed a similar distribution fo senile plaques, and additional, prominent, diffuse deposits of AβP within layers I and IVc. AChE fibres were markedly depleted in the striate cortex of AD cases. In control cases, AChE fibres were, like AβP immunoreactivity, concentrated within layers I and IVc. The results indicate that enhanced silver methods may not reveal the complete distribution of AβP. The codistribution of AβP-immunoreactive diffuse amyloid deposits and AChE fibres to the same cortical laminae is consistent with the possibility that these deposits may be formed from degenerating cholinergic elements. The formation of a line of senile plaques at the interface of two cortical laminae within the striate cortex, in an anatomically analogous situation to a similar line of plaques within the dentate gyrus, suggests that formation of well-defined plaques may be accelerated by the interaction of specific neuronal systems.

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References

  1. Agid Y, Ransmayr G, Cervera P, Hirsch EC, Hersh LB, Duyckaerts C, Hauw JJ (1989) Choline acetyltransferase immunoreactivity in the hippocampal formation of control subjects and in patients with Alzheimer's disease. Neurology 39 [Suppl 1]:193

    Google Scholar 

  2. Akiyama H, Tago H, Itagaki S, McGeer PL (1990) Occurrence of diffuse amyloid deposits in the presubicular parvopyramidal layer in Alzheimer's disease. Acta Neuropathol 79:537–544

    Google Scholar 

  3. Amaral DG, Campbell MJ (1986) Transmitter systems in the primate dentate gyrus. Hum Neurobiol 5:169–180

    Google Scholar 

  4. Beach TG, McGeer EG (1988) Lamina-specific arrangement of astrocytic gliosis and senile plaques in Alzheimer's disease visual cortex. Brain Res 463:357–361

    Google Scholar 

  5. Beach TG, Tago H, Nagai T, Kimura H, McGeer PL, McGeer EG (1987) Perfusion-fixation of the human brain for immunohistochemistry: comparison with immersion-fixation. J Neurosci Methods 19:183–192

    Google Scholar 

  6. Beach TG, Walker R, McGeer EG (1989) Lamina-selective A68 immunoreactivity in primary visual cortex of Alzheimer's disease patients. Brain Res 501:171–174

    Google Scholar 

  7. Beach TG, Walker R, McGeer EG (1989) Patterns of gliosis in Alzheimer's disease and aging cerebrum. Glia 2:420–436

    Google Scholar 

  8. Bear MF, Carnes KM, Ebner FF (1985) An investigation of cholinergic circuitry in cat striate cortex using acetylcholinesterase histochemistry. J Comp Neurol 234:411–430

    Google Scholar 

  9. Bell MA, Ball MJ (1985) Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 335:139–143

    Google Scholar 

  10. Bell MA, Ball MJ (1990) Neuritic plaques and vessels of visual cortex in aging and Alzheimer's dementia. Neurobiol Aging 11:359–370

    Google Scholar 

  11. Berger B, Trottier S, Verney C, Gaspar P, Alvarez C (1988) Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: a radioautographic study. J Comp Neurol 273:99–112

    Google Scholar 

  12. Braak H, Braak E, Ohm T, Bohl J (1986) Occurrence of neuropil threads in the senile human brain and in Alzheimer's disease: a third location of paired helical filaments outside of neurofibrillary tangles and senile plaques. Neurosci Lett 65:351–355

    Google Scholar 

  13. Braak H, Braak E, Kalus P (1989) Alzheimer's disease: areal and laminar pathology in the occipital isocortex. Acta Neuropathol 77:494–506

    Google Scholar 

  14. Braak H, Braak E, Bohl J, Lang W (1989) Alzheimer's disease: amyloid plaques in the cerebellum. J Neurol Sci 93:277–287

    Google Scholar 

  15. Brady DR, Mufson EJ (1990) Amygdaloid pathology in Alzheimer's disease. Dementia 1:5–17

    Google Scholar 

  16. Brashear HR, Codec MS, Carlsen J (1988) The distribution of neuritic plaques and acetylcholinesterase staining in the amygdala in Alzheimer's disease. Neurology 38:1694–1699

    Google Scholar 

  17. Campbell SK, Switzer RC, Martin TL (1987) Alzheimer's plaques and tangles: a controlled and enhanced silver-staining method. Soc Neurosci Abstr 13:678

    Google Scholar 

  18. Crain BJ, Burger PC (1988) The laminar distribution of neuritic plaques in the fascia dentata of patients with Alzheimer's disease. Acta Neuropathol 76:87–93

    Google Scholar 

  19. Duyckaerts C, Hauw J-J, Bastenaire F, Piette F, Poulain C, Rainsard V, Javoy-Agid F, Berthaux P (1986) Laminar distribution of neocortical senile plaques in senile dementia of the Alzheimer type. Acta Neuropathol (Berl) 70:249–256

    Google Scholar 

  20. Emson PC, Lindvall O (1986) Neuroanatomical aspects of neurotransmitters affected in Alzheimer's disease. Br Med Bull 42:57–62

    Google Scholar 

  21. Geddes JW, Anderson KJ, Cotman CW (1986) Senile plaques as aberrant sprout-stimulating structures. Exp Neurol 94:767–776

    Google Scholar 

  22. Geula C, Mesulam M-M (1989) Cortical cholinergic fibers in aging and Alzheimer's disease: a morphometric study. Neuroscience 33:469–481

    Google Scholar 

  23. Green RC, Mesulam M-M (1988) Acetylcholinesterase fiber staining in the human hippocampus and parahippocampal gyrus. J Comp Neurol 273:488–499

    Google Scholar 

  24. Hedreen JC, Uhl GR, Bacon SJ, Fambrough DM, Price DL (1984) Acetylcholinesterase-immunoreactive axonal network in monkey visual cortex. J Comp Neurol 226:246–254

    Google Scholar 

  25. Hedreen JC, Raskin LS, Struble RG, Price DL (1988) Selective silver impregnation of senile plaques: a method useful for computer imaging. J Neurosci Methods 25:151–158

    Google Scholar 

  26. Hendrickson AE, Hunt SP, Wu J-Y (1981) Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292:605–607

    Google Scholar 

  27. Hyman BT, Van Hoesen GW, Kromer LJ, Damasio AR (1986) Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann Neurol 20:472–481

    Google Scholar 

  28. Hyman BT, Kromer LJ, Van Hoesen GW (1988) A direct demonstration of the perforant pathway terminal zone in Alzheimer's disease using the monoclonal antibody Alz-50. Brain Res 450:392–397

    Google Scholar 

  29. Ishii T, Kametani F, Haga S, Sato M (1989) The immunohistochemical demonstration of subsequences of the precursor of the amyloid A4 protein in senile plaques in Alzheimer's disease. Neuropathol Appl Neurobiol 15:135–147

    Google Scholar 

  30. Joachim CL, Morris JH, Selkoe DJ (1989) Diffuse senile plaques occur commonly in the cerebellum in Alzheimer's disease. Am J Pathol 135:309–319

    Google Scholar 

  31. Kalus P, Braak H, Braak E, Bohl J (1989) The presubicular region in Alzheimer's disease: topography of amyloid deposits and neurofibrillary changes. Brain Res 494:198–203

    Google Scholar 

  32. Karnovsky MJ, Roots L (1964) A “direct-coloring” thiocholine method for cholinesterases. J Histochem Cytochem 12:219–221

    Google Scholar 

  33. Kosofsky BE, Molliver E, Morrison JH, Foote SL (1984) The serotonin and norepinephrine innervation of primary visual cortex in the cynomolgus monkey. J Comp Neurol 230:168–178

    Google Scholar 

  34. Lewis DA, Campbell MJ, Foote SL, Morrison JH (1986) The monoaminergic innervation of primate neocortex. Hum Neurobiol 5:181–188

    Google Scholar 

  35. Lewis DA, Campbell MJ, Terry RD, Morrison JH (1987) Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices. J Neurosci 7:1799–1808

    Google Scholar 

  36. Love S, Burrola P, Terry RD, Wiley CA (1989) Immunoelectron microscopy of Alzheimer and Pick brain tissue labelled with the monoclonal antibody Alz-50. Neuropathol Appl Neurobiol 15:223–231

    Google Scholar 

  37. McGeer EG (1989) Neurotransmitters. Curr Opin Neurol Neurosurg 2:520–531

    Google Scholar 

  38. Masliah E, Terry R, Buzsaki G (1989) Thalamic nuclei in Alzheimer disease: evidence against the cholinergic hypothesis of plaque formation. Brain Res 493:240–246

    Google Scholar 

  39. Mesulam M-M, Rosen AD, Mufson EJ (1984) Reginal variations in cortical cholinergic innervation: chemoarchitectonics of acetylcholinesterase-containing fibers in the macaque brain. Brain Res 311:245–258

    Google Scholar 

  40. Ogomori K, Kitamoto T, Tateishi J, Sato Y, Suetsugu M, Abe M (1989) Beta-protein amyloid is widely distributed in the central nervous system of patients with Alzheimer's disease. Am J Pathol 134:243–251

    Google Scholar 

  41. Ojima H, Kawajiri S-I, Yamasaki T (1989) Cholinergic innervation of the rat cerebellum: qualitative and quantitative analyses of elements immunoreactive to a monoclonal antibody against choline acetyltransferase. J Comp Neurol 290:41–52

    Google Scholar 

  42. Pearson RCA, Esiri MM, Hiorns RW, Wilcock GK, Powell TPS (1985) Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer's disease. Proc Natl Acad Sci USA 82:4531–4534

    Google Scholar 

  43. Rafalowska J, Barcikowska M, Wen GY, Wisniewski HM (1988) Laminar distribution of neuritic plaques in normal aging. Alzheimer's disease and Down's syndrome. Acta Neuropathol 77:21–25

    Google Scholar 

  44. Rakie P, Goldman-Rakic PS, Gallagher D (1988) Quantitative autoradiography of major neurotransmitter receptors in the monkey striate and extrastriate cortex. J Neurosci 8:3670–3690

    Google Scholar 

  45. Rozemuller JM, Eikelenboom P, Stam FC, Beyreuther K, Masters CL (1989) A4 protein in Alzheimer's disease: primary and secondary cellular events in extracellular amyloid deposition. J Neuropathol Exp Neurol 48:674–691

    Google Scholar 

  46. Rogers J, Morrison JH (1985) Quantitative morphology and regional and laminar distribution of senile plaques in Alzheimer's disease. J Neurosci 5:2801–2808

    Google Scholar 

  47. Rudelli RD, Ambler MW, Wisniewski HM (1984) Morphology and distribution of Alzheimer neuritic (senile) and amyloid plaques in striatum and diencephalon. Acta Neuropathol 64:273–281

    Google Scholar 

  48. Shaw C, Cynader M (1986) Laminar distribution of receptors in monkey (Macaca fascicularis) geniculostriate system. J Comp Neurol 248:310–312

    Google Scholar 

  49. Steward O (1976) Togographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167:285–314

    Google Scholar 

  50. Tago H, McGeer PL, McGeer EG (1987) Acetylcholinesterase fibers and the development of senile plaques. Brain Res 406:363–369

    Google Scholar 

  51. Takahashi H, Kurashima C, Utsuyama M, Hirokawa K (1990) Immunohistological study of senile brains using a monoclonal antibody recognizing β-amyloid precursor protein: significance of granular deposits in relation with senile plaques. Acta Neuropathol 80:260–265

    Google Scholar 

  52. Tigges J, Tigges M, Perachio AA (1977) Complementary laminar termination of afferents to area 17 originating in area 18 and in the lateral geniculate nucleus in squirrel monkey. J Comp Neurol 176:87–100

    Google Scholar 

  53. Van Hoesen GW (1982) The parahippocampal gyrus. New observations regarding its cortical connections in the monkey. Trends Neurosci 5:345–350

    Google Scholar 

  54. Van Hoesen GW, Pandya DN (1975) Some connections of the entorhinal area (area 28) and perirhinal area (area 35) cortices in the rhesus monkey. II. Entorhinal cortex efferents. Brain Res 95:39–59

    Google Scholar 

  55. von Braunmuhl A (1957) Alterserkrankungen des Zentralnervensystems. Senile Involution. Senile Demenz. Alzheimersche Krankheit. In: Scholz W (ed) Handbuch der Speziellen Pathologischen Anatomie und Histologie, vol XIII/1A. Springer, Berlin, pp 337–539

    Google Scholar 

  56. Wisniewski HM, Bancher C, Barcikowska M, Wen GY, Currie J (1989) Spectrum of morphological appearance of amyloid deposits in Alzheimer's disease. Acta Neuropathol 78:337–347

    Google Scholar 

  57. Wolozin B, Davies P (1987) Alzheimer-related neuronal protein A68: specificity and distribution. Ann Neurol 22:521–526

    Google Scholar 

  58. Wolozin BL, Pruchnicki A, Dickson DW, Davies P (1986) A neuronal antigen in the brains of Alzheimer patients. Science 232:648–650

    Google Scholar 

  59. Yamaguchi H, Hirai S, Morimatsu M, Shoji M, Ihara Y (1988) A variety of cerebral amyloid deposits in the brains of the Alzheimer-type dementia demonstrated by β protein immunostaining. Acta Neuropathol 76:541–549

    Google Scholar 

  60. Yamaguchi H, Hirai S, Morimatsu M, Shoji M, Harigaya Y (1988) Diffuse type of senile plaques in the brains of Alzheimer-type dementia. Acta Neuropathol 77:113–119

    Google Scholar 

  61. Yamaguchi H, Hirai S, Morimatsu M, Shoji M, Nakazato Y (1989) Diffuse type of senile plaques in the cerebellum of Alzheimer-type dementia demonstrated by β-protein immunostain. Acta Neuropathol 77:314–319

    Google Scholar 

  62. Yamaguchi H, Haga C, Hirai S, Nakazato Y, Kosaka K (1990) Distinctive, rapid, and easy labeling of diffuse plaques in the Alzheimer brains by a new methenamine silver stain. Acta Neuropathol 79:569–572

    Google Scholar 

  63. Yamaguchi H, Nakazato Y, Shoji M, IIhara V, Hirai S (1990) Ultrastructure of the neuropil threads in the Alzheimer brain: their dendritic origin and accumulation in the senile plaques. Acta Neuropathol 80:368–374

    Google Scholar 

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Authors and Affiliations

  1. Division of Neuropathology, University of British Columbia, Vancouver General Hospital, 855 West 12th Avenue, V5Z 1W5, Vancouver, B.C., Canada

    T. G. Beach

  2. Kinsmen Laboratory of Neurological Research, University of British Columbia, 2255 Wesbrook Mall, V6T 1W5, Vancouver, B.C., Canada

    E. G. McGeer

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Supported by a Fellowship from the British Columbia Health Care Research Foundation to TGB. This work is part of the PhD. dissertation of Dr. Beach (University of British Columbia, 1991)

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Beach, T.G., McGeer, E.G. Senile plaques, amyloid β-protein, and acetylcholinesterase fibres: laminar distributions in Alzheimer's disease striate cortex. Acta Neuropathol 83, 292–299 (1992). https://doi.org/10.1007/BF00296792

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  • DOI: https://doi.org/10.1007/BF00296792

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