Memory‐related neural systems in Alzheimer's disease: An anatomic study
Abstract
In the primate brain, there are strong connections among the entorhinal cortex, the hippocampal formation, and the amygdala, 3 structures of the ventromedial temporal lobe that are related to memory function. Because memory impairment is a central feature of Alzheimer's disease, we examined the probable cells of origin and terminal zones of these connections in the brains of humans affected by the disease, using thioflavine S, Alz-50, and anti-A4 amyloid protein immunocytochemistry. Specific cytoarchitectural areas and lamina that give rise to projections from the entorhinal cortex, the hippocampal formation, and the amygdala consistently contained neurofibrillary tangles. The terminal zones of many of these projections contained neuritic plaques, Alz-50-positive neuritic alterations, and A4 deposition. Other cytoarchitectural areas and lamina, sometimes immediately adjacent, were consistently spared from these Alzheimer changes. This pattern of Alzheimer-related alterations would disrupt projections among the entorhinal cortex, hippocampal formation, and amygdala at multiple sites, and also disrupt projections between these structures and cortical and subcortical targets. In functional terms, this pattern of structural damage is likely to be as devastating as bilateral destruction of the ventromedial temporal lobe, and thus contribute substantially to the memory disorder seen in this condition.
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According to Hyman et al., episodic memory deficit in AD results from anatomical and functional segregation of hippocampus from associative sensory inputs due to degeneration of perforant pathway.
“Indeed, according to Hyman et al. [29], [30], the episodic memory deficit in AD patients results from the anatomical and functional segregation of the hippocampus from associative sensory inputs due to degeneration of the perforant pathway.”
From Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease (2015) · cites this paper as [29]
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Buckner, R. L., Andrews‐Hanna, J. R., & Schacter, D. L. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1440.011 · Cited by 9,761 · see citing works
“Several theories have offered explanations for why memory structures are particularly vulnerable to the disease, including ideas based on anatomy (Hyman et al. 1990) and also the possibility that memory structures are sensitive to toxicity because of their role in plasticity (Mesulam 2000b).”
BackgroundGauthier, S. G., Reisberg, ., Zaudig, M., Petersen, R. C., Ritchie, K. A., Broich, K., Belleville, S., Brodaty, H., Bennett, D. A., Chertkow, H. M., et al. (2006) · The Lancet · doi:10.1016/s0140-6736(06)68542-5 · Cited by 3,920 · see citing works
Stages in the development of Parkinson’s disease-related pathology
Braak, H., Ghebremedhin, E., Rüb, U., Bratzke, H., & Del Tredici, K. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0956-9 · Cited by 2,689 · see citing works
“3B; Hyman et al. 1990; Mesulam 1998).”
Staging of alzheimer's disease-related neurofibrillary changes
Braak, H., & Braak, E. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00021-6 · Cited by 2,357 · see citing works
Buckner, R. L., Snyder, A. Z., Shannon, B. J., LaRossa, G., Sachs, R., Fotenos, A. F., Sheline, Y. I., Klunk, W. E., Mathis, C. A., Morris, J. C., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2177-05.2005 · Cited by 2,140 · see citing works
“Memory networks have been described previously as having particular vulnerability in AD based on their anatomic disruption (Hyman et al., 1990) and molecular properties associated with plasticity (Mesulam, 2000).”
BackgroundScheltens, P., Leys, D., Barkhof, F., Huglo, D. G., Weinstein, H. C., Vermersch, P., Kuiper, M. A., Steinling, M., Wolters, E. C., & Valk, J. (1992) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.55.10.967 · Cited by 1,781 · see citing works
Propagation of Tau Pathology in a Model of Early Alzheimer's Disease
de Calignon, A., Polydoro, M., Suárez-Calvet, M., William, C., Adamowicz, D. H., Kopeikina, K. J., Pitstick, R., Sahara, N., Ashe, K. H., Carlson, G. A., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.033 · Cited by 1,427 · see citing works
“Selective loss of these neurons are believed to contribute to the defects in memory and higher order cognitive functions in Alzheimer’s disease due to disconnection and deafferentation of critical neural circuits (Delacourte et al., 1999; Hyman et al., 1990).”
Self-citationLife and Death of Neurons in the Aging Brain
Morrison, J. H., & Hof, P. R. (1997) · Science · doi:10.1126/science.278.5337.412 · Cited by 1,344 · see citing works
Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease
West, M. J., Coleman, P. D., Flood, D. G., & Troncoso, J. C. (1994) · The Lancet · doi:10.1016/s0140-6736(94)92338-8 · Cited by 1,267 · see citing works
Schmahmann, J. D., & Pandya, D. N. (2006) · doi:10.1093/acprof:oso/9780195104233.001.0001 · Cited by 1,157 · see citing works
Izquierdo, I., & Medina, J. H. (1997) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3799 · Cited by 959 · see citing works
“manager regions of the prefrontal cortex (Fuster, 1995), which is related by the entorhinal cortex and the dentate gyrus (Hyman et al., 1990; Willner et al., 1993; Witter et al., 1989).”
BackgroundInfluentialEvolution of the neuropathology of Alzheimer's disease
Braak, H., & Braak, E. (1996) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1996.tb05866.x · Cited by 710 · see citing works
Galton, C. J. (2000) · Brain · doi:10.1093/brain/123.3.484 · Cited by 613 · see citing works
MUTANT GENES IN FAMILIAL ALZHEIMER'S DISEASE AND TRANSGENIC MODELS
Price, D. L., & Sisodia, S. S. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.479 · Cited by 568 · see citing works
Neocortical Neurofibrillary Tangles Correlate With Dementia Severity in Alzheimer's Disease
Bierer, L. M., Hof, P. R., Purohit, D. P., Carlin, L., Schmeidler, J., Davis, K. L., & Perl, D. P. (1995) · Archives of Neurology · doi:10.1001/archneur.1995.00540250089017 · Cited by 514 · see citing works
Perry, R. J., Watson, P., & Hodges, J. R. (2000) · Neuropsychologia · doi:10.1016/s0028-3932(99)00079-2 · Cited by 491 · see citing works
Evolution of neuronal changes in the course of Alzheimer’s disease
Braak, H., & Braak, E. (1998) · Journal of neural transmission. Supplementum · doi:10.1007/978-3-7091-6467-9_11 · Cited by 482 · see citing works
Entorhinal cortex pathology in Alzheimer's disease
van Hoesen, G. W., Hyman, B. T., & Damasio, A. R. (1991) · Hippocampus · doi:10.1002/hipo.450010102 · Cited by 475 · see citing works
Self-citationBobinski, M., de Leon, M. J., Wegiel, J., DeSanti, S., Convit, A., Saint Louis, L. A., Rusinek, H., & Wisniewski✠, H. M. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00476-5 · Cited by 455 · see citing works
Different molecular cascades in different sites of the brain control memory consolidation
Izquierdo, I., Bevilaqua, L. R., Rossato, J. I., Bonini, J. S., Medina, J. H., & Cammarota, M. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.07.005 · Cited by 452 · see citing works
“From the systems point of view, information leading to memory consolidation should flow from CA1 through the subiculum and then the entorhinal cortex to the rest of the cortex and the basolateral amygdala [9,27,87,88], which in turn should project back to the entorhinal cortex and the hippocampal dentate‐CA3‐CA1 syste…”
BackgroundInfluentialIzquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Alzheimer's disease and oxidative stress: implications for novel therapeutic approaches
Behl, C. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00055-0 · Cited by 444 · see citing works
Molecular Basis of the Neurodegenerative Disorders
Martin, J. B. (1999) · New England Journal of Medicine · doi:10.1056/nejm199906243402507 · Cited by 416 · see citing works
Diagnostic Criteria for Neuropathologic Assessment of Alzheimer’s Disease
Braak, H., & Braak, E. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00062-6 · Cited by 410 · see citing works
Kaye, J. A., Swihart, T., Howieson, D., Dame, A., Moore, M. M., Karnos, T., Camicioli, R., Ball, M., Oken, B., & Sexton, G. (1997) · Neurology · doi:10.1212/wnl.48.5.1297 · Cited by 399 · see citing works
Izquierdo, I., Cunha, C. D., Rosat, R. M., Jerusalinsky, D. A., Ferreira, M. B. C., & Medina, J. H. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90847-w · Cited by 395 · see citing works
Aggleton, J. P., Pralus, A., Nelson, A. J. D., & Hornberger, M. (2016) · Brain · doi:10.1093/brain/aww083 · Cited by 378 · see citing works
“, 1986), a region that shows pronounced cell loss and neurofibrillary tangle formation in Alzheimer’s disease (Hyman et al., 1990).”
BackgroundNeuropathology of Alzheimer’s disease: what is new since A. Alzheimer?
Braak, E., Griffing, K., Arai, K., Böhl, J., Bratzke, H., & Braak, H. (1999) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/pl00014168 · Cited by 370 · see citing works
Sequence of Aβ-protein deposition in the human medial temporal lobe
Thal, D. R., Rüb, U., Schultz, C., Sassin, I., Ghebremedhin, E., Del Tredici, K., Braak, E., & Braak, H. (2000) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/59.8.733 · Cited by 370 · see citing works
The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases
Braak, H., & Braak, E. (1992) · Neuroscience Research · doi:10.1016/0168-0102(92)90014-4 · Cited by 340 · see citing works
Pattern of brain destruction in Parkinson's and Alzheimer's diseases
Braak, H., Braak, E., Yilmazer‐Hanke, D., de Vos, R. A. I., Jansen, E. N. H., & Böhl, J. (1996) · Journal of Neural Transmission · doi:10.1007/bf01276421 · Cited by 329 · see citing works
“The structural integrity of many of these components is a prerequisite for the maintenance of emotional stability, learning abilities, and memory functions (Mishkin, 1982; Amaral, 1987; Squire and Zola-Morgan, 1988, 1991; Hyman et al., 1990; Damasio and Damasio, 1991; Zola-Morgan and Squire, 1993; Markowitsch, 1995).”
BackgroundHippocampal Atrophy in Normal Aging
Golomb, J. B. (1993) · Archives of Neurology · doi:10.1001/archneur.1993.00540090066012 · Cited by 323 · see citing works
The Temporal Relationship Between Depressive Symptoms and Dementia
Chen, P., Ganguli, M., Mulsant, B. H., & DeKosky, S. T. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.3.261 · Cited by 318 · see citing works
“Also, 2 conditions may share common pathways through an interaction between the hippocampus and the hypothalamicpituitary-adrenal axis.(40-48) Clues may emerge from trials of the effects of antidementia drugs on mood or of the effects of antidepressant drugs on cognition: studies of trichlorfon (metrifonate) and tacri…”
BackgroundBancher, C., Braak, H., Fischer, P., & Jellinger, K. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90590-h · Cited by 314 · see citing works
Izquierdo, I., Quillfeldt, J. A., Zanatta, M. S., Quevedo, J., Schaeffer, E. L., Schmitz, P. K., & Medina, J. H. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01427.x · Cited by 314 · see citing works
“It is logical to think that the sequential role of these structures in post-training memory processing obeys their anatomical connections (Witter et al., 1989; Hyman et al., 1990; Iijima et al., 1996; Suzuki, 1996).”
BackgroundLeone, P., Janson, C. G., Bilianuk, L., Wang, Z., Sorgi, F., Huang, L., Matalon, R. K., Kaul, R., Zeng, Z., Freese, A. B., et al. (2000) · Annals of Neurology · doi:10.1002/1531-8249(200007)48:1 · Cited by 174 · see citing works
Amygdalohippocampal MR volume measurements in the early stages of Alzheimer disease.
Lehéricy, S., Baulac, M., Jacques Chiras, C., Pierot, L., Martin-Duverneuil, N., Pillon, B., Deweer, B., Dubois, B., & Marsault, C. (1994) · PubMed Central · Cited by 308 · see citing works
Amygdala pathology in Parkinson's disease
Braak, H., Braak, E., Yilmazer‐Hanke, D., de Vos, R. A. I., Jansen, E. N. H., Böhl, J., & Jellinger, K. A. (1994) · Acta Neuropathologica · doi:10.1007/bf00296485 · Cited by 297 · see citing works
Sisodia, S., Koo, E., Hoffman, P., Perry, G. L., & Price, D. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-07-03136.1993 · Cited by 284 · see citing works
Alzheimer’s disease-related alterations in synaptic density: neocortex and hippocampus.
Scheff, S. W., & Price, D. A. (2006) · Journal of Alzheimer's Disease · doi:10.3233/jad-2006-9s312 · Cited by 284 · see citing works
“Many areas of the neocortex appear to be affected in AD and the progression appears to follow a course involving specific brain regions early in the disease process [10,11,41,75].”
Ginsberg, S. D., Alldred, M. J., Counts, S., Cataldo, A. M., Neve, R. L., Jiang, Y., Wuu, J., Chao, M. V., Mufson, E. J., Nixon, R. A., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.030 · Cited by 261 · see citing works
“Although hippocampal CA1 pyramidal neurons are particularly vulnerable to neurodegeneration during the early stages of AD (3,4), the mechanisms underlying their degeneration are poorly understood.”
Thompson, P. M., Hayashi, K. M., Dutton, R. A., Chiang, M., Leow, A., Sowell, E. R., de Zubicaray, G. I., Becker, J. T., López, O. L., Aizenstein, H. J., et al. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1379.017 · Cited by 250 · see citing works
“In contrast, NFT and neuropil threads in dendrites accumulate early in the late myelinating heteromodal association cortices, the posterior cingulate, and phylogenetically older limbic areas that remain highly plastic throughout life.41”
BackgroundMorrison, J. H., & Hof, P. R. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)36039-4 · Cited by 241 · see citing works
Hof, P., Bouras, C., Perl, D. P., Sparks, D., Mehta, N. A., & Morrison, J. H. (1995) · Archives of Neurology · doi:10.1001/archneur.1995.00540280065020 · Cited by 237 · see citing works
Therapeutic Opportunities for Muscarinic Receptors in the Central Nervous System
Felder, C. C., Bymaster, F. P., Ward, J. S., & DeLapp, N. W. (2000) · Journal of Medicinal Chemistry · doi:10.1021/jm990607u · Cited by 235 · see citing works
Francis, P. T., Sims, N. R., PROCTER, A. W., & Bowen, D. M. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb13381.x · Cited by 231 · see citing works
Hattiangady, B., Rao, M. S. R., Shetty, G. A., & Shetty, A. K. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.05.014 · Cited by 230 · see citing works
Sterniczuk, R., Antle, M. C., LaFerla, F. M., & Dyck, R. H. (2010) · Brain Research · doi:10.1016/j.brainres.2010.06.011 · Cited by 228 · see citing works
Beyreuther, K., & Masters, C. L. (1991) · Brain Pathology · doi:10.1111/j.1750-3639.1991.tb00667.x · Cited by 221 · see citing works
MRI and CSF studies in the early diagnosis of Alzheimer's disease
de Leon, M. J., DeSanti, S., Zinkowski, R. P., Mehta, P. D., Praticò, D., Segal, S., Clark, C. M., Kerkman, D. J., DeBernardis, J. F., Li, J., et al. (2004) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2004.01381.x · Cited by 221 · see citing works
Cognitive decline correlates with neuropathological stage in Parkinson's disease
Braak, H., Rüb, U., & Tredici, K. D. (2006) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2006.05.011 · Cited by 210 · see citing works
β-Amyloid and the Pathogenesis of Alzheimer's Disease
Flier, J. S., Underhill, L. H., Yankner, B. A., & Mesulam, M. M. (1991) · New England Journal of Medicine · doi:10.1056/nejm199112263252605 · Cited by 207 · see citing works
Tierney, M. C., Black, S. E., Szalai, J. P., Snow, W. G., Fisher, R. H., Nadon, G., & Chui, H. C. (2001) · Archives of Neurology · doi:10.1001/archneur.58.10.1654 · Cited by 207 · see citing works
“Following the guide provided by Jaeschke et al,21 this LR would generate a moderate change in the pretest-to-posttest probability of AD.”
BackgroundInfluentialImaging and CSF Studies in the Preclinical Diagnosis of Alzheimer's Disease
de Leon, M. J., Mosconi, L., Blennow, K., DeSanti, S., Zinkowski, R. P., Mehta, P. D., Praticò, D., Tsui, W., Louis, L. A. S., Sobanska, L., et al. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1379.012 · Cited by 198 · see citing works
Bussière, T., Giannakopoulos, P., Bouras, C., Perl, D. P., Morrison, J. H., & Hof, P. R. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10760 · Cited by 185 · see citing works
“…projections (Mutrux, 1947; Pearson et al., 1985; Rogers et al., 1985; Duyckaerts et al., 1986; Lewis et al., 1987; Morrison et al., 1987; Hyman et al., 1990; Braak and Braak, 1991; Hof et al., 1992; Bouras et al., 1993, 1994; Morrison and Hof, 1997), which can be linked to the…”
BackgroundSequestration of RNA in Alzheimer's disease neurofibrillary tangles and senile plaques
Ginsberg, S. D., Crino, P. B., Lee, V. M. ‐., Eberwine, J. H., & Trojanowski, J. Q. (1997) · Annals of Neurology · doi:10.1002/ana.410410211 · Cited by 188 · see citing works
España, J., Giménez‐Llort, L., Valero, J., Miñano-Molina, A. J., Rábano, A., Rodrı́guez-Álvarez, J., LaFerla, F. M., & Saura, C. A. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.06.015 · Cited by 184 · see citing works
Memory deficits in Alzheimer's patients: A comprehensive review
Carlesimo, G. A., & Oscar‐Berman, M. (1992) · Neuropsychology Review · doi:10.1007/bf01108841 · Cited by 184 · see citing works
Diffusion-weighted MR imaging of the hippocampus and temporal white matter in Alzheimer's disease
Hanyu, H., Sakurai, H., Iwamoto, T., Takasaki, M., Shindo, H., & Abe, K. (1998) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(98)00043-4 · Cited by 175 · see citing works
Giannakopoulos, P., Hof, P. R., Michel, J., Guimón, J., & Bouras, C. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00023-4 · Cited by 173 · see citing works
Hyman, B. T., Marzloff, K., Wenniger, J. J., Dawson, T. M., Bredt, D. S., & Snyder, S. H. (1992) · Annals of Neurology · doi:10.1002/ana.410320618 · Cited by 174 · see citing works
“It is possible that the relative sparing of NOS neurons in areas that have pronounced neuronal loss in patients with AD such as CA1 and subiculum [1-3] may lead to an imbalance of input to remaining neurons, and contribute to a cascade of events leading”
BackgroundSelf-citationCortical and striatal neurone number in Huntington's disease
Heinsen, H., Strik, M., Bauer, M., Luther, K., Ulmar, G., Gangnus, D., Jungkunz, G., Eisenmengers, W., & G�tz, M. (1994) · Acta Neuropathologica · doi:10.1007/bf00310376 · Cited by 175 · see citing works
“The pre-alpha layer exhibits massive neurofibrillary tangles in Alzheimer's disease [8, 11, 47, 63 , 93, 100], whereas the pre-beta and pri-layers are attenuated in Huntington's disease [12, 13, 57].”
BackgroundHippocampal plasticity during the progression of Alzheimer’s disease
Mufson, E. J., Mahady, L. J., Waters, D., Counts, S., Perez, S. E., DeKosky, S. T., Ginsberg, S. D., Ikonomović, M. D., Scheff, S. W., & Binder, L. I. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.03.006 · Cited by 172 · see citing works
“AD pathologic lesions and neuronal loss are found in multiple regions within the hippocampal formation as well as in the transentorhinal and entorhinal cortices (Hyman et al., 1984, 1990; Geddes, 1985; Gomez-Isla et al., 1996; Kordower et al., 2001).”
BackgroundMitochondrial involvement in Alzheimer’s disease
Bonilla, E., Tanji, K., Hirano, M., Vu, T., DiMauro, S., & Schon, E. A. (1999) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(98)00165-0 · Cited by 165 · see citing works
(1994) · PubMed Central · Cited by 169 · see citing works
Onozuka, M., Watanabe, K., MIRBOD, S. M., Ozono, S., Nishiyama, K., Karasawa, N., & Nagatsu, I. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01255-x · Cited by 167 · see citing works
Jerusalinsky, D. A., Ferreira, M. B. C., Walz, R., da Silva, R. C., Bianchin, M. M., Ruschel, A. C., Zanatta, M. S., Medina, J. H., & Izquierdo, I. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90982-a · Cited by 162 · see citing works
Simons, M., Strooper, B. D., Multhaup, G., Tienari, P. J., Dotti, C. G., & Beyreuther, K. T. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-03-00899.1996 · Cited by 161 · see citing works
Carlesimo, G. A., Piras, F., Orfei, M. D., Iorio, M., Caltagirone, C., & Spalletta, G. (2015) · Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring · doi:10.1016/j.dadm.2014.12.001 · Cited by 159 · see citing works
“[29,30], the episodic memory deficit in AD patients results from the anatomical and functional segregation of the hippocampus from associative sensory inputs due to degeneration of the perforant pathway.”
Which Memory System is Impaired First in Alzheimer's Disease?
Didic, M., Barbeau, E. J., Félician, O., Tramoni, E., Guedj, É., Poncet, M., & Ceccaldi, M. P. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-110557 · Cited by 156 · see citing works
Paola, M., Macaluso, E., Carlesimo, G. A., Tomaiuolo, F., Worsley, K. J., Fadda, L., & Caltagirone, C. (2007) · Journal of Neurology · doi:10.1007/s00415-006-0435-1 · Cited by 156 · see citing works
“All original MR images in native space were segmented into grey and white matter and CSF.”
BackgroundInfluentialAmygdalar Volume and Emotional Memory in Alzheimer’s Disease
Mori, E., Ikeda, M., Hirono, N., Kitagaki, H., Imamura, T., & Shimomura, T. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.2.216 · Cited by 154 · see citing works
Modeling the Relation Between Neurofibrillary Tangles and Intellectual Status
Duyckaerts, C. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)80306-5 · Cited by 150 · see citing works
Chapter 20 Neuropathological hallmarks of Alzheimer's and Parkinson's diseases
Braak, H., de Vos, R. A. I., Jansen, E. N. H., Bratzke, H., & Braak, E. (1998) · Progress in brain research · doi:10.1016/s0079-6123(08)64021-2 · Cited by 150 · see citing works
Temporal Lobe Atrophy on Magnetic Resonance Imaging in the Diagnosis of Early Alzheimer's Disease
Erkinjuntti, T., Lee, D. H., Gao, F., Steenhuis, R. E., Eliasziw, M., Fry, R., Merskey, H., & Hachinski, V. (1993) · Archives of Neurology · doi:10.1001/archneur.1993.00540030069017 · Cited by 148 · see citing works
D’Amelio, M., & Rossini, P. M. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.07.001 · Cited by 144 · see citing works
Clough, S., & Duff, M. C. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.00323 · Cited by 157 · see citing works
Dissociation of regional activation in mild AD during visual encoding
Kato, T., Knopman, D. S., & Liu, H. (2001) · Neurology · doi:10.1212/wnl.57.5.812 · Cited by 145 · see citing works
“the right visual association area (1), where acti-”
BackgroundInfluentialHauss‐Wegrzyniak, B., Lynch, M. A., Vraniak, P., & Wenk, G. L. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7966 · Cited by 143 · see citing works
The neuropathological diagnosis of Alzheimer's disease: clinical-pathological studies.
Hyman, B. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00066-3 · Cited by 146 · see citing works
Self-citationAGING, MILD COGNITIVE IMPAIRMENT, AND ALZHEIMER'S DISEASE
Petersen, R. C. (2000) · Neurologic Clinics · doi:10.1016/s0733-8619(05)70226-7 · Cited by 142 · see citing works
Mori, E., Yoneda, Y., Yamashita, H., Hirono, N., Ikeda, M., & Yamadori, A. (1997) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.63.2.214 · Cited by 140 · see citing works
“Neuropathological changes in Alzheimer’s disease include neurofibrillary tangles, senile plaques, and neuronal and synaptic loss and predominantly affect regions of the limbic and paralimbic medial temporal structures and association areas of the neocortex.”
BackgroundAlescio‐Lautier, B., Michel, B. F., Herrera, C. G., Ahmadi, A. E., Chambon, C., Touzet, C. F., & Paban, V. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2006.04.033 · Cited by 139 · see citing works
Bax expression in mammalian neurons undergoing apoptosis, and in Alzheimer's disease hippocampus
MacGibbon, G. A., Lawlor, P. A., Sirimanne, E. S., Walton, M. R., Connor, B. J., Young, D., Williams, C. E., Gluckman, P. D., Faull, R. L. M., Hughes, P. E., et al. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01351-0 · Cited by 140 · see citing works
Hippocampal atrophy in early Alzheimer's Disease: Anatomic specificity and validation
Convit, A., de Leon, M. D., Golomb, J., George, A., Tarshish, C., Bobinski, M., Tsui, W., Santi, S. D. D., Wegiel, J., & Wiśniewski, H. (2005) · Psychiatric quarterly · doi:10.1007/bf01064929 · Cited by 81 · see citing works
“The regional pattern of neuropathological degeneration documented in AD also correlates with the neuropsychological impairments observed (5).”
Corcoran, K. A., Lu, Y., Turner, R. S., & Maren, S. (2002) · Learning & Memory · doi:10.1101/lm.51002 · Cited by 135 · see citing works
“The anatomy of amyloid deposition in Tg2576 mice indicates that these mice might be deficient in forms of learning that depend on the hippocampus and amygdala, for example (Hyman et al. 1990).”
BackgroundResultBarros, D. M., Izquierdo, L. A., Souza, T. M. E., Ardenghi, P. G., Pereira, P., Medina, J. H., & Izquierdo, I. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00226-6 · Cited by 132 · see citing works
Volumetry of amygdala and hippocampus and memory performance in Alzheimer's disease
Basso, M. R., Yang, J., Warren, L. H., MacAvoy, M. G., Varma, P., Bronen, R. A., & van Dyck, C. H. (2006) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2006.01.007 · Cited by 132 · see citing works
“Although these findings occur in a range of brain structures, the site of earliest and most severe pathology in AD is the medial temporal lobe (Hyman et al., 1990; Braak and Braak, 1991).”
BackgroundWorking memory and apolipoprotein E: What's the connection?
Rosen, V. M. (2002) · Neuropsychologia · doi:10.1016/s0028-3932(02)00132-x · Cited by 128 · see citing works
Ginsberg, S. D., Mufson, E. J., Counts, S., Wuu, J., Alldred, M. J., Nixon, R. A., & Che, S. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-101080 · Cited by 128 · see citing works
Evolution of Alzheimer’s disease related cortical lesions
Braak, H., Braak, E., Bohl, J. R. E., & Bratzke, H. (1998) · Journal of neural transmission. Supplementum · doi:10.1007/978-3-7091-7508-8_9 · Cited by 128 · see citing works
Changes in Plasticity Across the Lifespan
Oberman, L. M., & Pascual‐Leone, Á. (2013) · Progress in brain research · doi:10.1016/b978-0-444-63327-9.00016-3 · Cited by 125 · see citing works
“The reason why memory structures are particularly vulnerable to AD and critically involved in disease progression remains unclear, though proposed theories include concepts based on anatomy (Hyman et al., 1990) and on mechanisms of plasticity (Mesulam, 2000).”
BackgroundPropagation of tau pathology in Alzheimer’s disease: identification of novel therapeutic targets
Pooler, A. M., Polydoro, M., Wegmann, S., Nicholls, S. B., Spires‐Jones, T. L., & Hyman, B. T. (2013) · Alzheimer s Research & Therapy · doi:10.1186/alzrt214 · Cited by 122 · see citing works
“The loss of NFT-affected neurons results in disconnection and deafferentation of critical neural circuits [8] and thus is likely to contribute to the defects in memory and higher-order cognitive functions in AD.”
BackgroundSelf-citationDelion, S., Chalon, S., Guilloteau, D., Lejeune, B., Besnard, J., & Durand, G. (1997) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)37235-7 · Cited by 124 · see citing works
Bussire, T., Gold, G., Kvari, E., Giannakopoulos, P., Bouras, C., Perl, D. P., Morrison, J. H., & Hof, P. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00942-9 · Cited by 122 · see citing works
Assessing neuronal networks: Understanding Alzheimer's disease
Bokde, A. L. W., Ewers, M., & Hampel, H. J. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.06.004 · Cited by 117 · see citing works
“It has been found that the projections among the hippocampal formation, entorhinal cortex, and amygdala contained NFT and the ends of the projections contained amyloid deposition (Hyman et al., 1990).”
BackgroundLife and Death of Neurons in The Aging Cerebral Cortex
Morrison, J. H., & Hof, P. R. (2007) · International review of neurobiology · doi:10.1016/s0074-7742(06)81004-4 · Cited by 120 · see citing works
Brain sites involved in fear memory reconsolidation and extinction of rodents
Baldi, E., & Bucherelli, C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.003 · Cited by 116 · see citing works
Hof, P. R. (1992) · Archives of Neurology · doi:10.1001/archneur.1992.00530330070019 · Cited by 118 · see citing works
Cognitive correlates of alterations in acetylcholinesterase in Alzheimer's disease
Bohnen, N. I., Kaufer, D., Hendrickson, R., Ivanco, L. S., Lopresti, B. J., Davis, J. G., Constantine, G. M., Mathis, C. A., Moore, R. Y., & DeKosky, S. T. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.01.031 · Cited by 117 · see citing works
- Authors
- Hyman, B. T., Hoesen, G. W. V., & Damasio, A. R.
- Affiliations
- University of Iowa (US)
- ORCID
- Hyman, B. T.
- Venue
- Neurology
- Published
- 1990-11
- Volume
- 40
- Issue
- 11
- Pages
- 1721-1721
- ISSN
- 0028-3878 (ISSN-L)
- 1526-632X
- OpenAlex
- W2160683996
- Cited by
- 449
- References
- 0
- Citations by year
- 2025: 4 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 8 · 2020: 9 · 2019: 5 · 2018: 3 · 2017: 6 · 2016: 3 · 2015: 10 · 2014: 5 · 2013: 7 · 2012: 7
- FWCI
- 16.38
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG-08487)
- National Institute of Neurological Disorders and Stroke (P0 NS 19632, R01NS014944, NS-14944)
- 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 › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- Alzheimer's disease, memory impairment, entorhinal cortex, hippocampal formation, amygdala, neurofibrillary tangles, neuritic plaques, thioflavine S
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Amygdala, Brain, Hippocampus, Humans, Immunohistochemistry, Memory, Middle Aged, Neurofibrils, Temporal Lobe
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