Interneurons in the human olfactory system in Alzheimer's disease

Experimental Neurology

Volumn 276, Issue , 2016, Pages 13-21

  Saiz Sanchez, Daniel ^a   Flores Cuadrado, Alicia ^a   Ubeda Bañon, Isabel ^a   de la Rosa Prieto, Carlos ^a   Martinez Marcos, Alino ^a  

^a University of Castilla La Mancha   (Spain)

Author keywords

Amyloid ; Archicortex; Calcium binding protein; Somatostatin; Tau

Indexed keywords

ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; CELL POPULATION; ENTORHINAL CORTEX; HUMAN; INTERNEURON; NEUROANATOMY; NEUROPATHOLOGY; NONHUMAN; OLFACTORY BULB; OLFACTORY DISCRIMINATION; OLFACTORY NUCLEUS; OLFACTORY SYSTEM; OLFACTORY TUBERCLE; PRIORITY JOURNAL; PYRIFORM CORTEX; REVIEW; CHOLINERGIC NERVE CELL; METABOLISM; ODOR; OLFACTORY RECEPTOR NEURON; PATHOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; CHOLINERGIC NEURONS; HUMANS; INTERNEURONS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SMELL;

EID: 84949035178     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.11.009     Document Type: Review

References (124)

1. Adamek G.D., Shipley M.T., Sanders M.S. The indusium griseum in the mouse: architecture, Timm's histochemistry and some afferent connections. Brain Res. Bull. 1984, 12:657-668.
2. Armstrong D.M., LeRoy S., Shields D., Terry R.D. Somatostatin-like immunoreactivity within neuritic plaques. Brain Res. 1985, 338:71-79.
3. Armstrong D.M., Benzing W.C., Evans J., Terry R.D., Shields D., Hansen L.A. Substance P and somatostatin coexist within neuritic plaques: implications for the pathogenesis of Alzheimer's disease. Neuroscience 1989, 31:663-671.
4. Arnold S.E., Lee E.B., Moberg P.J., Stutzbach L., Kazi H., Han L.Y., Lee V.M., Trojanowski J.Q. Olfactory epithelium amyloid-beta and paired helical filament-tau pathology in Alzheimer disease. Ann. Neurol. 2010, 67:462-469.
5. Attems J., Lintner F., Jellinger K.A. Olfactory involvement in aging and Alzheimer's disease: an autopsy study. J. Alzheimers Dis. 2005, 7:149-157. (discussion 173-180).
6. Attems J., Alpar A., Spence L., McParland S., Heikenwalder M., Uhlen M., Tanila H., Hokfelt T.G., Harkany T. Clusters of secretagogin-expressing neurons in the aged human olfactory tract lack terminal differentiation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6259-6264.
7. Attems J., Thomas A., Jellinger K. Correlations between cortical and subcortical tau pathology. Neuropathol. Appl. Neurobiol. 2012, 38:582-590.
8. Attems J., Walker L., Jellinger K.A. Olfactory bulb involvement in neurodegenerative diseases. Acta Neuropathol. 2014, 127:459-475.
9. Baker-Nigh A., Vahedi S., Davis E.G., Weintraub S., Bigio E.H., Klein W.L., Geula C. Neuronal amyloid-beta accumulation within cholinergic basal forebrain in ageing and Alzheimer's disease. Brain 2015.
10. Barresi M., Ciurleo R., Giacoppo S., Foti Cuzzola V., Celi D., Bramanti P., Marino S. Evaluation of olfactory dysfunction in neurodegenerative diseases. J. Neurol. Sci. 2012, 323:16-24.
11. Basso M., Yang J., Warren L., MacAvoy M.G., Varma P., Bronen R.A., van Dyck C.H. Volumetry of amygdala and hippocampus and memory performance in Alzheimer's disease. Psychiatry Res. 2006, 146:251-261.
12. Beal M.F., Mazurek M.F., Tran V.T., Chattha G., Bird E.D., Martin J.B. Reduced numbers of somatostatin receptors in the cerebral cortex in Alzheimer's disease. Science 1985, 229:289-291.
13. Beal M.F., Mazurek M.F., Svendsen C.N., Bird E.D., Martin J.B. Widespread reduction of somatostatin-like immunoreactivity in the cerebral cortex in Alzheimer's disease. Ann. Neurol. 1986, 20:489-495.
14. Bergmann O., Liebl J., Bernard S., Alkass K., Yeung M.S., Steier P., Kutschera W., Johnson L., Landen M., Druid H., Spalding K.L., Frisen J. The age of olfactory bulb neurons in humans. Neuron 2012, 74:634-639.
15. Bergmann O., Spalding K.L., Frisen J. Adult neurogenesis in humans. Cold Spring Harb. Perspect. Biol. 2015, 7:a018994.
16. Bhatnagar K.P., Kennedy R.C., Baron G., Greenberg R.A. Number of mitral cells and the bulb volume in the aging human olfactory bulb: a quantitative morphological study. Anat. Rec. 1987, 218:73-87.
17. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
18. Braak H., Braak E. Evolution of the neuropathology of Alzheimer's disease. Acta Neurol. Scand. Suppl. 1996, 165:3-12.
19. Brion J.P., Resibois A. A subset of calretinin-positive neurons are abnormal in Alzheimer's disease. Acta Neuropathol. 1994, 88:33-43.
20. Brosh I., Barkai E. Learning-induced enhancement of feedback inhibitory synaptic transmission. Learn. Mem. 2009, 16:413-416.
21. Bushdid C., Magnasco M.O., Vosshall L.B., Keller A. Humans can discriminate more than 1 trillion olfactory stimuli. Science 2014, 343:1370-1372.
22. Cai Y., Xue Z.Q., Zhang X.M., Li M.B., Wang H., Luo X.G., Cai H., Yan X.X. An age-related axon terminal pathology around the first olfactory relay that involves amyloidogenic protein overexpression without plaque formation. Neuroscience 2012, 215:160-173.
23. Candy J.M., Gascoigne A.D., Biggins J.A., Smith A.I., Perry R.H., Perry E.K., McDermott J.R., Edwardson J.A. Somatostatin immunoreactivity in cortical and some subcortical regions in Alzheimer's disease. J. Neurol. Sci. 1985, 71:315-323.
24. Capilla-Gonzalez V., Herranz-Perez V., Garcia-Verdugo J.M. The aged brain: genesis and fate of residual progenitor cells in the subventricular zone. Front. Cell. Neurosci. 2015, 9:365.
25. Cavedo E., Boccardi M., Ganzola R., Canu E., Beltramello A., Caltagirone C., Thompson P.M., Frisoni G.B. Local amygdala structural differences with 3T MRI in patients with Alzheimer disease. Neurology 2011, 76:727-733.
26. Chan-Palay V. Somatostatin immunoreactive neurons in the human hippocampus and cortex shown by immunogold/silver intensification on vibratome sections: coexistence with neuropeptide Y neurons, and effects in Alzheimer-type dementia. J. Comp. Neurol. 1987, 260:201-223.
27. Clavaguera F., Bolmont T., Crowther R.A., Abramowski D., Frank S., Probst A., Fraser G., Stalder A.K., Beibel M., Staufenbiel M., Jucker M., Goedert M., Tolnay M. Transmission and spreading of tauopathy in transgenic mouse brain. Nat. Cell Biol. 2009, 11:909-913.
28. Clavaguera F., Hench J., Goedert M., Tolnay M. Invited review: prion-like transmission and spreading of tau pathology. Neuropathol. Appl. Neurobiol. 2015, 41:47-58.
29. Conti M.Z., Vicini-Chilovi B., Riva M., Zanetti M., Liberini P., Padovani A., Rozzini L. Odor identification deficit predicts clinical conversion from mild cognitive impairment to dementia due to Alzheimer's disease. Arch. Clin. Neuropsychol. 2013, 28:391-399.
30. Curtis M.A., Kam M., Nannmark U., Anderson M.F., Axell M.Z., Wikkelso C., Holtas S., van Roon-Mom W.M., Bjork-Eriksson T., Nordborg C., Frisen J., Dragunow M., Faull R.L., Eriksson P.S. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007, 315:1243-1249.
31. Davies P., Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976, 2:1403.
32. Davies P., Terry R.D. Cortical somatostatin-like immunoreactivity in cases of Alzheimer's disease and senile dementia of the Alzheimer type. Neurobiol. Aging 1981, 2:9-14.
33. Davies P., Katzman R., Terry R.D. Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 1980, 288:279-280.
34. Devanand D.P., Michaels-Marston K.S., Liu X., Pelton G.H., Padilla M., Marder K., Bell K., Stern Y., Mayeux R. Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. Am. J. Psychiatry 2000, 157:1399-1405.
35. Devanand D.P., Lee S., Manly J., Andrews H., Schupf N., Doty R.L., Stern Y., Zahodne L.B., Louis E.D., Mayeux R. Olfactory deficits predict cognitive decline and Alzheimer dementia in an urban community. Neurology 2015, 84:182-189.
36. Doty R.L. Olfactory deficit in Alzheimer's disease?. Am. J. Psychiatry 2001, 158:1533-1534. (author reply 1534-1535).
37. Doty R.L., Shaman P., Kimmelman C.P., Dann M.S. University of Pennsylvania smell identification test: a rapid quantitative olfactory function test for the clinic. Laryngoscope 1984, 94:176-178.
38. Epelbaum J., Guillou J.L., Gastambide F., Hoyer D., Duron E., Viollet C. Somatostatin, Alzheimer's disease and cognition: an old story coming of age?. Prog. Neurobiol. 2009, 89:153-161.
39. Esiri M.M., Wilcock G.K. The olfactory bulbs in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 1984, 47:56-60.
40. Esiri M.M., Pearson R.C., Steele J.E., Bowen D.M., Powell T.P. A quantitative study of the neurofibrillary tangles and the choline acetyltransferase activity in the cerebral cortex and the amygdala in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 1990, 53:161-165.
41. Frost B., Jacks R.L., Diamond M.I. Propagation of tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 2009, 284:12845-12852.
42. Fukunaga I., Herb J.T., Kollo M., Boyden E.S., Schaefer A.T. Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb. Nat. Neurosci. 2014, 17:1208-1216.
43. Ghanbari H.A., Ghanbari K., Harris P.L., Jones P.K., Kubat Z., Castellani R.J., Wolozin B.L., Smith M.A., Perry G. Oxidative damage in cultured human olfactory neurons from Alzheimer's disease patients. Aging Cell 2004, 3:41-44.
44. Gheusi G., Lledo P.M. Adult neurogenesis in the olfactory system shapes odor memory and perception. Prog. Brain Res. 2014, 208:157-175.
45. Goedert M., Spillantini M.G. A century of Alzheimer's disease. Science 2006, 314:777-781.
46. Gschwend O., Abraham N.M., Lagier S., Begnaud F., Rodriguez I., Carleton A. Neuronal pattern separation in the olfactory bulb improves odor discrimination learning. Nat. Neurosci. 2015, 18:1474-1482.
47. Guo J.L., Lee V.M. Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nat. Med. 2014, 20:130-138.
48. Hardy J. A hundred years of Alzheimer's disease research. Neuron 2006, 52:3-13.
49. Harris J.A., Devidze N., Verret L., Ho K., Halabisky B., Thwin M.T., Kim D., Hamto P., Lo I., Yu G.Q., Palop J.J., Masliah E., Mucke L. Transsynaptic progression of amyloid-beta-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 2010, 68:428-441.
50. Hernandez F., Avila J. Tau aggregates and tau pathology. J. Alzheimers Dis. 2008, 14:449-452.
51. Hiltunen M., van Groen T., Jolkkonen J. Functional roles of amyloid-beta protein precursor and amyloid-beta peptides: evidence from experimental studies. J. Alzheimers Dis. 2009, 18:401-412.
52. Hof P.R., Cox K., Young W.G., Celio M.R., Rogers J., Morrison J.H. Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 1991, 50:451-462.
53. Howard J.D., Plailly J., Grueschow M., Haynes J.D., Gottfried J.A. Odor quality coding and categorization in human posterior piriform cortex. Nat. Neurosci. 2009, 12:932-938.
54. Iacopino A.M., Christakos S. Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:4078-4082.
55. Insausti R., Marcos P., Arroyo-Jimenez M.M., Blaizot X., Martinez-Marcos A. Comparative aspects of the olfactory portion of the entorhinal cortex and its projection to the hippocampus in rodents, nonhuman primates, and the human brain. Brain Res. Bull. 2002, 57:557-560.
56. Inta D., Cameron H.A., Gass P. New neurons in the adult striatum: from rodents to humans. Trends Neurosci. 2015, 38:517-523.
57. Kareken D.A., Doty R.L., Moberg P.J., Mosnik D., Chen S.H., Farlow M.R., Hutchins G.D. Olfactory-evoked regional cerebral blood flow in Alzheimer's disease. Neuropsychology 2001, 15:18-29.
58. Kjelvik G., Evensmoen H.R., Brezova V., Haberg A.K. The human brain representation of odor identification. J. Neurophysiol. 2012, 108:645-657.
59. Klein-Koerkamp Y., Heckemann R.A., Ramdeen K.T., Moreaud O., Keignart S., Krainik A., Hammers A., Baciu M., Hot P., Alzheimer'sdisease Neuroimaging I. Amygdalar atrophy in early Alzheimer's disease. Curr. Alzheimer Res. 2014, 11:239-252.
60. Koliatsos V.E., Kecojevic A., Troncoso J.C., Gastard M.C., Bennett D.A., Schneider J.A. Early involvement of small inhibitory cortical interneurons in Alzheimer's disease. Acta Neuropathol. 2006, 112:147-162.
61. Koss E., Weiffenbach J.M., Haxby J.V., Friedland R.P. Olfactory detection and identification performance are dissociated in early Alzheimer's disease. Neurology 1988, 38:1228-1232.
62. Kovacs T., Cairns N.J., Lantos P.L. Beta-amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in ageing and Alzheimer's disease. Neuropathol. Appl. Neurobiol. 1999, 25:481-491.
63. Kromer Vogt L.J., Hyman B.T., Van Hoesen G.W., Damasio A.R. Pathological alterations in the amygdala in Alzheimer's disease. Neuroscience 1990, 37:377-385.
64. Kunzle H. The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates. Anat. Embryol. 2004, 208:183-213.
65. Lazarini F., Gabellec M.M., Moigneu C., de Chaumont F., Olivo-Marin J.C., Lledo P.M. Adult neurogenesis restores dopaminergic neuronal loss in the olfactory bulb. J. Neurosci. 2014, 34:14430-14442.
66. Lazarov O., Lee M., Peterson D.A., Sisodia S.S. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci. 2002, 22:9785-9793.
67. Li W., Howard J.D., Gottfried J.A. Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 2010, 133:2714-2726.
68. Liu L., Drouet V., Wu J.W., Witter M.P., Small S.A., Clelland C., Duff K. Trans-synaptic spread of tau pathology in vivo. PLoS One 2012, 7.
69. Loopuijt L.D., Sebens J.B. Loss of dopamine receptors in the olfactory bulb of patients with Alzheimer's disease. Brain Res. 1990, 529:239-244.
70. Luna V.M., Schoppa N.E. GABAergic circuits control input-spike coupling in the piriform cortex. J. Neurosci. 2008, 28:8851-8859.
71. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., Wu C. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
72. Martinez-Marcos A. On the organization of olfactory and vomeronasal cortices. Prog. Neurobiol. 2009, 87:21-30.
73. Masurkar A.V., Devanand D.P. Olfactory dysfunction in the elderly: basic circuitry and alterations with normal aging and Alzheimer's disease. Curr. Geriatr. Rep. 2014, 3:91-100.
74. Mattson M.P. Calcium and neurodegeneration. Aging Cell 2007, 6:337-350.
75. Meyer-Luehmann M., Coomaraswamy J., Bolmont T., Kaeser S., Schaefer C., Kilger E., Neuenschwander A., Abramowski D., Frey P., Jaton A.L., Vigouret J.M., Paganetti P., Walsh D.M., Mathews P.M., Ghiso J., Staufenbiel M., Walker L.C., Jucker M. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 2006, 313:1781-1784.
76. Mikkonen M., Alafuzoff I., Tapiola T., Soininen H., Miettinen R. Subfield- and layer-specific changes in parvalbumin, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer's disease. Neuroscience 1999, 92:515-532.
77. Morrison J.H., Rogers J., Scherr S., Benoit R., Bloom F.E. Somatostatin immunoreactivity in neuritic plaques of Alzheimer's patients. Nature 1985, 314:90-92.
78. Mundinano I.C., Caballero M.C., Ordonez C., Hernandez M., DiCaudo C., Marcilla I., Erro M.E., Tunon M.T., Luquin M.R. Increased dopaminergic cells and protein aggregates in the olfactory bulb of patients with neurodegenerative disorders. Acta Neuropathol. 2011, 122:61-74.
79. Nath S., Agholme L., Kurudenkandy F.R., Granseth B., Marcusson J., Hallbeck M. Spreading of neurodegenerative pathology via neuron-to-neuron transmission of beta-amyloid. J. Neurosci. 2012, 32:8767-8777.
80. Nestor P.J., Scheltens P., Hodges J.R. Advances in the early detection of Alzheimer's disease. Nat. Med. 2004, 10(Suppl.):S34-S41.
81. Nussbaum J.M., Seward M.E., Bloom G.S. Alzheimer disease: a tale of two prions. Prion 2013, 7:14-19.
82. Nusser Z., Kay L.M., Laurent G., Homanics G.E., Mody I. Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J. Neurophysiol. 2001, 86:2823-2833.
83. Ohm T.G., Braak E., Probst A. Somatostatin-14-like immunoreactive neurons and fibres in the human olfactory bulb. Anat. Embryol. 1988, 179:165-171.
84. Ohm T.G., Muller H., Ulfig N., Braak E. Glutamic-acid-decarboxylase-and parvalbumin-like-immunoreactive structures in the olfactory bulb of the human adult. J. Comp. Neurol. 1990, 291:1-8.
85. Ohm T.G., Muller H., Braak E. Calbindin-D-28k-like immunoreactive structures in the olfactory bulb and anterior olfactory nucleus of the human adult: distribution and cell typology--partial complementarity with parvalbumin. Neuroscience 1991, 42:823-840.
86. Pala A., Petersen C.C. In vivo measurement of cell-type-specific synaptic connectivity and synaptic transmission in layer 2/3 mouse barrel cortex. Neuron 2015, 85:68-75.
87. Palop J.J., Mucke L. Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat. Neurosci. 2010, 13:812-818.
88. Palop J.J., Jones B., Kekonius L., Chin J., Yu G.Q., Raber J., Masliah E., Mucke L. Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9572-9577.
89. Perry E.K., Gibson P.H., Blessed G., Perry R.H., Tomlinson B.E. Neurotransmitter enzyme abnormalities in senile dementia. Choline acetyltransferase and glutamic acid decarboxylase activities in necropsy brain tissue. J. Neurol. Sci. 1977, 34:247-265.
90. Price J.L. Comparative aspects of amygdala connectivity. Ann. N. Y. Acad. Sci. 2003, 985:50-58.
91. Price J.L., Morris J.C. So what if tangles precede plaques?. Neurobiol. Aging 2004, 25:721-723. discussion 743-726.
92. Price J.L., Davis P.B., Morris J.C., White D.L. The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease. Neurobiol. Aging 1991, 12:295-312.
93. Reyes P.F., Golden G.T., Fagel P.L., Fariello R.G., Katz L., Carner E. The prepiriform cortex in dementia of the Alzheimer type. Arch. Neurol. 1987, 44:644-645.
94. Reyes P.F., Deems D.A., Suarez M.G. Olfactory-related changes in Alzheimer's disease: a quantitative neuropathologic study. Brain Res. Bull. 1993, 32:1-5.
95. Saito T., Iwata N., Tsubuki S., Takaki Y., Takano J., Huang S.M., Suemoto T., Higuchi M., Saido T.C. Somatostatin regulates brain amyloid beta peptide Abeta42 through modulation of proteolytic degradation. Nat. Med. 2005, 11:434-439.
96. Saive A.L., Royet J.P., Plailly J. A review on the neural bases of episodic odor memory: from laboratory-based to autobiographical approaches. Front. Behav. Neurosci. 2014, 8:240.
97. Saiz-Sanchez D., Ubeda-Banon I., de la Rosa-Prieto C., Argandona-Palacios L., Garcia-Munozguren S., Insausti R., Martinez-Marcos A. Somatostatin, tau, and beta-amyloid within the anterior olfactory nucleus in Alzheimer disease. Exp. Neurol. 2010, 223:347-350.
98. Saiz-Sanchez D., Ubeda-Banon I., De la Rosa-Prieto C., Martinez-Marcos A. Differential expression of interneuron populations and correlation with amyloid-beta deposition in the olfactory cortex of an AbetaPP/PS1 transgenic mouse model of Alzheimer's disease. J. Alzheimers Dis. 2012, 31:113-129.
99. Saiz-Sanchez D., De la Rosa-Prieto C., Ubeda-Banon I., Martinez-Marcos A. Interneurons, tau and amyloid-beta in the piriform cortex in Alzheimer's disease. Brain Struct. Funct. 2015, 220:2011-2025.
100. Sampson V.L., Morrison J.H., Vickers J.C. The cellular basis for the relative resistance of parvalbumin and calretinin immunoreactive neocortical neurons to the pathology of Alzheimer's disease. Exp. Neurol. 1997, 145:295-302.
101. Sanai N., Berger M.S., Garcia-Verdugo J.M., Alvarez-Buylla A. Comment on "human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension". Science 2007, 318:393. author reply 393.
102. Selden N., Geula C., Hersh L., Mesulam M.M. Human striatum: chemoarchitecture of the caudate nucleus, putamen and ventral striatum in health and Alzheimer's disease. Neuroscience 1994, 60:621-636.
103. Selden N., Mesulam M.M., Geula C. Human striatum: the distribution of neurofibrillary tangles in Alzheimer's disease. Brain Res. 1994, 648:327-331.
104. Sheng J.G., Price D.L., Koliatsos V.E. Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J. Neurosci. 2002, 22:9794-9799.
105. Simpson J., Yates C.M., Gordon A., St Clair D.M. Olfactory tubercle choline acetyltransferase activity in Alzheimer-type dementia, Down's syndrome and Huntington's chorea. J. Neurol. Neurosurg. Psychiatry 1984, 47:1138-1139.
106. Smith R.L., Baker H., Greer C.A. Immunohistochemical analyses of the human olfactory bulb. J. Comp. Neurol. 1993, 333:519-530.
107. Solodkin A., Veldhuizen S.D., Van Hoesen G.W. Contingent vulnerability of entorhinal parvalbumin-containing neurons in Alzheimer's disease. J. Neurosci. 1996, 16:3311-3321.
108. Spillantini M.G., Goedert M. Tau pathology and neurodegeneration. Lancet Neurol. 2013, 12:609-622.
109. Stamps J.J., Bartoshuk L.M., Heilman K.M. A brief olfactory test for Alzheimer's disease. J. Neurol. Sci. 2013, 333:19-24.
110. Suzuki N., Bekkers J.M. Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex. Cereb. Cortex 2010, 20:2971-2984.
111. Tabert M.H., Liu X., Doty R.L., Serby M., Zamora D., Pelton G.H., Marder K., Albers M.W., Stern Y., Devanand D.P. A 10-item smell identification scale related to risk for Alzheimer's disease. Ann. Neurol. 2005, 58:155-160.
112. ter Laak H.J., Renkawek K., van Workum F.P. The olfactory bulb in Alzheimer disease: a morphologic study of neuron loss, tangles, and senile plaques in relation to olfaction. Alzheimer Dis. Assoc. Disord. 1994, 8:38-48.
113. Thorns V., Licastro F., Masliah E. Locally reduced levels of acidic FGF lead to decreased expression of 28-kda calbindin and contribute to the selective vulnerability of the neurons in the entorhinal cortex in Alzheimer's disease. Neuropathology 2001, 21:203-211.
114. Unger J.W., Lange W. NADPH-diaphorase-positive cell populations in the human amygdala and temporal cortex: neuroanatomy, peptidergic characteristics and aspects of aging and Alzheimer's disease. Acta Neuropathol. 1992, 83:636-646.
115. van de Nes J.A., Sandmann-Keil D., Braak H. Interstitial cells subjacent to the entorhinal region expressing somatostatin-28 immunoreactivity are susceptible to development of Alzheimer's disease-related cytoskeletal changes. Acta Neuropathol. 2002, 104:351-356.
116. Vasavada M.M., Wang J., Eslinger P.J., Gill D.J., Sun X., Karunanayaka P., Yang Q.X. Olfactory cortex degeneration in Alzheimer's disease and mild cognitive impairment. J. Alzheimers Dis. 2015, 45:947-958.
117. Verret L., Mann E.O., Hang G.B., Barth A.M., Cobos I., Ho K., Devidze N., Masliah E., Kreitzer A.C., Mody I., Mucke L., Palop J.J. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 2012, 149:708-721.
118. Wang J., Eslinger P.J., Doty R.L., Zimmerman E.K., Grunfeld R., Sun X., Meadowcroft M.D., Connor J.R., Price J.L., Smith M.B., Yang Q.X. Olfactory deficit detected by fMRI in early Alzheimer's disease. Brain Res. 2010, 1357:184-194.
119. Wesson D.W., Borkowski A.H., Landreth G.E., Nixon R.A., Levy E., Wilson D.A. Sensory network dysfunction, behavioral impairments, and their reversibility in an Alzheimer's beta-amyloidosis mouse model. J. Neurosci. 2011, 31:15962-15971.
120. Westervelt H.J., Bruce J.M., Coon W.G., Tremont G. Odor identification in mild cognitive impairment subtypes. J. Clin. Exp. Neuropsychol. 2008, 30:151-156.
121. Winner B., Winkler J. Adult neurogenesis in neurodegenerative diseases. Cold Spring Harb. Perspect. Biol. 2015, 7.
122. Witter M.P. The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog. Brain Res. 2007, 163:43-61.
123. Wolff S.B., Grundemann J., Tovote P., Krabbe S., Jacobson G.A., Muller C., Herry C., Ehrlich I., Friedrich R.W., Letzkus J.J., Luthi A. Amygdala interneuron subtypes control fear learning through disinhibition. Nature 2014, 509:453-458.
124. Zelano C., Sobel N. Humans as an animal model for systems-level organization of olfaction. Neuron 2005, 48:431-454.