Early and selective localization of tau filaments to glutamatergic subcellular domains within the human anterodorsal thalamus.
Humans
tau Proteins
/ metabolism
Female
Male
Aged
Aged, 80 and over
Alzheimer Disease
/ pathology
Middle Aged
Neurons
/ metabolism
Vesicular Glutamate Transport Protein 2
/ metabolism
Glutamic Acid
/ metabolism
Anterior Thalamic Nuclei
/ metabolism
Calbindin 2
/ metabolism
Neurofibrillary Tangles
/ pathology
Presynaptic Terminals
/ metabolism
Alzheimer’s disease
Paired helical filaments
Tau
Thalamus
vGLUT2
Journal
Acta neuropathologica
ISSN: 1432-0533
Titre abrégé: Acta Neuropathol
Pays: Germany
ID NLM: 0412041
Informations de publication
Date de publication:
11 Jun 2024
11 Jun 2024
Historique:
received:
12
01
2024
accepted:
01
06
2024
revised:
21
05
2024
medline:
11
6
2024
pubmed:
11
6
2024
entrez:
11
6
2024
Statut:
epublish
Résumé
Widespread cortical accumulation of misfolded pathological tau proteins (ptau) in the form of paired helical filaments is a major hallmark of Alzheimer's disease. Subcellular localization of ptau at various stages of disease progression is likely to be informative of the cellular mechanisms involving its spread. Here, we found that the density of ptau within several distinct rostral thalamic nuclei in post-mortem human tissue (n = 25 cases) increased with the disease stage, with the anterodorsal nucleus (ADn) consistently being the most affected. In the ADn, ptau-positive elements were present already in the pre-cortical (Braak 0) stage. Tau pathology preferentially affected the calretinin-expressing subpopulation of glutamatergic neurons in the ADn. At the subcellular level, we detected ptau immunoreactivity in ADn cell bodies, dendrites, and in a specialized type of presynaptic terminal that expresses vesicular glutamate transporter 2 (vGLUT2) and likely originates from the mammillary body. The ptau-containing terminals displayed signs of degeneration, including endosomal/lysosomal organelles. In contrast, corticothalamic axon terminals lacked ptau. The data demonstrate the involvement of a specific cell population in ADn at the onset of the disease. The presence of ptau in subcortical glutamatergic presynaptic terminals supports hypotheses about the transsynaptic spread of tau selectively affecting specialized axonal pathways.
Identifiants
pubmed: 38861157
doi: 10.1007/s00401-024-02749-3
pii: 10.1007/s00401-024-02749-3
doi:
Substances chimiques
tau Proteins
0
Vesicular Glutamate Transport Protein 2
0
Glutamic Acid
3KX376GY7L
Calbindin 2
0
MAPT protein, human
0
CALB2 protein, human
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
98Subventions
Organisme : Alzheimer Society
ID : 522 AS-PhD-19a-010
Organisme : Medical Research Council
ID : MR/R011567/1
Pays : United Kingdom
Organisme : H2020 European Research Council
ID : FRONTHAL 742595
Organisme : H2020 European Research Council
ID : INHIBITHUMAN 694988
Organisme : "Lendület" Program
ID : LP2023-2/2023
Organisme : European Union project, Artificial Intelligence National Laboratory
ID : RRF-2.3.1-21-2022-00004
Organisme : John Fell Fund, University of Oxford
ID : 0007192
Organisme : Nuffield Benefaction for Medicine and the Wellcome Institutional Strategic Support Fund
ID : 0009985
Organisme : Nemzeti Kutatási, Fejlesztési és Innovaciós Alap
ID : NKFIH_SNN_132999
Informations de copyright
© 2024. Crown.
Références
Acsády L (2022) Organization of thalamic inputs. In: Halassa MM (ed) The thalamus. Cambridge University Press, Cambridge, pp 27–44
doi: 10.1017/9781108674287.003
Aggleton JP, O’Mara SM (2022) The anterior thalamic nuclei: core components of a tripartite episodic memory system. Nat Rev Neurosci 23:505–516. https://doi.org/10.1038/s41583-022-00591-8
doi: 10.1038/s41583-022-00591-8
pubmed: 35478245
Aggleton JP, Pralus A, Nelson AJ, Hornberger M (2016) Thalamic pathology and memory loss in early Alzheimer’s disease: moving the focus from the medial temporal lobe to Papez circuit. Brain 139:1877–1890. https://doi.org/10.1093/brain/aww083
doi: 10.1093/brain/aww083
pubmed: 27190025
pmcid: 4939698
Ahmed Z, Cooper J, Murray TK, Garn K, McNaughton E, Clarke H et al (2014) A novel in vivo model of tau propagation with rapid and progressive neurofibrillary tangle pathology: the pattern of spread is determined by connectivity, not proximity. Acta Neuropathol 127:667–683. https://doi.org/10.1007/s00401-014-1254-6
doi: 10.1007/s00401-014-1254-6
pubmed: 24531916
pmcid: 4252866
Allison SL, Fagan AM, Morris JC, Head D (2016) Spatial navigation in preclinical Alzheimer’s disease. J Alzheimers Dis 52:77–90. https://doi.org/10.3233/JAD-150855
doi: 10.3233/JAD-150855
pubmed: 26967209
pmcid: 5091813
Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51–86. https://doi.org/10.1002/cne.901950106
doi: 10.1002/cne.901950106
pubmed: 7204652
Andres-Benito P, Fernandez-Duenas V, Carmona M, Escobar LA, Torrejon-Escribano B, Aso E et al (2017) Locus coeruleus at asymptomatic early and middle Braak stages of neurofibrillary tangle pathology. Neuropathol Appl Neurobiol 43:373–392. https://doi.org/10.1111/nan.12386
doi: 10.1111/nan.12386
pubmed: 28117912
Arima K (2007) Tubular profile of the Gallyas- and tau-positive argyrophilic threads in corticobasal degeneration: an electronmicroscopic study. Neuropathology 16:65–70. https://doi.org/10.1111/j.1440-1789.1996.tb00157.x
doi: 10.1111/j.1440-1789.1996.tb00157.x
Arima K (2006) Ultrastructural characteristics of tau filaments in tauopathies: immuno-electron microscopic demonstration of tau filaments in tauopathies. Neuropathology 26:475–483. https://doi.org/10.1111/j.1440-1789.2006.00669.x
doi: 10.1111/j.1440-1789.2006.00669.x
pubmed: 17080728
Arima K, Izumiyama Y, Nakamura M, Nakayama H, Kimura M, Ando S et al (1998) Argyrophilic tau-positive twisted and non-twisted tubules in astrocytic processes in brains of Alzheimer-type dementia: an electron microscopical study. Acta Neuropathol 95:28–39. https://doi.org/10.1007/s004010050762
doi: 10.1007/s004010050762
pubmed: 9452819
Arima K, Nakamura M, Sunohara N, Nishio T, Ogawa M, Hirai S et al (1999) Immunohistochemical and ultrastructural characterization of neuritic clusters around ghost tangles in the hippocampal formation in progressive supranuclear palsy brains. Acta Neuropathol 97:565–576. https://doi.org/10.1007/s004010051032
doi: 10.1007/s004010051032
pubmed: 10378375
Backman L, Small BJ, Fratiglioni L (2001) Stability of the preclinical episodic memory deficit in Alzheimer’s disease. Brain 124:96–102. https://doi.org/10.1093/brain/124.1.96
doi: 10.1093/brain/124.1.96
pubmed: 11133790
Beaudet A, Descarries L (1978) The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience 3:851–860. https://doi.org/10.1016/0306-4522(78)90115-x
doi: 10.1016/0306-4522(78)90115-x
pubmed: 215936
Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112:389–404. https://doi.org/10.1007/s00401-006-0127-z
doi: 10.1007/s00401-006-0127-z
pubmed: 16906426
pmcid: 3906709
Braak H, Braak E (1991) Alzheimer’s disease affects limbic nuclei of the thalamus. Acta Neuropathol 81:261–268. https://doi.org/10.1007/BF00305867
doi: 10.1007/BF00305867
pubmed: 1711755
Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259. https://doi.org/10.1007/BF00308809
doi: 10.1007/BF00308809
pubmed: 1759558
Braak H, Del Tredici K (2011) The pathological process underlying Alzheimer’s disease in individuals under thirty. Acta Neuropathol 121:171–181. https://doi.org/10.1007/s00401-010-0789-4
doi: 10.1007/s00401-010-0789-4
pubmed: 21170538
Braak H, Del Tredici K (2016) Potential pathways of abnormal tau and alpha-synuclein dissemination in sporadic Alzheimer’s and Parkinson’s diseases. Cold Spring Harb Perspect Biol 8:a023630. https://doi.org/10.1101/cshperspect.a023630
doi: 10.1101/cshperspect.a023630
pubmed: 27580631
pmcid: 5088528
Braak H, Thal DR, Ghebremedhin E, Del Tredici K (2011) Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100 years. J Neuropathol Exp Neurol 70:960–969. https://doi.org/10.1097/NEN.0b013e318232a379
doi: 10.1097/NEN.0b013e318232a379
pubmed: 22002422
Clavaguera F, Akatsu H, Fraser G, Crowther RA, Frank S, Hench J et al (2013) Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci USA 110:9535–9540. https://doi.org/10.1073/pnas.1301175110
doi: 10.1073/pnas.1301175110
pubmed: 23690619
pmcid: 3677441
Clavaguera F, Hench J, Goedert M, Tolnay M (2015) Invited review: prion-like transmission and spreading of tau pathology. Neuropathol Appl Neurobiol 41:47–58. https://doi.org/10.1111/nan.12197
doi: 10.1111/nan.12197
pubmed: 25399729
Colmant L, Boyer E, Gérard T, Bierbrauer A, Kunz L, Sleegers K et al (2023) Path integration deficits related to Alzheimer’s disease pathology in clinically normal older adults. Alzheimers Dement 19:e078924. https://doi.org/10.1002/alz.078924
doi: 10.1002/alz.078924
Colom-Cadena M, Davies C, Sirisi S, Lee JE, Simzer EM, Tzioras M et al (2023) Synaptic oligomeric tau in Alzheimer’s disease—a potential culprit in the spread of tau pathology through the brain. Neuron 111(2170–2183):e2176. https://doi.org/10.1016/j.neuron.2023.04.020
doi: 10.1016/j.neuron.2023.04.020
Colonnier M (1964) Experimental degeneration in the cerebral cortex. J Anat 98:47–53
pubmed: 14109813
pmcid: 1261310
Coughlan G, Laczo J, Hort J, Minihane AM, Hornberger M (2018) Spatial navigation deficits—overlooked cognitive marker for preclinical Alzheimer disease? Nat Rev Neurol 14:496–506. https://doi.org/10.1038/s41582-018-0031-x
doi: 10.1038/s41582-018-0031-x
pubmed: 29980763
Crotti A, Sait HR, McAvoy KM, Estrada K, Ergun A, Szak S et al (2019) BIN1 favors the spreading of Tau via extracellular vesicles. Sci Rep 9:9477. https://doi.org/10.1038/s41598-019-45676-0
doi: 10.1038/s41598-019-45676-0
pubmed: 31263146
pmcid: 6603165
Delpech JC, Pathak D, Varghese M, Kalavai SV, Hays EC, Hof PR et al (2021) Wolframin-1-expressing neurons in the entorhinal cortex propagate tau to CA1 neurons and impair hippocampal memory in mice. Sci Transl Med 13:eabe8455. https://doi.org/10.1126/scitranslmed.abe8455
doi: 10.1126/scitranslmed.abe8455
pubmed: 34524859
pmcid: 8763211
DeVos SL, Corjuc BT, Oakley DH, Nobuhara CK, Bannon RN, Chase A et al (2018) Synaptic tau seeding precedes tau pathology in human Alzheimer’s disease Brain. Front Neurosci 12:267. https://doi.org/10.3389/fnins.2018.00267
doi: 10.3389/fnins.2018.00267
pubmed: 29740275
pmcid: 5928393
Ehrenberg AJ, Nguy AK, Theofilas P, Dunlop S, Suemoto CK, Di Lorenzo Alho AT et al (2017) Quantifying the accretion of hyperphosphorylated tau in the locus coeruleus and dorsal raphe nucleus: the pathological building blocks of early Alzheimer’s disease. Neuropathol Appl Neurobiol 43:393–408. https://doi.org/10.1111/nan.12387
doi: 10.1111/nan.12387
pubmed: 28117917
pmcid: 5642282
Forno G, Llado A, Hornberger M (2021) Going round in circles—the Papez circuit in Alzheimer’s disease. Eur J Neurosci 54:7668–7687. https://doi.org/10.1111/ejn.15494
doi: 10.1111/ejn.15494
pubmed: 34656073
Fortin M, Asselin MC, Gould PV, Parent A (1998) Calretinin-immunoreactive neurons in the human thalamus. Neuroscience 84:537–548. https://doi.org/10.1016/s0306-4522(97)00486-7
doi: 10.1016/s0306-4522(97)00486-7
pubmed: 9539224
Frost BE, Martin SK, Cafalchio M, Islam MN, Aggleton JP, O’Mara SM (2021) Anterior thalamic inputs are required for subiculum spatial coding, with associated consequences for hippocampal spatial memory. J Neurosci 41:6511–6525. https://doi.org/10.1523/JNEUROSCI.2868-20.2021
doi: 10.1523/JNEUROSCI.2868-20.2021
pubmed: 34131030
pmcid: 8318085
Gilvesy A, Husen E, Magloczky Z, Mihaly O, Hortobagyi T, Kanatani S et al (2022) Spatiotemporal characterization of cellular tau pathology in the human locus coeruleus-pericoerulear complex by three-dimensional imaging. Acta Neuropathol 144:651–676. https://doi.org/10.1007/s00401-022-02477-6
doi: 10.1007/s00401-022-02477-6
pubmed: 36040521
pmcid: 9468059
Goedert M, Jakes R, Vanmechelen E (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 189:167–169. https://doi.org/10.1016/0304-3940(95)11484-e
doi: 10.1016/0304-3940(95)11484-e
pubmed: 7624036
Guison NG, Ahmed AK, Dong K, Yamadori T (1995) Projections from the lateral mammillary nucleus to the anterodorsal thalamic nucleus in the rat. Kobe J Med Sci 41:213–220
pubmed: 8869007
Harding A, Halliday G, Caine D, Kril J (2000) Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. Brain 123(Pt 1):141–154. https://doi.org/10.1093/brain/123.1.141
doi: 10.1093/brain/123.1.141
pubmed: 10611128
Hayakawa T, Zyo K (1989) Retrograde double-labeling study of the mammillothalamic and the mammillotegmental projections in the rat. J Comp Neurol 284:1–11. https://doi.org/10.1002/cne.902840102
doi: 10.1002/cne.902840102
pubmed: 2502564
Hort J, Laczo J, Vyhnalek M, Bojar M, Bures J, Vlcek K (2007) Spatial navigation deficit in amnestic mild cognitive impairment. Proc Natl Acad Sci USA 104:4042–4047. https://doi.org/10.1073/pnas.0611314104
doi: 10.1073/pnas.0611314104
pubmed: 17360474
pmcid: 1820705
Iba M, McBride JD, Guo JL, Zhang B, Trojanowski JQ, Lee VM (2015) Tau pathology spread in PS19 tau transgenic mice following locus coeruleus (LC) injections of synthetic tau fibrils is determined by the LC’s afferent and efferent connections. Acta Neuropathol 130:349–362. https://doi.org/10.1007/s00401-015-1458-4
doi: 10.1007/s00401-015-1458-4
pubmed: 26150341
pmcid: 4545685
Ishizawa T, Ko LW, Cookson N, Davias P, Espinoza M, Dickson DW (2002) Selective neurofibrillary degeneration of the hippocampal CA2 sector is associated with four-repeat tauopathies. J Neuropathol Exp Neurol 61:1040–1047. https://doi.org/10.1093/jnen/61.12.1040
doi: 10.1093/jnen/61.12.1040
pubmed: 12484566
Jones EG (1998) Viewpoint: the core and matrix of thalamic organization. Neuroscience 85:331–345. https://doi.org/10.1016/s0306-4522(97)00581-2
doi: 10.1016/s0306-4522(97)00581-2
pubmed: 9622234
Kaitz SS, Robertson RT (1981) Thalamic connections with limbic cortex. II. Corticothalamic projections. J Comp Neurol 195:527–545. https://doi.org/10.1002/cne.901950309
doi: 10.1002/cne.901950309
pubmed: 7204660
Kalia LV, Lang AE (2015) Parkinson’s disease. Lancet 386:896–912. https://doi.org/10.1016/S0140-6736(14)61393-3
doi: 10.1016/S0140-6736(14)61393-3
pubmed: 25904081
Kidd M (1964) Alzheimer’s disease—an electron microscopical study. Brain 87:307–320. https://doi.org/10.1093/brain/87.2.307
doi: 10.1093/brain/87.2.307
pubmed: 14188276
Kidd M (1963) Paired helical filaments in electron microscopy of Alzheimer’s disease. Nature 197:192–193. https://doi.org/10.1038/197192b0
doi: 10.1038/197192b0
pubmed: 14032480
Kovacs GG, Ferrer I, Grinberg LT, Alafuzoff I, Attems J, Budka H et al (2016) Aging-related tau astrogliopathy (ARTAG): harmonized evaluation strategy. Acta Neuropathol 131:87–102. https://doi.org/10.1007/s00401-015-1509-x
doi: 10.1007/s00401-015-1509-x
pubmed: 26659578
Laurens J, Kim B, Dickman JD, Angelaki DE (2016) Gravity orientation tuning in macaque anterior thalamus. Nat Neurosci 19:1566–1568. https://doi.org/10.1038/nn.4423
doi: 10.1038/nn.4423
pubmed: 27775722
pmcid: 5791896
Liu L, Drouet V, Wu JW, Witter MP, Small SA, Clelland C et al (2012) Trans-synaptic spread of tau pathology in vivo. PLoS ONE 7:e31302. https://doi.org/10.1371/journal.pone.0031302
doi: 10.1371/journal.pone.0031302
pubmed: 22312444
pmcid: 3270029
Masliah E, Hansen L, Albright T, Mallory M, Terry RD (1991) Immunoelectron microscopic study of synaptic pathology in Alzheimer’s disease. Acta Neuropathol 81:428–433. https://doi.org/10.1007/BF00293464
doi: 10.1007/BF00293464
pubmed: 1903014
Mitchell AS, Dalrymple-Alford JC (2006) Lateral and anterior thalamic lesions impair independent memory systems. Learn Mem 13:388–396. https://doi.org/10.1101/lm.122206
doi: 10.1101/lm.122206
pubmed: 16741289
pmcid: 1475822
Mizoguchi A, Nakanishi H, Kimura K, Matsubara K, Ozaki-Kuroda K, Katata T et al (2002) Nectin: an adhesion molecule involved in formation of synapses. J Cell Biol 156:555–565. https://doi.org/10.1083/jcb.200103113
doi: 10.1083/jcb.200103113
pubmed: 11827984
pmcid: 2173327
Munkle MC, Waldvogel HJ, Faull RL (2000) The distribution of calbindin, calretinin and parvalbumin immunoreactivity in the human thalamus. J Chem Neuroanat 19:155–173. https://doi.org/10.1016/s0891-0618(00)00060-0
doi: 10.1016/s0891-0618(00)00060-0
pubmed: 10989260
Nakano I, Iwatsubo T, Otsuka N, Kamei M, Matsumura K, Mannen T (1992) Paired helical filaments in astrocytes: electron microscopy and immunohistochemistry in a case of atypical Alzheimer’s disease. Acta Neuropathol 83:228–232. https://doi.org/10.1007/BF00296783
doi: 10.1007/BF00296783
pubmed: 1557954
Nehra G, Bauer B, Hartz AMS (2022) Blood-brain barrier leakage in Alzheimer’s disease: from discovery to clinical relevance. Pharmacol Ther 234:108119. https://doi.org/10.1016/j.pharmthera.2022.108119
doi: 10.1016/j.pharmthera.2022.108119
pubmed: 35108575
pmcid: 9107516
Nishimura M, Tomimoto H, Suenaga T, Namba Y, Ikeda K, Akiguchi I et al (1995) Immunocytochemical characterization of glial fibrillary tangles in Alzheimer’s disease brain. Am J Pathol 146:1052–1058
pubmed: 7747799
pmcid: 1869277
Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A et al (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 64:113–122. https://doi.org/10.1093/jnen/64.2.113
doi: 10.1093/jnen/64.2.113
pubmed: 15751225
Perry BAL, Mercer SA, Barnett SC, Lee J, Dalrymple-Alford JC (2018) Anterior thalamic nuclei lesions have a greater impact than mammillothalamic tract lesions on the extended hippocampal system. Hippocampus 28:121–135. https://doi.org/10.1002/hipo.22815
doi: 10.1002/hipo.22815
pubmed: 29150979
Petrof I, Sherman SM (2009) Synaptic properties of the mammillary and cortical afferents to the anterodorsal thalamic nucleus in the mouse. J Neurosci 29:7815–7819. https://doi.org/10.1523/JNEUROSCI.1564-09.2009
doi: 10.1523/JNEUROSCI.1564-09.2009
pubmed: 19535593
pmcid: 2739449
Rovo Z, Ulbert I, Acsady L (2012) Drivers of the primate thalamus. J Neurosci 32:17894–17908. https://doi.org/10.1523/JNEUROSCI.2815-12.2012
doi: 10.1523/JNEUROSCI.2815-12.2012
pubmed: 23223308
pmcid: 3672843
Roy DS, Zhang Y, Aida T, Choi S, Chen Q, Hou Y et al (2021) Anterior thalamic dysfunction underlies cognitive deficits in a subset of neuropsychiatric disease models. Neuron 109(2590–2603):e2513. https://doi.org/10.1016/j.neuron.2021.06.005
doi: 10.1016/j.neuron.2021.06.005
Rub U, Stratmann K, Heinsen H, Del Turco D, Ghebremedhin E, Seidel K et al (2016) Hierarchical distribution of the tau cytoskeletal pathology in the thalamus of Alzheimer’s disease patients. J Alzheimers Dis 49:905–915. https://doi.org/10.3233/JAD-150639
doi: 10.3233/JAD-150639
pubmed: 26519431
Saunders RC, Mishkin M, Aggleton JP (2005) Projections from the entorhinal cortex, perirhinal cortex, presubiculum, and parasubiculum to the medial thalamus in macaque monkeys: identifying different pathways using disconnection techniques. Exp Brain Res 167:1–16. https://doi.org/10.1007/s00221-005-2361-3
doi: 10.1007/s00221-005-2361-3
pubmed: 16143859
Schultz C, Ghebremedhin E, Del Tredici K, Rub U, Braak H (2004) High prevalence of thorn-shaped astrocytes in the aged human medial temporal lobe. Neurobiol Aging 25:397–405. https://doi.org/10.1016/S0197-4580(03)00113-1
doi: 10.1016/S0197-4580(03)00113-1
pubmed: 15123344
Sherman SM, Guillery RW (2009) The afferent axons to the thalamus. Exploring the thalamus and its role in cortical function. The MIT Press, Cambridge
Shibata H (1993) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol 337:431–445. https://doi.org/10.1002/cne.903370307
doi: 10.1002/cne.903370307
pubmed: 7506716
Shibata H (1993) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330:533–542. https://doi.org/10.1002/cne.903300409
doi: 10.1002/cne.903300409
pubmed: 8320343
Simon D, Garcia-Garcia E, Royo F, Falcon-Perez JM, Avila J (2012) Proteostasis of tau. Tau overexpression results in its secretion via membrane vesicles. FEBS Lett 586:47–54. https://doi.org/10.1016/j.febslet.2011.11.022
doi: 10.1016/j.febslet.2011.11.022
pubmed: 22138183
Somogyi G, Hajdu F, Tombol T (1978) Ultrastructure of the anterior ventral and anterior medial nuclei of the cat thalamus. Exp Brain Res 31:417–431. https://doi.org/10.1007/BF00237299
doi: 10.1007/BF00237299
pubmed: 648606
Stratmann K, Heinsen H, Korf HW, Del Turco D, Ghebremedhin E, Seidel K et al (2016) Precortical phase of Alzheimer’s disease (AD)-related tau cytoskeletal pathology. Brain Pathol 26:371–386. https://doi.org/10.1111/bpa.12289
doi: 10.1111/bpa.12289
pubmed: 26193084
Swaddiwudhipong N, Whiteside DJ, Hezemans FH, Street D, Rowe JB, Rittman T (2023) Pre-diagnostic cognitive and functional impairment in multiple sporadic neurodegenerative diseases. Alzheimers Dement 19:1752–1763. https://doi.org/10.1002/alz.12802
doi: 10.1002/alz.12802
pubmed: 36223793
Szentagothai J, Hamori J, Tombol T (1966) Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Exp Brain Res 2:283–301. https://doi.org/10.1007/BF00234775
doi: 10.1007/BF00234775
pubmed: 5957903
Tai HC, Serrano-Pozo A, Hashimoto T, Frosch MP, Spires-Jones TL, Hyman BT (2012) The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. Am J Pathol 181:1426–1435. https://doi.org/10.1016/j.ajpath.2012.06.033
doi: 10.1016/j.ajpath.2012.06.033
pubmed: 22867711
pmcid: 3463637
Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86. https://doi.org/10.1523/JNEUROSCI.15-01-00070.1995
doi: 10.1523/JNEUROSCI.15-01-00070.1995
pubmed: 7823153
pmcid: 6578288
Terry RD, Gonatas NK, Weiss M (1964) Ultrastructural studies in Alzheimer’s presenile dementia. Am J Pathol 44:269–297
pubmed: 14119171
pmcid: 1906996
Theofilas P, Ehrenberg AJ, Nguy A, Thackrey JM, Dunlop S, Mejia MB et al (2018) Probing the correlation of neuronal loss, neurofibrillary tangles, and cell death markers across the Alzheimer’s disease Braak stages: a quantitative study in humans. Neurobiol Aging 61:1–12. https://doi.org/10.1016/j.neurobiolaging.2017.09.007
doi: 10.1016/j.neurobiolaging.2017.09.007
pubmed: 29031088
Tourtellotte WG, Van Hoesen GW, Hyman BT, Tikoo RK, Damasio AR (1990) Alz-50 immunoreactivity in the thalamic reticular nucleus in Alzheimer’s disease. Brain Res 515:227–234. https://doi.org/10.1016/0006-8993(90)90600-g
doi: 10.1016/0006-8993(90)90600-g
pubmed: 2357561
Tracy TE, Madero-Perez J, Swaney DL, Chang TS, Moritz M, Konrad C et al (2022) Tau interactome maps synaptic and mitochondrial processes associated with neurodegeneration. Cell 185(712–728):e714. https://doi.org/10.1016/j.cell.2021.12.041
doi: 10.1016/j.cell.2021.12.041
Van der Werf YD, Witter MP, Uylings HB, Jolles J (2000) Neuropsychology of infarctions in the thalamus: a review. Neuropsychologia 38:613–627. https://doi.org/10.1016/s0028-3932(99)00104-9
doi: 10.1016/s0028-3932(99)00104-9
pubmed: 10689038
van Groen T, Kadish I, Michael Wyss J (2002) Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat. Behav Brain Res 132:19–28. https://doi.org/10.1016/s0166-4328(01)00390-4
doi: 10.1016/s0166-4328(01)00390-4
pubmed: 11853854
Veazey RB, Amaral DG, Cowan WM (1982) The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). II. Efferent connections. J Comp Neurol 207:135–156. https://doi.org/10.1002/cne.902070204
doi: 10.1002/cne.902070204
pubmed: 6808031
Viney TJ, Sarkany B, Ozdemir AT, Hartwich K, Schweimer J, Bannerman D et al (2022) Spread of pathological human Tau from neurons to oligodendrocytes and loss of high-firing pyramidal neurons in aging mice. Cell Rep 41:111646. https://doi.org/10.1016/j.celrep.2022.111646
doi: 10.1016/j.celrep.2022.111646
pubmed: 36384116
pmcid: 9681663
Walker JM, Richardson TE, Farrell K, Iida MA, Foong C, Shang P et al (2021) Early selective vulnerability of the CA2 hippocampal subfield in primary age-related tauopathy. J Neuropathol Exp Neurol 80:102–111. https://doi.org/10.1093/jnen/nlaa153
doi: 10.1093/jnen/nlaa153
pubmed: 33367843
pmcid: 8453611
Wilton LA, Baird AL, Muir JL, Honey RC, Aggleton JP (2001) Loss of the thalamic nuclei for “head direction” impairs performance on spatial memory tasks in rats. Behav Neurosci 115:861–869
doi: 10.1037/0735-7044.115.4.861
pubmed: 11508725
Wu JW, Hussaini SA, Bastille IM, Rodriguez GA, Mrejeru A, Rilett K et al (2016) Neuronal activity enhances tau propagation and tau pathology in vivo. Nat Neurosci 19:1085–1092. https://doi.org/10.1038/nn.4328
doi: 10.1038/nn.4328
pubmed: 27322420
pmcid: 4961585
Xuereb JH, Perry RH, Candy JM, Perry EK, Marshall E, Bonham JR (1991) Nerve cell loss in the thalamus in Alzheimer’s disease and Parkinson’s disease. Brain 114(Pt 3):1363–1379
pubmed: 2065255
Yamada K, Holth JK, Liao F, Stewart FR, Mahan TE, Jiang H et al (2014) Neuronal activity regulates extracellular tau in vivo. J Exp Med 211:387–393. https://doi.org/10.1084/jem.20131685
doi: 10.1084/jem.20131685
pubmed: 24534188
pmcid: 3949564
Yamada T, McGeer PL (1990) Oligodendroglial microtubular masses: an abnormality observed in some human neurodegenerative diseases. Neurosci Lett 120:163–166. https://doi.org/10.1016/0304-3940(90)90028-8
doi: 10.1016/0304-3940(90)90028-8
pubmed: 2293103