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01-07-2015 | Original Article

Interneurons, tau and amyloid-β in the piriform cortex in Alzheimer’s disease

Authors: Daniel Saiz-Sanchez, Carlos De la Rosa-Prieto, Isabel Ubeda-Banon, Alino Martinez-Marcos

Published in: Brain Structure and Function | Issue 4/2015

Abstract

Impaired olfaction has been described as an early symptom of Alzheimer’s disease. Neuroanatomical changes underlying this deficit in the olfactory system are largely unknown. Interestingly, neuropathology begins in the transentorhinal cortex and extends to the neighboring limbic system and basal telencephalic structures that mediate olfactory processing, including the anterior olfactory nucleus and olfactory bulb. The human piriform cortex has been described as a crucial area in odor quality coding; disruption of this region mediates early olfactory deficits in Alzheimer’s disease. Most neuropathological investigations have focused on the entorhinal cortex and hippocampus, whereas the piriform cortex has largely been neglected. This work aims to characterize the expression of the neuropathological amyloid-β peptide, tau protein and interneuron population markers (calretinin, parvalbumin and somatostatin) in the piriform cortex of ten Alzheimer-diagnosed (80.4 ± 8.3 years old) and five control (69.6 ± 11.1) cases. Here, we examined the distribution of different interneuronal markers as well as co-localization of interneurons and pathological markers. Results indicated preferential vulnerability of somatostatin- (p = 0.0001 < α = 0.05) and calretinin-positive (p = 0.013 < α = 0.05) cells that colocalized with amyloid-β peptide, while the prevalence of parvalbumin-positive cells was increased (p = 0.045 < α = 0.05) in the Alzheimer’s cases. These data may help to reveal the neural basis of olfactory deficits linked to Alzheimer’s disease as well as to characterize neuronal populations preferentially vulnerable to neuropathology in regions critically involved in early stages of the disease.

Arzi A, Sobel N (2011) Olfactory perception as a compass for olfactory neural maps. Trends Cogn Sci 15:537–545. doi:10.1016/j.tics.2011.09.007 PubMed

Attems J, Lintner F, Jellinger KA (2005) Olfactory involvement in aging and Alzheimer’s disease: an autopsy study. J Alzheimers Dis 7:149–157 (discussion 173–180)PubMed

Attems J, Preusser M, Grosinger-Quass M, Wagner L, Lintner F, Jellinger K (2008) Calcium-binding protein secretagogin-expressing neurones in the human hippocampus are largely resistant to neurodegeneration in Alzheimer’s disease. Neuropathol Appl Neurobiol 34:23–32. doi:10.1111/j.1365-2990.2007.00854.x PubMed

Benarroch EE (2010) Olfactory system: functional organization and involvement in neurodegenerative disease. Neurology 75:1104–1109. doi:10.1212/WNL.0b013e3181f3db84 PubMed

Bezprozvanny I, Mattson MP (2008) Neuronal calcium mishandling and the pathogenesis of Alzheimer’s disease. Trends Neurosci 31:454–463. doi:10.1016/j.tins.2008.06.005 PubMedCentralPubMed

Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82:239–259PubMed

Braak H, Del Tredici K (2011) Alzheimer’s pathogenesis: is there neuron-to-neuron propagation? Acta Neuropathol 121:589–595. doi:10.1007/s00401-011-0825-z PubMed

Braak H, Braak E, Bohl J, Bratzke H (1998) Evolution of Alzheimer’s disease related cortical lesions. J Neural Transm Suppl 54:97–106PubMed

Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211. [pii]: S0197458002000659PubMed

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. doi:10.1007/s00401-006-0127-z PubMedCentralPubMed

Brady DR, Mufson EJ (1997) Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer’s diseased brain. Neuroscience 80:1113–1125PubMed

Burgos-Ramos E, Hervas-Aguilar A, Aguado-Llera D, Puebla-Jimenez L, Hernandez-Pinto AM, Barrios V et al (2008) Somatostatin and Alzheimer’s disease. Mol Cell Endocrinol 286:104–111. doi:10.1016/j.mce.2008.01.014 PubMed

Burns A (2000) Might olfactory dysfunction be a marker of early Alzheimer’s disease? Lancet 355:84–85. doi:10.1016/S0140-6736(99)90402-6 PubMed

Buxbaum JD, Thinakaran G, Koliatsos V, O’Callahan J, Slunt HH, Price DL et al (1998) Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J Neurosci 18:9629–9637PubMed

Cao L, Schrank BR, Rodriguez S, Benz EG, Moulia TW, Rickenbacher GT et al (2012) Abeta alters the connectivity of olfactory neurons in the absence of amyloid plaques in vivo. Nat Commun 3:1009. doi:10.1038/ncomms2013 PubMedCentralPubMed

Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A et al (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11:909–913. doi:10.1038/ncb1901 PubMedCentralPubMed

Davies P, Katzman R, Terry RD (1980) Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementia. Nature 288:279–280PubMed

Davis KL, Davidson M, Yang RK, Davis BM, Siever LJ, Mohs RC et al (1988) CSF somatostatin in Alzheimer’s disease, depressed patients, and control subjects. Biol Psychiatry 24:710–712PubMed

de Calignon A, Polydoro M, Suarez-Calvet M, William C, Adamowicz DH, Kopeikina KJ et al (2012) Propagation of tau pathology in a model of early Alzheimer’s disease. Neuron 73:685–697. doi:10.1016/j.neuron.2011.11.033 PubMedCentralPubMed

Devanand DP, Michaels-Marston KS, Liu X, Pelton GH, Padilla M, Marder K et al (2000) Olfactory deficits in patients with mild cognitive impairment predict Alzheimer’s disease at follow-up. Am J Psychiatry 157:1399–1405PubMed

Djordjevic J, Jones-Gotman M, De Sousa K, Chertkow H (2008) Olfaction in patients with mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 29:693–706. doi:10.1016/j.neurobiolaging.2006.11.014 PubMed

Doty RL (2008) The olfactory vector hypothesis of neurodegenerative disease: is it viable? Ann Neurol 63:7–15. doi:10.1002/ana.21327 PubMed

Eisele YS, Obermuller U, Heilbronner G, Baumann F, Kaeser SA, Wolburg H et al (2010) Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 330:980–982. doi:10.1126/science.1194516 PubMedCentralPubMed

Epelbaum J, Guillou JL, Gastambide F, Hoyer D, Duron E, Viollet C (2009) Somatostatin, Alzheimer’s disease and cognition: an old story coming of age? Prog Neurobiol 89:153–161. doi:10.1016/j.pneurobio.2009.07.002 PubMed

Esiri MM, Wilcock GK (1984) The olfactory bulbs in Alzheimer’s disease. J Neurol Neurosurg Psychiatry 47:56–60PubMedCentralPubMed

Filali M, Lalonde R (2009) Age-related cognitive decline and nesting behavior in an APPswe/PS1 bigenic model of Alzheimer’s disease. Brain Res 1292:93–99. doi:10.1016/j.brainres.2009.07.066 PubMed

Florio T (2008) Molecular mechanisms of the antiproliferative activity of somatostatin receptors (SSTRs) in neuroendocrine tumors. Front Biosci 13:822–840PubMed

Fonseca M, Soriano E (1995) Calretinin-immunoreactive neurons in the normal human temporal cortex and in Alzheimer’s disease. Brain Res 691:83–91. [pii]: 0006-8993(95)00622-WPubMed

Fotuhi M, Hachinski V, Whitehouse PJ (2009) Changing perspectives regarding late-life dementia. Nat Rev Neurol 5:649–658. doi:10.1038/nrneurol.2009.175 PubMed

Goedert M, Spillantini MG (2006) A century of Alzheimer’s disease. Science 314:777–781. doi:10.1126/science.1132814 PubMed

Gottfried JA, Deichmann R, Winston JS, Dolan RJ (2002) Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J Neurosci 22:10819–10828PubMed

Hama E, Saido TC (2005) Etiology of sporadic Alzheimer’s disease: somatostatin, neprilysin, and amyloid beta peptide. Med Hypotheses 65:498–500. doi:10.1016/j.mehy.2005.02.045 PubMed

Hansen C, Angot E, Bergstrom AL, Steiner JA, Pieri L, Paul G et al (2011) alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Investig 121:715–725. doi:10.1172/JCI43366 PubMedCentralPubMed

Harris JA, Devidze N, Verret L, Ho K, Halabisky B, Thwin MT et al (2010) Transsynaptic progression of amyloid-beta-induced neuronal dysfunction within the entorhinal–hippocampal network. Neuron 68:428–441. doi:10.1016/j.neuron.2010.10.020 PubMedCentralPubMed

Hawkes C, Doty RL (2009) The neurology of olfaction. Cambridge University Press, Cambridge

Hawkes CH, Del Tredici K, Braak H (2007) Parkinson’s disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 33:599–614. doi:10.1111/j.1365-2990.2007.00874.x PubMed

Heizmann CW, Braun K (1992) Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends Neurosci 15:259–264. [pii]: 0166-2236(92)90067-IPubMed

Hernandez F, Avila J (2008) Tau aggregates and tau pathology. J Alzheimers Dis 14:449–452PubMed

Hof PR, Morrison JH (1991) Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer’s disease. Exp Neurol 111:293–301PubMed

Hof PR, Cox K, Young WG, Celio MR, Rogers J, Morrison JH (1991) Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer’s disease. J Neuropathol Exp Neurol 50:451–462PubMed

Hof PR, Nimchinsky EA, Celio MR, Bouras C, Morrison JH (1993) Calretinin-immunoreactive neocortical interneurons are unaffected in Alzheimer’s disease. Neurosci Lett 152:145–148PubMed

Howard JD, Plailly J, Grueschow M, Haynes JD, Gottfried JA (2009) Odor quality coding and categorization in human posterior piriform cortex. Nat Neurosci 12:932–938. doi:10.1038/nn.2324 PubMedCentralPubMed

Iacopino AM, Christakos S (1990) Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 87:4078–4082PubMedCentralPubMed

Iritani S, Niizato K, Emson PC (2001) Relationship of calbindin D28K-immunoreactive cells and neuropathological changes in the hippocampal formation of Alzheimer’s disease. Neuropathology 21:162–167PubMed

Kato HK, Gillet SN, Peters AJ, Isaacson JS, Komiyama T (2013) Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80:1218–1231. doi:10.1016/j.neuron.2013.08.036 PubMed

Kjelvik G, Evensmoen HR, Brezova V, Haberg AK (2012) The human brain representation of odor identification. J Neurophysiol. doi:10.1152/jn.01036.2010 PubMed

Kovacs T, Cairns NJ, Lantos PL (1999) Beta-amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in ageing and Alzheimer’s disease. Neuropathol Appl Neurobiol 25:481–491. [pii]: nan208PubMed

Leinwand SG, Chalasani SH (2011) Olfactory networks: from sensation to perception. Curr Opin Genet Dev 21:806–811. doi:10.1016/j.gde.2011.07.006 PubMed

Leuba G, Kraftsik R, Saini K (1998) Quantitative distribution of parvalbumin, calretinin, and calbindin D-28k immunoreactive neurons in the visual cortex of normal and Alzheimer cases. Exp Neurol 152:278–291. doi:10.1006/exnr.1998.6838 PubMed

Li W, Howard JD, Gottfried JA (2010) Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer’s disease. Brain 133:2714–2726. doi:10.1093/brain/awq209 PubMedCentralPubMed

Mai JK, Paxinos G, Voss T (2008) Atlas of the human brain. Elsevier, New York

Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E et al (2006) Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313:1781–1784. doi:10.1126/science.1131864 PubMed

Mikkonen M, Alafuzoff I, Tapiola T, Soininen H, Miettinen R (1999) Subfield- and layer-specific changes in parvalbumin, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer’s disease. Neuroscience 92:515–532. [pii]: S0306-4522(99)00047-0PubMed

Miyamichi K, Amat F, Moussavi F, Wang C, Wickersham I, Wall NR et al (2011) Cortical representations of olfactory input by trans-synaptic tracing. Nature 472:191–196. doi:10.1038/nature09714 PubMedCentralPubMed

Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L, Mizrahi A (2013) Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80:1232–1245. doi:10.1016/j.neuron.2013.08.027 PubMedCentralPubMed

Mount C, Downton C (2006) Alzheimer disease: progress or profit? Nat Med 12:780–784. doi:10.1038/nm0706-780 PubMed

Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G et al (2000) High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20:4050–4058PubMed

Nelson PT, Braak H, Markesbery WR (2009) Neuropathology and cognitive impairment in Alzheimer disease: a complex but coherent relationship. J Neuropathol Exp Neurol 68:1–14. doi:10.1097/NEN.0b013e3181919a48 PubMedCentralPubMed

Nelson PT, Alafuzoff I, Bigio EH, Bouras C, Braak H, Cairns NJ et al (2012) Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol 71:362–381. doi:10.1097/NEN.0b013e31825018f7 PubMedCentralPubMed

Nestor PJ, Scheltens P, Hodges JR (2004) Advances in the early detection of Alzheimer’s disease. Nat Med 10(Suppl):S34–S41. doi:10.1038/nrn1433nrn1433 PubMed

Ni H, Huang L, Chen N, Zhang F, Liu D, Ge M et al (2010) Upregulation of barrel GABAergic neurons is associated with cross-modal plasticity in olfactory deficit. PLoS ONE 5:e13736. doi:10.1371/journal.pone.0013736 PubMedCentralPubMed

Nilsson CL, Brinkmalm A, Minthon L, Blennow K, Ekman R (2001) Processing of neuropeptide Y, galanin, and somatostatin in the cerebrospinal fluid of patients with Alzheimer’s disease and frontotemporal dementia. Peptides 22:2105–2112PubMed

Ohm TG, Braak H (1987) Olfactory bulb changes in Alzheimer’s disease. Acta Neuropathol 73:365–369PubMed

Palop JJ, Mucke L (2010) Amyloid-beta-induced neuronal dysfunction in Alzheimer’s disease: from synapses toward neural networks. Nat Neurosci 13:812–818. doi:10.1038/nn.2583 PubMedCentralPubMed

Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J et al (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer’s disease-related cognitive deficits. Proc Natl Acad Sci USA 100:9572–9577. doi:10.1073/pnas.1133381100 PubMedCentralPubMed

Palop JJ, Chin J, Mucke L (2006) A network dysfunction perspective on neurodegenerative diseases. Nature 443:768–773. doi:10.1038/nature05289 PubMed

Perrin RJ, Fagan AM, Holtzman DM (2009) Multimodal techniques for diagnosis and prognosis of Alzheimer’s disease. Nature 461:916–922. doi:10.1038/nature08538 PubMedCentralPubMed

Poo C, Isaacson JS (2009) Odor representations in olfactory cortex: “sparse” coding, global inhibition, and oscillations. Neuron 62:850–861. doi:10.1016/j.neuron.2009.05.022 PubMedCentralPubMed

Poo C, Isaacson JS (2011) A major role for intracortical circuits in the strength and tuning of odor-evoked excitation in olfactory cortex. Neuron 72:41–48. doi:10.1016/j.neuron.2011.08.015 PubMedCentralPubMed

Price JL, Morris JC (2004) So what if tangles precede plaques? Neurobiol Aging 25:721–723. doi:10.1016/j.neurobiolaging.2003.12.017 (discussion 743–746)PubMed

Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer’s disease. Neurobiol Aging 12:295–312PubMed

Roman G, Pascual B (2012) Contribution of neuroimaging to the diagnosis of Alzheimer’s disease and vascular dementia. Arch Med Res 43:671–676. doi:10.1016/j.arcmed.2012.10.018 PubMed

Rowe CC, Villemagne VL (2013) Amyloid imaging with PET in early Alzheimer disease diagnosis. Med Clin N Am 97:377–398. doi:10.1016/j.mcna.2012.12.017 PubMed

Rubio A, Sanchez-Mut JV, Garcia E, Velasquez ZD, Oliver J, Esteller M et al (2012) Epigenetic control of somatostatin and cortistatin expression by beta amyloid peptide. J Neurosci Res 90:13–20. doi:10.1002/jnr.22731 PubMed

Runyan CA, Schummers J, Van Wart A, Kuhlman SJ, Wilson NR, Huang ZJ et al (2010) Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 67:847–857. doi:10.1016/j.neuron.2010.08.006 PubMedCentralPubMed

Saito T, Iwata N, Tsubuki S, Takaki Y, Takano J, Huang SM et al (2005) Somatostatin regulates brain amyloid beta peptide Abeta42 through modulation of proteolytic degradation. Nat Med 11:434–439. doi:10.1038/nm1206 PubMed

Saiz-Sanchez D, Ubeda-Banon I, de la Rosa-Prieto C, Argandona-Palacios L, Garcia-Munozguren S, Insausti R et al (2010) Somatostatin, tau, and beta-amyloid within the anterior olfactory nucleus in Alzheimer disease. Exp Neurol 223:347–350. doi:10.1016/j.expneurol.2009.06.010 PubMed

Saiz-Sanchez D, Ubeda-Banon I, de La Rosa-Prieto C, Martinez-Marcos A (2012) Differential expression of interneuron populations and correlation with amyloid-deposition in the olfactory cortex of an APP/PS1 transgenic mouse model of Alzheimer’s disease. J Alzheimers Dis 30:1–17

Saiz-Sanchez D, De La Rosa-Prieto C, Ubeda-Banon I, Martinez-Marcos A (2013) Interneurons and beta-amyloid in the olfactory bulb, anterior olfactory nucleus and olfactory tubercle in APPxPS1 transgenic mice model of Alzheimer’s disease. Anat Rec (Hoboken) 296:1413–1423. doi:10.1002/ar.22750

Sampson VL, Morrison JH, Vickers JC (1997) The cellular basis for the relative resistance of parvalbumin and calretinin immunoreactive neocortical neurons to the pathology of Alzheimer’s disease. Exp Neurol 145:295–302. doi:10.1006/exnr.1997.6433 PubMed

Selkoe DJ (2001) Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev 81:741–766PubMed

Serby M, Richardson SB, Twente S, Siekierski J, Corwin J, Rotrosen J (1984) CSF somatostatin in Alzheimer’s disease. Neurobiol Aging 5:187–189PubMed

Sheng JG, Price DL, Koliatsos VE (2002) Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J Neurosci 22:9794–9799PubMed

Small SA, Duff K (2008) Linking Abeta and tau in late-onset Alzheimer’s disease: a dual pathway hypothesis. Neuron 60:534–542. doi:10.1016/j.neuron.2008.11.007 PubMedCentralPubMed

Solodkin A, Veldhuizen SD, Van Hoesen GW (1996) Contingent vulnerability of entorhinal parvalbumin-containing neurons in Alzheimer’s disease. J Neurosci 16:3311–3321PubMed

Sosulski DL, Bloom ML, Cutforth T, Axel R, Datta SR (2011) Distinct representations of olfactory information in different cortical centres. Nature 472:213–216. doi:10.1038/nature09868 PubMedCentralPubMed

Stettler DD, Axel R (2009) Representations of odor in the piriform cortex. Neuron 63:854–864. doi:10.1016/j.neuron.2009.09.005 PubMed

Suzuki N, Bekkers JM (2010) Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J Comp Neurol 518:1670–1687. doi:10.1002/cne.22295 PubMed

Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R et al (1991) Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572–580. doi:10.1002/ana.410300410 PubMed

Tsuboi Y, Wszolek ZK, Graff-Radford NR, Cookson N, Dickson DW (2003) Tau pathology in the olfactory bulb correlates with Braak stage, Lewy body pathology and apolipoprotein epsilon4. Neuropathol Appl Neurobiol 29:503–510. [pii]: 453PubMed

Umeda T, Tomiyama T, Sakama N, Tanaka S, Lambert MP, Klein WL et al (2011) Intraneuronal amyloid beta oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J Neurosci Res 89:1031–1042. doi:10.1002/jnr.22640 PubMed

Verret L, Mann EO, Hang GB, Barth AM, Cobos I, Ho K et al (2012) Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149:708–721. doi:10.1016/j.cell.2012.02.046 PubMedCentralPubMed

Vickers JC, Dickson TC, Adlard PA, Saunders HL, King CE, McCormack G (2000) The cause of neuronal degeneration in Alzheimer’s disease. Prog Neurobiol 60:139–165. [pii]: S0301008299000234PubMed

Viollet C, Lepousez G, Loudes C, Videau C, Simon A, Epelbaum J (2008) Somatostatinergic systems in brain: networks and functions. Mol Cell Endocrinol 286:75–87. doi:10.1016/j.mce.2007.09.007 PubMed

Wang J, Eslinger PJ, Doty RL, Zimmerman EK, Grunfeld R, Sun X et al (2010) Olfactory deficit detected by fMRI in early Alzheimer’s disease. Brain Res 1357:184–194. doi:10.1016/j.brainres.2010.08.018 PubMedCentralPubMed

Wesson DW, Levy E, Nixon RA, Wilson DA (2010) Olfactory dysfunction correlates with amyloid-beta burden in an Alzheimer’s disease mouse model. J Neurosci 30:505–514. doi:10.1523/JNEUROSCI.4622-09.2010 PubMedCentralPubMed

Wesson DW, Borkowski AH, Landreth GE, Nixon RA, Levy E, Wilson DA (2011) Sensory network dysfunction, behavioral impairments, and their reversibility in an Alzheimer’s beta-amyloidosis mouse model. J Neurosci 31:15962–15971. doi:10.1523/JNEUROSCI.2085-11.2011 PubMedCentralPubMed

Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519. doi:10.1016/j.neuron.2011.10.027 PubMedCentralPubMed

Wilson RS, Arnold SE, Schneider JA, Boyle PA, Buchman AS, Bennett DA (2009) Olfactory impairment in presymptomatic Alzheimer’s disease. Ann N Y Acad Sci 1170:730–735. doi:10.1111/j.1749-6632.2009.04013.x PubMedCentralPubMed

Wood PL, Etienne P, Lal S, Gauthier S, Cajal S, Nair NP (1982) Reduced lumbar CSF somatostatin levels in Alzheimer’s disease. Life Sci 31:2073–2079PubMed

Wu N, Rao X, Gao Y, Wang J, Xu F (2013) Amyloid-beta deposition and olfactory dysfunction in an Alzheimer’s disease model. J Alzheimers Dis 37:699–712. doi:10.3233/JAD-122443 PubMed

Young JW, Sharkey J, Finlayson K (2009) Progressive impairment in olfactory working memory in a mouse model of mild cognitive impairment. Neurobiol Aging 30:1430–1443. doi:10.1016/j.neurobiolaging.2007.11.018 PubMed

Zelano C, Sobel N (2005) Humans as an animal model for systems-level organization of olfaction. Neuron 48:431–454. doi:10.1016/j.neuron.2005.10.009 PubMed

Zhang W, Hao J, Liu R, Zhang Z, Lei G, Su C et al (2011) Soluble Abeta levels correlate with cognitive deficits in the 12-month-old APPswe/PS1dE9 mouse model of Alzheimer’s disease. Behav Brain Res 222:342–350. doi:10.1016/j.bbr.2011.03.072 PubMed

Title: Interneurons, tau and amyloid-β in the piriform cortex in Alzheimer’s disease
Authors: Daniel Saiz-Sanchez
Carlos De la Rosa-Prieto
Isabel Ubeda-Banon
Alino Martinez-Marcos
Publication date: 01-07-2015
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 4/2015
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-014-0771-3

At a glance: The STEP trials

Springer Medicine

Interneurons, tau and amyloid-β in the piriform cortex in Alzheimer’s disease

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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