Cited by 102Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Basal forebrain cholinergic system in the dementias: Vulnerability, resilience, and resistance

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Geula, Changiz, Dunlop, Sara R., Ayala, Ivan, Kawles, Allegra S., Flanagan, Margaret E., Gefen, Tamar, Mesulam, Marek‐Marsel·2021·Journal of Neurochemistry

Abstract

The basal forebrain cholinergic neurons (BFCN) provide the primary source of cholinergic innervation of the human cerebral cortex. They are involved in the cognitive processes of learning, memory, and attention. These neurons are differentially vulnerable in various neuropathologic entities that cause dementia. This review summarizes the relevance to BFCN of neuropathologic markers associated with dementias, including the plaques and tangles of Alzheimer's disease (AD), the Lewy bodies of diffuse Lewy body disease, the tauopathy of frontotemporal lobar degeneration (FTLD‐TAU) and the TDP‐43 proteinopathy of FTLD‐TDP. Each of these proteinopathies has a different relationship to BFCN and their corticofugal axons. Available evidence points to early and substantial degeneration of the BFCN in AD and diffuse Lewy body disease. In AD, the major neurodegenerative correlate is accumulation of phosphotau in neurofibrillary tangles. However, these neurons are less vulnerable to the tauopathy of FTLD. An intriguing finding is that the intracellular tau of AD causes destruction of the BFCN, whereas that of FTLD does not. This observation has profound implications for exploring the impact of different species of tauopathy on neuronal survival. The proteinopathy of FTLD‐TDP shows virtually no abnormal inclusions within the BFCN. Thus, the BFCN are highly vulnerable to the neurodegenerative effects of tauopathy in AD, resilient to the neurodegenerative effect of tauopathy in FTLD and apparently resistant to the emergence of proteinopathy in FTLD‐TDP and perhaps also in Pick's disease. Investigations are beginning to shed light on the potential mechanisms of this differential vulnerability and their implications for therapeutic intervention. image

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  • Selective vulnerability of basal forebrain cholinergic neurons is often attributed to deficiency of NGF, which normally sustains them.

    “This selective vulnerability is often attributed to a deficiency of nerve growth factor (NGF), which normally sustains basal forebrain cholinergic neurons.”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [97]

    Section 5 says Ch1–Ch4 neurons depend on NGF for survival and considers NGF deficiency a conceivable cause of selective vulnerability. It does not say this explanation is often invoked; it also reports no loss or an increase in cortical and hippocampal NGF in AD, consistent with defective transport instead. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Loss of trophic support combined with metabolic and proteostatic stressors renders basal forebrain cholinergic neurons especially susceptible to degeneration in AD.

    “Loss of trophic support, combined with metabolic and proteostatic stressors, renders these neurons especially susceptible to degeneration in AD [97].”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [97]

    Section 5, “Selective Vulnerability of Basal Forebrain Cholinergic System” (page unavailable), says disrupted retrograde NGF transport is likely to contribute to cholinergic neuron loss in AD. It also links neurofibrillary tangles to degeneration, but the cited passages do not establish metabolic stress or characterize the pathology as proteostatic stress acting in combination with lost trophic support. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • In AD, the cholinergic system is disrupted at multiple levels: ChAT activity is markedly reduced impairing ACh synthesis; Aβ toxicity disrupts nutrient balance and vesicular storage/release; and alterations in receptor signaling compromise cholinergic neurotransmission.

    “In AD, this finely tuned system is disrupted at multiple levels, such as (i) ChAT activity is markedly reduced, impairing ACh synthesis; (ii) Aβ toxicity disrupts nutrient balance and interferes with vesicular storage and release; and (iii) alterations in receptor signaling further compromise cholinergic neurotransmission [97].”

    From Toward a Unified Framework in Molecular Neurobiology of Alzheimer’s Disease: Revisiting the Pathophysiological Hypotheses (2026) · cites this paper as [97]

    Split into 3 atoms — 1 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

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Cites

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Research works printed but not linked: 146

  1. Allen, S. J., MacGowan, S. H., Treanor, J. J., Feeney, R., Wilcock, G. K., & Dawbarn, D. (1991). Normal beta-NGF content in Alzheimer's dis- ease cerebral cortex and hippocampus. Neuroscience Letters, 131, 135-139.
  2. Alzheimer, A. (1977). A unique illness involving the cerebral cortex. In D. A. Rothenberg & F. H. Hochberg (Eds.), Neurological classics in modern translation (pp. 41-43). Hafner Press.
  3. Araujo, D. M., Lapchak, P. A., Robitaille, Y., Gauthier, S., & Quirion, R. (1988). Differential alteration of various cholinergic markers in cor- tical and subcortical regions of human brain in Alzheimer's disease. Journal of Neurochemistry, 50, 1914-1923. https://doi.org/10.1111/ j.1471-4159.1988.tb024 · DOI
  4. x Arendt, T., Bigl, V., Tennstedt, A., & Arndt, A. (1985). Neuronal loss in dif- ferent parts of the nucleus basalis is related to neuritic plaque for- mation in cortical target areas in Alzheimer's disease. Neuroscience, 14, 1-14. https://doi.org/10.1016/0306-4522(85)90160 -5 · DOI
  5. Arikuni, T., & Kubota, K. (1984). Substantia innominata projection to cau- date nucleus in macaque monkeys. Brain Research, 302, 184-189. https://doi.org/10.1016/0006-8993(84)91299 -X · DOI
  6. Arriagada, P. V., Marzloff, K., & Hyman, B. T. (1992). Distribution of Alzheimer-type pathologic changes in nondemented elderly indi- viduals matches the pattern in Alzheimer's disease. Neurology, 42, 1681-1688. https://doi.org/10.1212/WNL.42.9.1681 · DOI · Paper page
  7. Asahina, M., Suhara, T., Shinotoh, H., Inoue, O., Suzuki, K., & Hattori, T. (1998). Brain muscarinic receptors in progressive supranuclear 14714159, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jnc.15471, Wiley Online Library on [30/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License palsy and Parkinson's disease: A positron emission tomographic study. Journal of Neurology, Neurosurgery, and Psychiatry, 65, 155- 163. https://doi.org/10.1136/jnnp.65.2.155 · DOI
  8. Attems, J., Toledo, J. B., Walker, L., Gelpi, E., Gentleman, S., Halliday, G., Hortobagyi, T., Jellinger, K., Kovacs, G. G., Lee, E. B., Love, S., McAleese, K. E., Nelson, P. T., Neumann, M., Parkkinen, L., Polvikoski, T., Sikorska, B., Smith, C., Grinberg, L. T., … McKeith, I. G. (2021). Neuropathological consensus criteria for the evaluation of Lewy pathology in post-mortem brains: A multi-centre study. Acta Neuropathologica, 141, 159-172. https://doi.org/10.1007/s0040 1- 020-02255 -2 · DOI
  9. Bhasin, M., Rowan, E., Edwards, K., & McKeith, I. (2007). Cholinesterase inhibitors in dementia with Lewy bodies: A comparative analysis. International Journal of Geriatric Psychiatry, 22, 890-895. https:// doi.org/10.1002/gps.1759 · DOI
  10. Bierer, L. M., Haroutunian, V., Gabriel, S., Knott, P. J., Carlin, L. S., Purohit, D. P., Perl, D. P., Schmeidler, J., Kanof, P., & Davis, K. L. (1995). Neurochemical correlates of dementia severity in Alzheimer's disease: Relative importance of the cholinergic deficits. Journal of Neurochemistry, 64, 749-750. https://doi.org/10.1046/ j.1471-4159.1995.64020 749.x · DOI
  11. Bird, T. D., Stranaham, S., Sumi, S. M., & Raskind, M. (1983). Alzheimer's disease: Choline acetyltransferase activity in brain tissue from clin- ical and pathological subgroups. Annals of Neurology, 14, 284-293. https://doi.org/10.1002/ana.41014 0306 · DOI
  12. Bowen, D. M., Smith, C. B., White, P., & Davison, A. N. (1976). Neurotransmitter-related enzymes and indices of hypoxia in senile dementia and other abiotrophies. Brain, 99, 459-496. https://doi. org/10.1093/brain/ 99.3.459 · DOI
  13. Braak, H., & Braak, E. (1995). Staging of Alzheimer's disease-related neu- rofibrillary changes. Neurobiology of Aging, 16, 271-278. discussion 278-284. https://doi.org/10.1016/0197-4580(95)00021 -6 · DOI · Paper page
  14. Braak, H., Del Tredici, K., Bratzke, H., Hamm-Clement, J., Sandmann-Keil, D., & Rub, U. (2002). Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson's disease (preclini- cal and clinical stages). Journal of Neurology, 249(5), 1-5. https://doi. org/10.1007/s0041 5-002-1301-4 · DOI
  15. Braak, H., Rub, U., & Del Tredici, K. (2006). Cognitive decline correlates with neuropathological stage in Parkinson's disease. Journal of the Neurological Sciences, 248, 255-258. https://doi.org/10.1016/j. jns.2006.05.011 · DOI
  16. Brann, M. R., Elis, J., Jorgensen, H., Hill-Eubanks, D., & Jones, S. V. P. (1993). Muscarinic acetylcholine receptor subtypes: Localization and structure/function. In A. C. Cuello (Ed.), Progress in Brain Research (pp. 121-127). Elsevier Science Publishers.
  17. Buciuc, M., Whitwell, J. L., Kasanuki, K., Graff-Radford, J., Machulda, M. M., Duffy, J. R., Strand, E. A., Lowe, V. J., Graff-Radford, N. R., Rush, B. K., Franczak, M. B., Flanagan, M. E., Baker, M. C., Rademakers, R., Ross, O. A., Ghetti, B. F., Parisi, J. E., Raghunathan, A., Reichard, R. R., … Josephs, K. A. (2021). Lewy body disease is a contributor to logopenic progressive aphasia phenotype. Annals of Neurology, 89, 520-533. https://doi.org/10.1002/ana.25979 · DOI
  18. Buratti, E., De Conti, L., Stuani, C., Romano, M., Baralle, M., & Baralle, F. (2010). Nuclear factor TDP-43 can affect selected mi- croRNA levels. The FEBS Journal, 277, 2268-2281. https://doi. org/10.1111/j.1742-4658.2010.07643.x · DOI
  19. Cairns, N. J., Neumann, M., Bigio, E. H., Holm, I. E., Troost, D., Hatanpaa, K. J., Foong, C., White, C. L., Schneider, J. A., Kretzschmar, H. A., Carter, D., Taylor-Reinwald, L., Paulsmeyer, K., Strider, J., Gitcho, M., Goate, A. M., Morris, J. C., Mishra, M., Kwong, L. K., … Mackenzie, I. R. (2007). TDP-43 in familial and sporadic frontotemporal lobar de- generation with ubiquitin inclusions. American Journal of Pathology, 171, 227-240.
  20. Celio, M. R. (1990). Calbindin D-28K and parvalbumin in the rat nervous system. Neuroscience, 35, 375-475. https://doi. org/10.1016/0306-4522(90)90091 -H Celio, M. R., & Norman, A. W. (1985). Nucleus basalis Meynert neu- rons contain the vitamin D-induced calcium-binding protein (Calbindin-D 28K). Anatomy and Embryology, 173, 143-148. https:// doi.org/10.1007/BF003 16296 · DOI
  21. Colloby, S. J., Perry, E. K., Pakrasi, S., Pimlott, S. L., Wyper, D. J., McKeith, I. G., Williams, E. D., & O'Brien, J. T. (2010). Nicotinic 123I- 5IA-85380 single photon emission computed tomography as a pre- dictor of cognitive progression in Alzheimer's disease and dementia with Lewy bodies. American Journal of Geriatric Psychiatry, 18, 86- 90. https://doi.org/10.1097/JGP.0b013 e3181 b972aa · DOI
  22. Cortes, R., Probst, A., & Palacios, J. M. (1987). Quantitative light micro- scopic autoradiographic localization of cholinergic muscarinic re- ceptors in the human brain: Forebrain. Neuroscience, 20, 65-107. https://doi.org/10.1016/0306-4522(87)90006 -6 · DOI
  23. Davies, P. (1979). Neurotransmitter-related enzymes in senile dementia of the Alzheimer type. Brain Research, 171, 319-327. https://doi. org/10.1016/0006-8993(79)90336 -6 · DOI
  24. Davies, P., & Maloney, A. J. F. (1976). Selective loss of central cholin- ergic neurons in Alzheimer's disease. Lancet, 2, 1403. https://doi. org/10.1016/S0140 -6736(76)91936 -X · DOI · Paper page
  25. DeKosky, S. T., Harbaugh, R. E., Schmitt, F. A., Bakay, R. A. E., Chui, H. C., Knopman, D. S., Reeder, T. M., Shetter, A. G., Senter, H. J., & Markesbery, W. R. (1992). Cortical biopsy in Alzheimer's disease: diagnostic accuracy and neurochemical, neuropathological, and cognitive correlates. Annals of Neurology, 32, 625-632.
  26. Dingledine, R., & Kelly, J. S. (1977). Brain stem stimulation and the acetyl- choline-evoked inhibition of neurons in the feline nucleus reticu- laris thalami. Journal of Physiology (London), 271, 135-154.
  27. Doucette, R. B., & Ball, N. J. (1987). Left-right symmetry of neuronal cell counts in the nucleus basalis of Meynert of control and of Alzheimer-diseased brains. Brain Research, 422, 357-360. https:// doi.org/10.1016/0006-8993(87)90944 -9 · DOI
  28. Drachman, D. A., & Leavitt, J. (1974). Human memory and the cholinergic system: A relationship to aging? Archives of Neurology, 30, 113-121. https://doi.org/10.1001/archn eur.1974.00490 32000 1001 · DOI
  29. Ehlers, M. D., Kaplan, D. R., Price, D. L., & Koliatsos, V. E. (1995). NGF- stimulated retrograde transport of trkA in the mammalian ner- vous system. Journal of Cell Biology, 130, 149-156. https://doi. org/10.1083/jcb.130.1.149 · DOI
  30. Emre, M., Aarsland, D., Albanese, A., Byrne, E. J., Deuschl, G., De Deyn, P. P., Durif, F., Kulisevsky, J., van Laar, T., Lees, A., Poewe, W., Robillard, A., Rosa, M. M., Wolters, E., Quarg, P., Tekin, S., & Lane, R. (2004). Rivastigmine for dementia associated with Parkinson's disease. New England Journal of Medicine, 351, 2509-2518.
  31. Emre, M., Heckers, S., Mash, D. C., Geula, C., & Mesulam, M. M. (1993). Cholinergic innervation of the amygdaloid complex in the human brain and its alterations in old age and Alzheimer's disease. Journal of Comparative Neurology, 336, 117-134.
  32. Etienne, P., Robitaille, Y., Wood, P., Gauthier, S., Nair, N. P. V., & Quirion, R. (1986). Nucleus basalis neuronal loss, neuritic plaques, and choline acetyltransferase activity in advanced Alzheimer's disease. Neuroscience, 19, 1279-1291. https://doi. org/10.1016/0306-4522(86)90142 -9 · DOI
  33. Ferguson, I. A., Schweitzer, J. B., Bartlett, P. F., & Johnson, E. M. Jr (1991). Receptor-mediated retrograde transport in CNS neurons after intraventricular administration of NGF and growth factors. The Journal of Comparative Neurology, 313, 680-692.
  34. Fine, A., Hoyle, C., Maclean, C. J., Levatte, T. L., Baker, H. F., & Ridley, R. M. (1997). Learning impairments following injection of a selective cholinergic immunotoxin, ME20.4 IgG-saporin, into the basal nu- cleus of Meynert in monkeys. Neuroscience, 81, 331-343. https:// doi.org/10.1016/S0306 -4522(97)00208 -X · DOI
  35. Fisher, A. (2012). Cholinergic modulation of amyloid precursor pro- tein processing with emphasis on M1 muscarinic receptor: Perspectives and challenges in treatment of Alzheimer's dis- ease. Journal of Neurochemistry, 120(Suppl 1), 22-33. https://doi. org/10.1111/j.1471-4159.2011.07507.x · DOI
  36. Flynn, D. D., Ferraridileo, G., Mash, D. C., & Levey, A. I. (1995). Differential regulation of molecular subtypes of muscarinic receptors in Alzheimer's disease. Journal of Neurochemistry, 64, 1888-1891. https://doi.org/10.1046/j.1471-4159.1995.64041 888.x · DOI
  37. Flynn, D. D., & Mash, D. C. (1986). Characterization of L-[3H]nicotine binding in human cerebral cortex: Comparison between Alzheimer's disease and the normal. Journal of Neurochemistry, 47, 1948-1954.
  38. Gamage, R., Wagnon, I., Rossetti, I., Childs, R., Niedermayer, G., Chesworth, R., & Gyengesi, E. (2020). Cholinergic modulation of glial function during aging and chronic neuroinflammation. Frontiers in Cellular Neuroscience, 14, 577912. https://doi.org/10.3389/ fncel.2020.577912 · DOI
  39. Geula, C., Bu, J., Nagykery, N., Scinto, L. F., Chan, J., Joseph, J., Parker, R., & Wu, C. K. (2003). Loss of calbindin-D28k from aging human cholinergic basal forebrain: Relation to neuronal loss. The Journal of Comparative Neurology, 455, 249-259. https://doi.org/10.1002/ cne.10475 · DOI
  40. Geula, C., & Mesulam, M. M. (1989). Cortical cholinergic fibers in aging and Alzheimer's disease: A morphometric study. Neurosciene, 33, 469-481. https://doi.org/10.1016/0306-4522(89)90399 -0 · DOI
  41. Geula, C., & Mesulam, M. M. (1999). Cholinergic systems in Alzheimer disease. In R. D. Terry, R. Katzman, K. L. Bick, & S. S. Sisodia (Eds.), Alzheimer Disease, Vol. 2 (pp. 269-292). Lippincott Williams and Wilkins.
  42. Geula, C., Nagykery, N., Nicholas, A., & Wu, C. K. (2008). Cholinergic neuronal and axonal abnormalities are present early in aging and in Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 67, 309-318.
  43. Geula, C., Nagykery, N., Wu, C. K., & Bu, J. (2003). Loss of calbindin- D28K from aging human cholinergic basal forebrain: Relation to plaques and tangles. Journal of Neuropathology and Experimental Neurology, 62, 605-616.
  44. Geula, C., Schatz, C. R., & Mesulam, M. M. (1993). Differential localiza- tion of NADPH-diaphorase and calbindin-D28k within the cho- linergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience, 54, 461-476. https://doi.org/10.1016/0306-4522(93)90266 -I · DOI
  45. Gibbons, G. S., Banks, R. A., Kim, B., Changolkar, L., Riddle, D. M., Leight, S. N., Irwin, D. J., Trojanowski, J. Q., & Lee, V. M. Y. (2018). Detection of Alzheimer disease (AD)-specific tau pathology in AD and NonAD tauopathies by immunohistochemistry with novel conformation- selective tau antibodies. Journal of Neuropathology and Experimental Neurology, 77, 216-228. https://doi.org/10.1093/jnen/nly010 · DOI · Paper page
  46. Graeber, M. B., & Muller, U. (2003). Dementia with Lewy bodies: Disease concept and genetics. Neurogenetics, 4, 157-162. https://doi. org/10.1007/s1004 8-003-0155-y · DOI
  47. Graham, A. J., Ray, M. A., Perry, E. K., Jaros, E., Perry, R. H., Volsen, S. G., Bose, S., Evans, N., Lindstrom, J., & Court, J. A. (2003). Differential nicotinic acetylcholine receptor subunit expression in the human hippocampus. Journal of Chemical Neuroanatomy, 25, 97-113. https://doi.org/10.1016/S0891 -0618(02)00100 -X · DOI
  48. Halliday, G. M., McCann, H. L., Pamphlett, R., Brooks, W. S., Creasey, H., McCusker, E., Cotton, R. G., Broe, G. A., & Harper, C. G. (1992). Brain stem serotonin-synthesizing neurons in Alzheimer's disease: A clinicopathological correlation. Acta Neuropathologica, 84, 638- 650. https://doi.org/10.1007/BF002 27741 · DOI
  49. Hansen, L. A. (1994). Pathology of other dementias. In R. D. Terry, R. Katzman, & K. L. Bick (Eds.), Alzheimer disease (pp. 167-177). Raven Press.
  50. Hansen, L. A., DeTeresa, R., Tobias, H., Alford, M., & Terry, R. D. (1988). Neocortical morphometry and cholinergic neurochemistry in Pick's disease. American Journal of Pathology, 131, 507-518.
  51. Hedreen, J. C., Struble, R. G., Whitehouse, P. J., & Price, D. L. (1998). Topography of the magnocellular basal forebrain system in human brain. Journal of Neuropathology & Experimental Neurology, 43, 1-21.
  52. Henke, H., & Lang, W. (1983). Cholinergic enzymes in neocortex, hip- pocampus and basal forebrain of non-neurological and senile de- mentia of Alzheimer-type patients. Brain Research, 267, 281-291. https://doi.org/10.1016/0006-8993(83)90880 -6 · DOI
  53. 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 a historical re- port. Acta Neuropathologica, 86, 215-223. https://doi.org/10.1007/ BF003 04135 · DOI
  54. Hoskin, J. L., Al-Hasan, Y., & Sabbagh, M. N. (2019). Nicotinic acetylcho- line receptor agonists for the treatment of Alzheimer's dementia: An update. Nicotine & Tobacco Research, 21, 370-376. https://doi. org/10.1093/ntr/nty116 · DOI
  55. Hyman, B. T., & Trojanowski, J. Q. (1997). Consensus recommenda- tions for the postmortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 56, 1095-1097.
  56. Janeczek, M., Gefen, T., Samimi, M., Kim, G., Weintraub, S., Bigio, E., Rogalski, E., Mesulam, M. M., & Geula, C. (2018). Variations in ace- tylcholinesterase activity within human cortical pyramidal neurons across age and cognitive trajectories. Cerebral Cortex, 28, 1329- 1337. https://doi.org/10.1093/cerco r/bhx047 · DOI
  57. Janowsky, D. S., Davis, J. M., El-Yousef, M. K., & Sekerke, H. J. (1972). A cholinergic-adrenergic hypothesis of mania and de- pression. Lancet, 2, 632-635. https://doi.org/10.1016/S0140 -6736(72)93021 -8 · DOI · Paper page
  58. Johnson, J. K., Head, E., Kim, R., Starr, A., & Cotman, C. W. (1999). Clinical and pathological evidence for a frontal variant of Alzheimer disease. Archives of Neurology, 56, 1233-1239. https://doi.org/10.1001/ archn eur.56.10.1233 · DOI
  59. Kanel, P., Muller, M., van der Zee, S., Sanchez-Catasus, C. A., Koeppe, R. A., Frey, K. A., & Bohnen, N. I. (2020). Topography of choliner- gic changes in dementia with lewy bodies and key neural network hubs. Journal of Neuropsychiatry and Clinical Neurosciences, 32, 370- 375. https://doi.org/10.1176/appi.neuro psych.19070165 · DOI
  60. Kasashima, S., & Oda, Y. (2003). Cholinergic neuronal loss in the basal forebrain and mesopontine tegmentum of progressive supranu- clear palsy and corticobasal degeneration. Acta Neuropathologica, 105, 117-124. https://doi.org/10.1007/s0040 1-002-0621-x · DOI
  61. Kim, G., Bolbolan, K., Shahidehpour, R., Jamshidi, P., Gefen, T., Ayala, I. A., Weintraub, S., Bigio, E. H., Mesulam, M.-M., & Geula, C. (2019). Morphology and distribution of TDP-43 pre-inclusions in primary progressive aphasia. Journal of Neuropathology and Experimental Neurology, 78, 229-237. https://doi.org/10.1093/jnen/nlz005 · DOI
  62. Koliatsos, V. E., Martin, L. J., Walker, L. C., Richardson, R. T., Delong, M. R., & Price, D. L. (1988). Topographic, non-collateralized basal fore- brain projections to amygdala, hippocampus and anterior cingulate cortex in the rhesus monkey. Brain Research, 463, 133-139. https:// doi.org/10.1016/0006-8993(88)90535 -5 · DOI
  63. Kordower, J. H., Chen, E. Y., Sladek, J. R. Jr, & Mufson, E. J. (1994). trk- immunoreactivity in the monkey central nervous system: Forebrain. The Journal of Comparative Neurology, 349, 20-35. https://doi. org/10.1002/cne.90349 0103 · DOI
  64. Koukouli, F., & Changeux, J. P. (2020). Do nicotinic receptors modulate high-order cognitive processing? Trends in Neurosciences, 43, 550- 564. https://doi.org/10.1016/j.tins.2020.06.001 · DOI
  65. Ladner, C. J., Celesia, G. G., Magnuson, D. J., & Lee, J. M. (1995). Regional al- terations in M1 muscarinic receptor-G protein coupling in Alzheimer's disease. Journal of Neuropathology and Experimental Neurology, 54, 783-789.
  66. Lang, W., & Henke, H. (1983). Cholinergic receptor binding and auto- radiography in brains of non-neurological and senile dementia of Alzheimer-type patients. Brain Research, 267, 271-280. https://doi. org/10.1016/0006-8993(83)90879 -X · DOI
  67. Leanza, G., Muir, J., Nilsson, O. G., Wiley, R. G., Dunnett, S. B., & Bjorklund, A. (1996). Selective immunolesioning of the basal forebrain cholin- ergic system disrupts short-term memory in rats. European Journal of Neuroscience, 8, 1535-1544.
  68. Lee, E. B., Porta, S., Michael Baer, G., Xu, Y., Suh, E. R., Kwong, L. K., Elman, L., Grossman, M., Lee, V.-Y., Irwin, D. J., Van Deerlin, V. M., & Trojanowski, J. Q. (2017). Expansion of the classification of FTLD-TDP: Distinct pathology associated with rapidly progressive frontotemporal degeneration. Acta Neuropathologica, 134, 65-78. https://doi.org/10.1007/s0040 1-017-1679-9 · DOI
  69. Lehericy, S., Hirsch, E. C., Cervera-Pierot, P., Hersh, L. B., Bakchine, S., Piette, F., Duyckaerts, C., Hauw, J. J., Javoy-Agid, F., & Agid, Y. (1993). Heterogeneity and selectivity of the degeneration of cho- linergic neurons in the basal forebrain of patients with Alzheimer's disease. Journal of Comparative Neurolrology, 330, 15-31.
  70. Lidow, M. S., Gallager, D. W., Rakic, P., & Goldman-Rakic, P. S. (1989). Regional differences in the distribution of muscarinic cholinergic re- ceptors in the macaque cerebral cortex. The Journal of Comparative Neurology, 289, 247-259.
  71. Lin, S. C., Olson, K. C., Okazaki, H., & Richelson, E. (1986). Studies on muscarinic binding sites in human brain identified with [3H]piren- zepine. Journal of Neurochemistry, 46, 274-279.
  72. Liu, A. K., Chang, R. C., Pearce, R. K., & Gentleman, S. M. (2015). Nucleus basalis of Meynert revisited: Anatomy, history and dif- ferential involvement in Alzheimer's and Parkinson's disease. Acta Neuropathologica, 129, 527-540. https://doi.org/10.1007/s0040 1-015-1392-5 · DOI
  73. Liu, C., Zhao, Y., Xi, H., Jiang, J., Yu, Y., & Dong, W. (2021). The membrane interaction of alpha-synuclein. Frontiers in Cellular Neuroscience, 15, 633727. https://doi.org/10.3389/fncel.2021.633727 · DOI
  74. Lorenzo, A., & Yankner, B. A. (1994). B-Amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proceedings of the National Academy of Sciences of the United States of America, 91, 12243-12247.
  75. Mackenzie, I. R. A., Neumann, M., Baborie, A., Sampathu, D. M., Du Plessis, D., Jaros, E., Perry, R. H., Trojanowski, J. Q., Mann, D. M. A., & Lee, V. M. Y. (2011). A harmonized classification system for FTLD- TDP pathology. Acta Neuropathologica, 122, 111-113. https://doi. org/10.1007/s0040 1-011-0845-8 · DOI
  76. Mann, D. M. A., Yates, P. O., & Marcyniuk, B. (1985). Correlation be- tween senile plaque and neurofibrillary tangle counts in cerebral cortex and neuronal counts in cortex and subcortical structures in Alzheimer's disease. Neuroscience Letters, 56, 51-55. https://doi. org/10.1016/0304-3940(85)90439 -2 · DOI · Paper page
  77. Mash, D. C., White, W. F., & Mesulam, M. M. (1988). Distribution of mus- carinic receptor subtypes within architectonic subregions of the primate cerebral cortex. The Journal of Comparative Neurology, 278, 265-274.
  78. McGeer, E. G., McGeer, P. L., Kamo, H., Tago, H., & Harrop, R. (1986). Cortical metabolism, acetylcholinesterase staining and pathologi- cal changes in Alzheimer's disease. Canadian Journal of Neurological Sciences, 13, 511-516.
  79. McKeith, I. G., Boeve, B. F., Dickson, D. W., Halliday, G., Taylor, J.-P., Weintraub, D., Aarsland, D., Galvin, J., Attems, J., Ballard, C. G., Bayston, A., Beach, T. G., Blanc, F., Bohnen, N., Bonanni, L., Bras, J., Brundin, P., Burn, D., Chen-Plotkin, A., … Kosaka, K. (2017). Diagnosis and management of dementia with Lewy bodies: Fourth consensus report of the DLB consortium. Neurology, 89, 88-100. https://doi.org/10.1212/WNL.00000 00000 004058 · DOI · Paper page
  80. McKeith, I. G., Galasko, D., Kosaka, K., Perry, E. K., Dickson, D. W., Hansen, L. A., Salmon, D. P., Lowe, J., Mirra, S. S., Byrne, E. J., Lennox, G., Quinn, N. P., Edwardson, J. A., Ince, P. G., Bergeron, C., Burns, A., Miller, B. L., Lovestone, S., Collerton, D., … Perry, R. H. (1996). Consensus guidelines for the clinical and pathologic diagno- sis of dementia with Lewy bodies (DLB): Report of the consortium on DLB international workshop. Neurology, 47, 1113-1124. https:// doi.org/10.1212/WNL.47.5.1113 · DOI · Paper page
  81. Mesulam, M. M., & Geula, C. (1988). Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: Observations based on the distribution of acetylcholinesterase and choline acetyltransfer- ase. The Journal of Comparative Neurology, 275, 216-240. https:// doi.org/10.1002/cne.90275 0205 · DOI
  82. Mesulam, M. M., & Geula, C. (1991). Acetylcholinesterase-rich neurons of the human cerebral cortex: Cytoarchitectonic and ontogenetic patterns of distribution. The Journal of Comparative Neurology, 306, 193-220. https://doi.org/10.1002/cne.90306 0202 · DOI
  83. Mesulam, M. M., Geula, C., Bothwell, M. A., & Hersh, L. B. (1989). Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical compar- isons to forebrain cholinergic neurons. The Journal of Comparative Neurology, 281, 611-633. https://doi.org/10.1002/cne.90283 0414 · DOI
  84. Mesulam, M.-M., Lalehzari, N., Rahmani, F., Ohm, D., Shahidehpour, R., Kim, G., Gefen, T., Weintraub, S., Bigio, E., & Geula, C. (2019). Cortical cholinergic denervation in primary progressive aphasia with Alzheimer pathology. Neurology, 92, e1580-e1588. https:// doi.org/10.1212/WNL.00000 00000 007247 · DOI
  85. Mesulam, M. M., Mash, D., Hersh, L., Bothwell, M., & Geula, C. (1992). Cholinergic innervation of the human striatum, globus pallidus, subthalamic nucleus, substantia nigra, and red nucleus. The Journal of Comparative Neurology, 323, 252-268. https://doi.org/10.1002/ cne.90323 0209 · DOI
  86. Mesulam, M., Shaw, P., Mash, D., & Weintraub, S. (2004). Cholinergic nu- cleus basalis tauopathy emerges early in the aging-MCI-AD contin- uum. Annals of Neurology, 55, 815-828.
  87. Mesulam, M. M., & Van Hoesen, G. W. (1976). Acetylcholinesterase- rich projections from the basal forebrain of the rhesus mon- key to neocortex. Brain Research, 109, 152-157. https://doi. org/10.1016/0006-8993(76)90385 -1 · DOI
  88. Mesulam, M. M., Volicer, L., Marquis, J. K., Mufson, E. J., & Green, R. C. (1986). Systematic regional differences in the cholinergic inner- vation of the primate cerebral cortex: Distribution of enzyme ac- tivities and some behavioral implications. Annals of Neurology, 19, 144-151. https://doi.org/10.1002/ana.41019 0206 · DOI
  89. Mirra, S. S., Hart, M. N., & Terry, R. D. (1993). Making the diagnosis of Alzheimer's disease. A primer for practicing pathologists [see com- ments]. [Review]. Archives of Pathology and Laboratory Medicine, 117, 132-144.
  90. Mizukami, K., & Kosaka, K. (1989). Neuropathological study on the nu- cleus basalis of Meynert in Pick's disease. Acta Neuropathologica, 78, 52-56. https://doi.org/10.1007/BF006 87402 · DOI
  91. Moran, S. P., Maksymetz, J., & Conn, P. J. (2019). Targeting muscarinic acetylcholine receptors for the treatment of psychiatric and neu- rological disorders. Trends in Pharmacological Sciences, 40, 1006- 1020. https://doi.org/10.1016/j.tips.2019.10.007 · DOI
  92. Mufson, E. J., Bothwell, M., Hersh, L. B., & Kordower, J. H. (1989). Nerve growth factor receptor immunoreactive profiles in the normal, aged human basal forebrain: Colocalization with cholinergic neu- rons. The Journal of Comparative Neurology, 285, 196-217.
  93. Mufson, E. J., Bothwell, M., & Kordower, J. H. (1989). Loss of nerve growth factor receptor-containing neurons in Alzheimer's dis- ease: A quantitative analysis across subregions of the basal forebrain. Experimental Neurology, 105, 221-232. https://doi. org/10.1016/0014-4886(89)90124 -6 · DOI
  94. Mufson, E. J., Ma, S. Y., Cochran, E. J., Bennett, D. A., Beckett, L. A., Jaffar, S., Saragovi, H. U., & Kordower, J. H. (2000). Loss of nucleus basalis neurons containing trkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease. The Journal of Comparative Neurology, 427, 19-30.
  95. Mufson, E. J., Ma, S. Y., Dills, J. et al (2002). Loss of basal forebrain p75(NTR) immunoreactivity in subjects with mild cognitive impair- ment and Alzheimer's disease. The Journal of Comparative Neurology, 443, 136-153.
  96. Muir, J. L., Dunnett, S. B., Robbins, T. W., & Everitt, B. J. (1992). Attentional functions of the forebrain cholinergic systems: Effects of intraven- tricular hemicholinium, physostigmine, basal forebrain lesions and intracortical grafts on a multiple-choice serial reaction time task. Experimental Brain Research, 89, 611-622. https://doi.org/10.1007/ BF002 29886 14714159, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jnc.15471, Wiley Online Library on [30/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License · DOI
  97. Narasimhan, S., Guo, J. L., Changolkar, L., Stieber, A., McBride, J. D., Silva, L. V., He, Z., Zhang, B., Gathagan, R. J., Trojanowski, J. Q., & Lee, V. M. Y. (2017). Pathological tau strains from human brains reca- pitulate the diversity of tauopathies in nontransgenic mouse brain. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 37, 11406-11423. https://doi.org/10.1523/JNEUR OSCI.1230-17.2017 · DOI · Paper page
  98. Narayanan, R. K., Mangelsdorf, M., Panwar, A., Butler, T. J., Noakes, P. G., & Wallace, R. H. (2012). Identification of RNA bound to the TDP-43 ribonucleoprotein complex in the adult mouse brain. Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration, 14(4), 252-260. https://doi.org/10.3109/21678 421.2012.734520 · DOI
  99. Nelson, P. T., Dickson, D. W., Trojanowski, J. Q., Jack, C. R., Boyle, P. A., Arfanakis, K., Rademakers, R., Alafuzoff, I., Attems, J., Brayne, C., Coyle-Gilchrist, I. T. S., Chui, H. C., Fardo, D. W., Flanagan, M. E., Halliday, G., Hokkanen, S. R. K., Hunter, S., Jicha, G. A., Katsumata, Y., … Schneider, J. A. (2019). Limbic-predominant age-related TDP- 43 encephalopathy (LATE): Consensus working group report. Brain, 142, 1503-1527. https://doi.org/10.1093/brain/ awz099 · DOI · Paper page
  100. Nordberg, A., Adem, A., Hardy, J., & Winblad, B. (1988). Changes in nic- otinic receptor subtypes in temporal cortex of Alzheimer brains. Neuroscience Letters, 36, 317-321.
  101. Nordberg, A., Alafuzoff, I., & Winblad, B. (1992). Nicotinic and musca- rinic subtypes in the human brain: Changes with aging and de- mentia. Journal of Neuroscience Research, 31, 103-111. https://doi. org/10.1002/jnr.49031 0115 · DOI
  102. Perry, E. K., Gibson, P. H., Blessed, G., Perry, R. H., & Tomlinson, B. E. (1977). Neurotransmitter enzyme abnormalities in senile dementia. Journal of the Neurological Sciences, 34, 247-265.
  103. Perry, E. K., Morris, C. M., Court, J. A., Cheng, A., Fairbairn, A. F., McKeith, I. G., Irving, D., Brown, A., & Perry, R. H. (1995). Alteration in nicotine binding sites in Parkinson's disease, Lewy body dementia and Alzheimer's disease: Possible index of early neuropathology. Neuroscience, 64, 385-395. https://doi. org/10.1016/0306-4522(94)00410 -7 · DOI
  104. Podlisny, M. B., Ostaszewski, B. L., Squazzo, S. L., Koo, E. H., Rydell, R. E., Teplow, D. B., & Selkoe, D. J. (1995). Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. Journal of Biological Chemistry, 270, 9564-9570.
  105. Ransmayr, G., Cervera, P., Hirsch, E. C., Berger, W., Fischer, W., & Agid, Y. (1992). Alzheimer's disease: Is the decrease of the cho- linergic innervation of the hippocampus related to intrinsic hippocampal pathology? Neuroscience, 47, 843-851. https://doi. org/10.1016/0306-4522(92)90034 -Y Ransmayr, G., Cervera, P., Hirsch, E., Ruberg, M., Hersh, L. B., Duyckaerts, C., Hauw, J. J., Dellumeau, C., & Agid, Y. (1989). Choline acetyltransferase-like immunoreactivity in the hip- pocampal formation of control subjects and patients with Alzheimer's disease. Neuroscience, 32, 701-714. https://doi. org/10.1016/0306-4522(89)90291 -1 · DOI
  106. Riascos, D., de Leon, D., Baker-Nigh, A., Nicholas, A., Yukhananov, R., Bu, J., Wu, C. K., & Geula, C. (2011). Age-related loss of calcium buffering and selec- tive neuronal vulnerability in Alzheimer's disease. Acta Neuropathologica, 122, 565-576. https://doi.org/10.1007/s0040 1-011-0865-4 · DOI
  107. Rinne, J. O., Paljarvi, L., & Rinne, U. K. (1987). Neuronal size and density in the nucleus basalis of Meynert in Alzheimer's disease. Journal of the Neurological Sciences, 79, 67-76.
  108. Rintoul, G. L., Raymond, L. A., & Baimbridge, K. G. (2001). Calcium buff- ering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells. Cell Calcium, 29, 277-287. https:// doi.org/10.1054/ceca.2000.0190 · DOI
  109. Rodriguez-Puertas, R., Pascual, J., Vilaro, T., & Pazos, A. (1997). Autoradiographic distribution of M1, M2, M3, and M4 muscarinic receptor subtypes in Alzheimer's disease. Synapse (New York, N. Y.), 26, 341-350. https://doi.org/10.1002/(SICI)1098-2396(19970 8)26:4<341:AID-SYN2>3.0.CO;2-6 · DOI
  110. Rogalski, E., Sridhar, J., Rader, B., Martersteck, A., Chen, K., Cobia, D., Thompson, C. K., Weintraub, S., Bigio, E. H., & Mesulam, M.-M. (2016). Aphasic variant of Alzheimer disease: Clinical, anatomic, and genetic features. Neurology, 87, 1337-1343. https://doi. org/10.1212/WNL.00000 00000 003165 · DOI
  111. Rossor, M. N., Garrett, N. J., Johnson, A. L., Mountjoy, C. Q., Roth, M., & Iversen, L. L. (1982). A post-mortem study of the cholinergic and GABA systems in senile dementia. Brain, 105, 313-330. https://doi. org/10.1093/brain/ 105.2.313 · DOI
  112. Rossor, M. N., Iversen, L. L., Johnson, A. J., Mountjoy, C. Q., & Roth, M. (1981). Cholinergic deficit in frontal cerebral cortex in Alzheimer's disease is age dependent. Lancet, 2, 1422. https://doi.org/10.1016/ S0140 -6736(81)92836 -1 · DOI
  113. Sahin, H. A., Emre, M., Ziabreva, I., Perry, E., Celasun, B., & Perry, R. (2006). The distribution pattern of pathology and cholinergic defi- cits in amygdaloid complex in Alzheimer's disease and dementia with Lewy bodies. Acta Neuropathologica, 111, 115-125. https:// doi.org/10.1007/s0040 1-005-0003-2 · DOI
  114. Scott, S. A., Mufson, E. J., Weingartner, J. A., Skau, K. A., & Crutcher, K. A. (1995). Nerve growth factor in Alzheimer's disease: Increased lev- els throughout the brain coupled with declines in nucleus basalis. Journal of Neuroscience, 15, 6213-6221. https://doi.org/10.1523/ JNEUR OSCI.15-09-06213.1995 · DOI
  115. Selkoe, D. J. (1994). Normal and abnormal biology of the á-amyloid pre- curser protein. Annual Review of Neuroscience, 17, 489-517.
  116. Shah, P., Lal, N., Leung, E., Traul, D. E., Gonzalo-Ruiz, A., & Geula, C. (2010). Neuronal and axonal loss are selectively linked to fibrillar amyloid-{beta} within plaques of the aged primate cerebral cortex. American Journal of Pathology, 177, 325-333.
  117. Shimohama, S., Taniguchi, T., Fujiwara, M., & Kameyama, M. (1986). Changes in nicotinic and muscarinic cholinergic receptors in Alzheimer-type dementia. Journal of Neurochemistry, 46, 288-293. https://doi.org/10.1111/j.1471-4159.1986.tb129 60.x Shiozaki, K., & Iseki, E. (2004). Decrease in GTP-sensitive high affinity agonist binding of muscarinic acetylcholine receptors in autop- sied brains of dementia with Lewy bodies and Alzheimer's disease. Journal of the Neurological Sciences, 223, 145-148. https://doi. org/10.1016/j.jns.2004.05.002 · DOI
  118. Stoehr, J. D., Mobley, S. L., Roice, D., Brooks, R., Baker, L. M., Wiley, R. G., & Wenk, G. L. (1997). The effects of selective cholinergic basal fore- brain lesions and aging upon expectancy in the rat. Neurobiology of Learning and Memory, 67, 214-227.
  119. Svensson, A. L., Warpman, U., Hellstrom-Lindahl, E., Bogdanovic, N., Lannfelt, L., & Nordberg, A. (1997). Nicotinic receptors, muscarinic receptors and choline acetyltransferase activity in the temporal cortex of Alzheimer patients with differing apolipoprotein E gen- otypes. Neuroscience Letters, 232, 37-40. https://doi.org/10.1016/ S0304 -3940(97)00573 -9 · DOI
  120. Tagliavini, F., Pillari, G., Bouras, C., Constantinidis, J., & Acta, N. S. (1984). The basal nucleus of Meynert in idiopathic Parkinson's disease. No Journal Found, 69, 20-28. https://doi.org/10.1111/ j.1600-0404.1984.tb007 · DOI
  121. x Tagliavini, F., & Pilleri, G. (1983). Basal nucleus of Meynert: A neuro- pathological study in Alzheimer's disease, simple senile dementia, pick's disease and huntington's chorea. Journal of the Neurological Sciences, 62, 243-260. · DOI
  122. Tagliavini, F., Pilleri, G., Bouras, C., & Constantinidis, J. (1984). The basal nucleus of Meynert in patients with progressive supra- nuclear palsy. Neuroscience Letters, 44, 37-42. https://doi. org/10.1016/0304-3940(84)90217 -9 · DOI
  123. Tagliavini, F., Pilleri, G., Gemignani, F., & Lechi, A. (1983). Neuronal loss in the basal nucleus of Meynert in progressive supranuclear palsy. Acta Neuropathologica, 61, 157-160. https://doi.org/10.1007/ BF006 97397 · DOI
  124. Teaktong, T., Graham, A. J., Court, J. A., Perry, R. H., Jaros, E., Johnson, M., Hall, R., & Perry, E. K. (2004). Nicotinic acetylcholine receptor immunohistochemistry in Alzheimer's disease and dementia with Lewy bodies: Differential neuronal and astroglial pathology. Journal of the Neurological Sciences, 225, 39-49. https://doi.org/10.1016/j. jns.2004.06.015 · DOI
  125. Terry, R. D. (1998). The cytoskeleton in Alzheimer disease. Journal of Neural Transmission, 53, 141-145.
  126. Terry, R. D., Masliah, E., & Hansen, L. A. (1994). Structural basis of cognitive alterations in Alzheimer's disease. In R. D. Terry, R. Katzman, & K. L. Bick (Eds.), Alzheimer Disease (pp. 179-196).
  127. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., & Katzman, R. (1991). Physical basis of cognitive al- terations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Annals of Neurology, 30, 572-580.
  128. Terry, R. D., & Wisniewski, H. M. (1972). Ultrastructure of senile demen- tia and of experimental analogues. In C. M. Gaitz (Ed.), Aging and the Brain (pp. 89-116). Plenum Press.
  129. Tiraboschi, P., Hansen, L. A., Alford, M., Sabbagh, M. N., Schoos, B., Masliah, E., Thal, L. J., & Corey-Bloom, J. (2000). Cholinergic dys- function in diseases with Lewy bodies. Neurology, 54, 407-411. https://doi.org/10.1212/WNL.54.2.407 · DOI
  130. Tollervey, J. R., Curk, T., Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobágyi, T., Nishimura, A. L., Župunski, V., Patani, R., Chandran, S., Rot, G., Zupan, B., Shaw, C. E., & Ule, J. (2011). Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nature Neuroscience, 14, 452-458. https:// doi.org/10.1038/nn.2778 · DOI · Paper page
  131. Tuszynski, M. H., U, H. S., Amaral, D. G., & Gage, F. H. (1990). Nerve growth factor infusion in the primate brain reduces lesion-induced cho- linergic neuronal degeneration. Journal of Neuroscience, 10, 3604- 3614. https://doi.org/10.1523/JNEUR OSCI.10-11-03604.1990 · DOI
  132. Uhl, G. R., Hilt, D. C., Hedreen, J. C., Whitehouse, P. J., & Price, D. L. (1983). Pick's disease (lobar sclerosis): Depletion of neurons in the nucleus basalis of Meynert. Neurology, 33, 1470-1473. https://doi. org/10.1212/WNL.33.11.1470 · DOI
  133. Vanderhayden, P., Ebinger, G., Dierckx, R., & Vauquelin, G. (1987). Muscarinic cholinergic receptor subtypes in normal human brain and Alzheimer's presenile dementia. Journal of the Neurological Sciences, 82, 257-269.
  134. Walsh, T. J., Herzog, C. D., Gandhi, C., Stackman, R. W., & Wiley, R. G. (1996). Injection of IgG 192-saporin into the medial septum pro- duces cholinergic hypofunction and dose-dependent working memory deficits. Brain Research, 726, 69-79.
  135. Warren, N. M., Piggott, M. A., Lees, A. J., Perry, E. K., & Burn, D. J. (2008). Intact coupling of M1 receptors and preserved M2 and M4 recep- tors in the cortex in progressive supranuclear palsy: Contrast with other dementias. Journal of Chemical Neuroanatomy, 35, 268-274. https://doi.org/10.1016/j.jchem neu.2008.01.001 · DOI
  136. Whitehouse, P. J., Hedreen, J. C., White, C. L., & Price, D. L. (1983). Basal forebrain neurons in the dementia of Parkinson disease. Annals of Neurology, 13, 243-348.
  137. Whitehouse, P. J., Martino, A. M., Marcus, K. A., Zweig, R. M., Singer, H. S., Price, D. L., & Kellar, K. J. (1988). Reductions in acetyl- choline and nicotine binding in several degenerative diseases. Archives of Neurology, 45, 722-724. https://doi.org/10.1001/archn eur.1988.00520 31002 8012 · DOI
  138. Whitehouse, P. J., Price, D. L., Clark, A. W., Coyle, J. T., & DeLong, M. R. (1981). Alzheimer disease: Evidence for selective loss of cholinergic neurons in the nucleus basalis. Annals of Neurology, 10, 122-126. https://doi.org/10.1002/ana.41010 0203 · DOI · Paper page
  139. Wilcock, G. K., Esiri, M. M., Bowen, D. M., & Smith, C. C. T. (1982). Alzheimer's disease. Correlation of cortical choline acetyltransfer- ase activity with the severity of dementia and histological abnor- malities. Journal of the Neurological Sciences, 57, 407-417.
  140. Wisniewski, H. M., Bancher, C., Barcikowska, M., Wen, G. Y., & Currie, J. (1989). Spectrum of morphological appearance of amyloid deposits in Alzheimer's disease. Acta Neuropathologica, 78, 337-347. https:// doi.org/10.1007/BF006 88170 · DOI
  141. Wood, P. L., Etienne, P., Lal, S., Nair, N., Finlayson, M. H., Gauthier, S., Palo, J., Haltia, M., Paetau, A., & Bird, E. D. (1983). A post-mortem comparison of the cortical cholinergic system in Alzheimer's dis- ease and Pick's disease. Journal of the Neurological Sciences, 62, 211-217. https://doi.org/10.1016/0022-510X(83)90200 -9 · DOI
  142. Wood, P. L., Nair, N. P. V., Etienne, P., Lal, S., Gauthier, S., Robitaille, Y., Bird, E. D., Palo, J., Haltia, M., & Paetau, A. (1983). Lack of 14714159, 2021, 6, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jnc.15471, Wiley Online Library on [30/08/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License cholinergic deficit in the neocortex in Pick's disease. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 7, 725-727. https://doi.org/10.1016/0278-5846(83)90053 -2 · DOI
  143. Wu, C. K., Mesulam, M. M., & Geula, C. (1997). Age-related loss of calbin- din from human basal forebrain cholinergic neurons. NeuroReport, 8, 2209-2213. https://doi.org/10.1097/00001 756-19970 7070- 00024 · DOI
  144. Wu, C. K., Nagykery, N., Hersh, L. B., Scinto, L. F., & Geula, C. (2003). Selective age-related loss of calbindin-D28k from basal forebrain cholinergic neurons in the common marmoset (Callithrix jacchus). Neuroscience, 120, 249-259. https://doi.org/10.1016/S0306 -4522(03)00248 -3 · DOI
  145. Xu, H., O'Reilly, M., Gibbons, G. S., Changolkar, L., McBride, J. D., Riddle, D. M., Zhang, B., Stieber, A., Nirschl, J., Kim, S.-J., Hoxha, K.-H., Brunden, K. R., Schellenberg, G. D., Trojanowski, J. Q., & Lee, V.-Y. (2021). In vitro amplification of pathogenic tau conserves disease- specific bioactive characteristics. Acta Neuropathologica, 141, 193- 215. https://doi.org/10.1007/s0040 1-020-02253 -4 · DOI
  146. Yates, C. M., Simpson, J., Maloney, A. F., & Gordon, A. (1980). Neurochemical observations in a case of Pick's disease. Journal of the Neurological Sciences, 48, 257-263.

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Authors
Geula, C., Dunlop, S. R., Ayala, I., Kawles, A. S., Flanagan, M. E., Gefen, T., & Mesulam, M.
Affiliations
  • Northwestern University (US)
  • Mesulam Center for Cognitive Neurology and Alzheimer’s Disease Feinberg School of Medicine Chicago Northwestern University Chicago Illinois USA
Corresponding author
Geula, Changiz
Venue
Journal of Neurochemistry
Publisher
Wiley
Published
2021-08-06
Volume
158
Issue
6
Pages
1394-1411
ISSN
  • 0022-3042 (ISSN-L)
  • 1471-4159
OpenAlex
W3179818940
Cited by
102
References
9
Citations by year
2026: 25 · 2025: 21 · 2024: 26 · 2023: 12 · 2022: 15 · 2021: 3
FWCI
1.85
Type
journal article
Language
en
Open access
Locations
  • Journal of Neurochemistry (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Neurological Disorders and Stroke (NS085770)
  • National Institute on Deafness and Other Communication Disorders (DC008552)
  • National Institute on Aging (AG013854, AG062566, AG065463)
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
basal forebrain cholinergic neurons, dementia, Alzheimer's disease, dementia with Lewy bodies, frontotemporal lobar degeneration, FTLD-tau, FTLD-TDP, Pick's disease, tauopathy, TDP-43 proteinopathy, neurofibrillary tangles, Lewy bodies, corticofugal axons, neuronal vulnerability, neuronal resilience
MeSH terms
Alzheimer Disease, Animals, Choline O-Acetyltransferase, Dementia, Disease Susceptibility, Humans, Nerve Degeneration, Receptors, Cholinergic, Lewy Body Disease, Tauopathies, Resilience, Psychological, Frontotemporal Lobar Degeneration, Cholinergic Neurons, Basal Forebrain

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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