Amyloid Beta Inhibits Olfactory Bulb Activity and the Ability to Smell

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Alvarado Martínez, Reynaldo ^a   Salgado Puga, Karla ^a   Peña Ortega, Fernando ^a  

^a INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEEDING BEHAVIOR; HISTOLOGY; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; OLFACTORY BULB NETWORK ACTIVITY; OUTCOME ASSESSMENT; PYRIFORM CORTEX; RAT; SIGNAL DETECTION; SIGNAL TRANSDUCTION; SMELLING; SYNAPTIC TRANSMISSION;

AGING; AMYLOID BETA-PEPTIDES; ANIMALS; DISEASE MODELS, ANIMAL; MALE; MICE; MICE, TRANSGENIC; OLFACTORY BULB; OLFACTORY PATHWAYS; RATS; RATS, WISTAR; SMELL;

EID: 84884599125     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075745     Document Type: Article

References (121)

1. Thompson MD, Knee K, Golden CJ, (1998) Olfaction in persons with Alzheimer's disease. Neuropsychol Rev 8: 11-23. doi:10.1023/A:1025627106073. PubMed: 9585920.
2. Warner MD, Peabody CA, Flattery JJ, Tinklenberg JR, (1986) Olfactory deficits and Alzheimer's disease. Biol Psychiatry 21: 116-118. doi:10.1016/0006-3223(86)90013-2. PubMed: 3942798.
3. Mesholam RI, Moberg PJ, Mahr RN, Doty RL, (1998) Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Arch Neurol 55: 84-90. doi:10.1001/archneur.55.1.84. PubMed: 9443714.
4. Murphy C, Gilmore MM, Seery CS, Salmon DP, Lasker BR, (1990) Olfactory thresholds are associated with degree of dementia in Alzheimer's disease. Neurobiol Aging 11: 465-469. doi:10.1016/0197-4580(90)90014-Q. PubMed: 2381506.
5. Serby M, Larson P, Kalkstein D, (1991) The nature and course of olfactory deficits in Alzheimer's disease. Am J Psychiatry 148: 357-360. PubMed: 1992839.
6. Schofield PW, Ebrahimi H, Jones AL, Bateman GA, Murray SR, (2012) An olfactory 'stress test' may detect preclinical Alzheimer's disease. BMC Neurol 12: 24. doi:10.1186/1471-2377-12-24. PubMed: 22551361.
7. 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: 295-312. doi:10.1016/0197-4580(91)90006-6. PubMed: 1961359.
8. Kovács T, (2004) Mechanisms of olfactory dysfunction in aging and neurodegenerative disorders. Ageing Res Rev 3: 215-232. doi:10.1016/j.arr.2003.10.003. PubMed: 15177056.
9. Kovács T, Cairns NJ, Lantos PL, (1999) Beta-amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in aging and Alzheimer's disease. Neuropathol Appl Neurobiol 25: 481-491. doi:10.1046/j.1365-2990.1999.00208.x. PubMed: 10632898.
10. Attems J, Lintner F, Jellinger KA, (2005) Olfactory involvement in aging and Alzheimer's disease: an autopsy study. J Alzheimers Dis 7: 149-157. PubMed: 15851853.
11. Arnold SE, Lee EB, Moberg PJ, Stutzbach L, Kazi H, et al. (2010) Olfactory epithelium amyloid-beta and paired helical filament-tau pathology in Alzheimer disease. Ann Neurol 67: 462-469. doi:10.1002/ana.21910. PubMed: 20437581.
12. Coronas-Sámano G, Medina-Aguirre I, Aguilar-Vázquez A, Portillo-Martínez W, González-Luna I, et al. (2011) Conducta olfativa en un modelo murino de Alzheimer. Rev Dig Univ 12: 1067-1079.
13. Guérin D, Sacquet J, Mandairon N, Jourdan F, Didier A, (2009) Early locus coeruleus degeneration and olfactory dysfunctions in Tg2576 mice. Neurobiol Aging 30: 272-283. doi:10.1016/j.neurobiolaging.2007.05.020. PubMed: 17618708.
14. 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: 18242780.
15. 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. PubMed: 20071513.
16. Wesson DW, Morales-Corraliza J, Mazzella MJ, Wilson DA, Mathews PM, (2013) Chronic anti-murine Abeta immunization preserves odor guided behaviors in an Alzheimer's beta-amyloidosis model. Behav Brain Res 237: 96-102. doi:10.1016/j.bbr.2012.09.019. PubMed: 23000537.
17. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, et al. (2011) Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134: 258-277. doi:10.1093/brain/awq341. PubMed: 21186265.
18. Montgomery KS, Simmons RK, Edwards G 3rd, Nicolle MM, Gluck MA, et al. (2011) Novel age-dependent learning deficits in a mouse model of Alzheimer's disease: implications for translational research. Neurobiol Aging 32: 1273-1285. doi:10.1016/j.neurobiolaging.2009.08.003. PubMed: 19720431.
19. Cramer PE, Cirrito JR, Wesson DW, Lee CY, Karlo JC, et al. (2012) ApoE-directed therapeutics rapidly clear beta-amyloid and reverse deficits in AD mouse models. Science 335: 1503-1506. doi:10.1126/science.1217697. PubMed: 22323736.
20. Cao L, Schrank BR, Rodriguez S, Benz EG, Moulia TW, 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. PubMed: 22910355.
21. Lehman EJ, Kulnane LS, Lamb BT, (2003) Alterations in beta-amyloid production and deposition in brain regions of two transgenic models. Neurobiol Aging 24: 645-653. doi:10.1016/S0197-4580(02)00153-7. PubMed: 12885572.
22. Kameshima N, Nanjou T, Fukuhara T, Yanagisawa D, Tooyama I, (2012) Correlation of Abeta deposition in the nasal cavity with the formation of senile plaques in the brain of a transgenic mouse model of Alzheimer's disease. Neurosci Lett 513: 166-169. doi:10.1016/j.neulet.2012.02.026. PubMed: 22343315.
23. Rey NL, Jardanhazi-Kurutz D, Terwel D, Kummer MP, Jourdan F, et al. (2012) Locus coeruleus degeneration exacerbates olfactory deficits in APP/PS1 transgenic mice. Neurobiol Aging 33: 426.e1-426.e11. PubMed: 21109328.
24. Cheng N, Cai H, Belluscio L, (2011) In vivo olfactory model of APP-induced neurodegeneration reveals a reversible cell-autonomous function. J Neurosci 31(39):: 13699-13704. doi:10.1523/JNEUROSCI.1714-11.2011. PubMed: 21957232.
25. Calderón-Garcidueñas L, Franco-Lira M, Torres-Jardón R, Henriquez-Roldán C, Barragán-Megía G, et al. (2007) Pediatric respiratory and systemic effects of chronic air pollution exposure: nose, lung, heart, and brain pathology. Toxicol Pathol 35: 154-162. doi:10.1080/01926230601059985. PubMed: 17325984.
26. Calderón-Garcidueñas L, Franco-Lira M, Henríquez-Roldán C, Osnaya N, González-Maciel A, et al. (2010) Urban air pollution: influences on olfactory function and pathology in exposed children and young adults. Exp Toxicol Pathol 62: 91-102. doi:10.1016/j.etp.2009.02.117. PubMed: 19297138.
27. Nieuwenhuys R, (1967) Comparative anatomy of olfactory centres and tracts. Prog Brain Res 23: 1-64. PubMed: 6020786.
28. Shepherd GM, (1972) Synaptic organization of the mammalian olfactory bulb. Physiol Rev 52: 864-917. PubMed: 4343762.
29. Adrian ED, (1950) The electrical activity of the mammalian olfactory bulb. Electroencephalogr Clin Neurophysiol 2: 377-388. doi:10.1016/0013-4694(50)90075-7. PubMed: 14793507.
30. Beshel J, Kopell N, Kay LM, (2007) Olfactory bulb gamma oscillations are enhanced with task demands. J Neurosci 27: 8358-8365. doi:10.1523/JNEUROSCI.1199-07.2007. PubMed: 17670982.
31. Kay LM, Beshel J, (2010) A beta oscillation network in the rat olfactory system during a 2 alternative choice odor discrimination task. J Neurophysiol 104: 829-839. doi:10.1152/jn.00166.2010. PubMed: 20538778.
32. Kay LM, Beshel J, Brea J, Martin C, Rojas-Líbano D, (2009) Olfactory oscillations: the what, how and what for. Trends Neurosci 32: 207-214. doi:10.1016/j.tins.2008.11.008. PubMed: 19243843.
33. Rojas-Líbano D, Kay LM, (2008) Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cogn Neurodyn 2: 179-194. doi:10.1007/s11571-008-9053-1. PubMed: 19003484.
34. Friedman D, Strowbridge BW, (2000) Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84: 39-50. PubMed: 10899181.
35. Friedman D, Strowbridge BW, (2003) Both electrical and chemical synapses mediate fast network oscillations in the olfactory bulb. J Neurophysiol 89: 2601-2610. doi:10.1152/jn.00887.2002. PubMed: 12740407.
36. Murakami M, Kashiwadani H, Kirino Y, Mori K, (2005) State-dependent sensory gating in olfactory cortex. Neuron 46: 285-296. doi:10.1016/j.neuron.2005.02.025. PubMed: 15848806.
37. Wachowiak M, Shipley MT, (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17: 411-423. doi:10.1016/j.semcdb.2006.04.007. PubMed: 16765614.
38. Martin C, Gervais R, Chabaud P, Messaoudi B, Ravel N, (2004) Learning-induced modulation of oscillatory activities in the mammalian olfactory system: the role of the centrifugal fibres. J Physiol Paris 98: 467-478. doi:10.1016/j.jphysparis.2005.09.003. PubMed: 16274975.
39. Martin C, Gervais R, Messaoudi B, Ravel N, (2006) Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur J Neurosci Volumes 7: 1801-1810. PubMed: 16623837.
40. Gervais R, Buonviso N, Martin C, Ravel N, (2007) What do electrophysiological studies tell us about processing at the olfactory bulb level? J Physiol Paris 101: 40-45. doi:10.1016/j.jphysparis.2007.10.006. PubMed: 18054211.
41. Stakic J, Suchanek JM, Ziegler GP, Griff ER, (2011) The source of spontaneous activity in the main olfactory bulb of the rat. PLOS ONE 6: e23990. doi:10.1371/journal.pone.0023990. PubMed: 21912614.
42. Nusser Z, Kay LM, Laurent G, Homanics GE, Mody I, (2001) Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86: 2823-2833. PubMed: 11731539.
43. Le Pichon CE, Valley MT, Polymenidou M, Chesler AT, Sagdullaev BT, et al. (2009) Olfactory behavior and physiology are disrupted in prion protein knockout mice. Nat Neurosci 12: 60-69. doi:10.1038/nn.2238. PubMed: 19098904.
44. Lepousez G, Mouret A, Loudes C, Epelbaum J, Viollet C, (2010) Somatostatin contributes to in vivo gamma oscillation modulation and odor discrimination in the olfactory bulb. J Neurosci 30: 870-875. doi:10.1523/JNEUROSCI.4958-09.2010. PubMed: 20089895.
45. Peña F, Ordaz B, Balleza-Tapia H, Bernal-Pedraza R, Márquez-Ramos A, et al. (2010) Beta-amyloid protein (25-35) disrupts hippocampal network activity: role of Fyn-kinase. Hippocampus 20: 78-96. PubMed: 19294646.
46. Villette V, Poindessous-Jazat F, Simon A, Léna C, Roullot E, et al. (2010) Decreased rhythmic GABAergic septal activity and memory-associated theta oscillations after hippocampal amyloid-beta pathology in the rat. J Neurosci 30: 10991-11003. doi:10.1523/JNEUROSCI.6284-09.2010. PubMed: 20720106.
47. Colom LV, Castañeda MT, Bañuelos C, Puras G, García-Hernández A, et al. (2010) Medial septal beta-amyloid 1-40 injections alter septo-hippocampal anatomy and function. Neurobiol Aging 31: 46-57. doi:10.1016/j.neurobiolaging.2008.05.006. PubMed: 18547680.
48. Pena-Ortega F, Solis-Cisneros A, Ordaz B, Balleza-Tapia H, López-Guerrero J, (2012) Amyloid beta 1-42 inhibits entorhinal cortex activity in the beta-gamma range: role of GSK-3. Curr Alzheimers 9: 857-863. doi:10.2174/156720512802455403. PubMed: 22631612.
49. Peña-Ortega F, Bernal-Pedraza R, (2012) Amyloid Beta Peptide slows down sensory-induced hippocampal oscillations. Int J Pept, 2012(2012): 236289. PubMed: 22611415.
50. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, 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. PubMed: 22541439.
51. Peña-Ortega F, (2013) Amyloid Beta-Protein and Neural Network Dysfunction. Neurodegener Dis: pp. 2013: 657470.
52. Balleza-Tapia H, Huanosta-Gutiérrez A, Márquez-Ramos A, Arias N, Peña F, (2010) Amyloid β oligomers decrease hippocampal spontaneous network activity in an age-dependent manner. Curr Alzheimer Res 7: 453-462. doi:10.2174/156720510791383859. PubMed: 20043810.
53. Näslund J, Haroutunian V, Mohs R, Davis KL, Davies P, et al. (2000) Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283: 1571-1577. doi:10.1001/jama.283.12.1571. PubMed: 10735393.
54. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, et al. (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155: 853-862. doi:10.1016/S0002-9440(10)65184-X. PubMed: 10487842.
55. Peña F, Gutierrez-Lerma A, Quirzo-Baez R, Arias C, (2006) The role of beta amyloid protein in synaptic function: implications for Alzheimer's disease therapy. Curr Neurpharmacol 4: 149-163. doi:10.2174/157015906776359531.
56. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421. doi:10.1016/S0896-6273(03)00434-3. PubMed: 12895417.
57. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95: 6448-6453. doi:10.1073/pnas.95.11.6448. PubMed: 9600986.
58. Paxinos G, Watson C, (2007) The rat brain: in stereotaxic coordinates. (P. G and W. C, Eds.) (sixth edit., pp. 456) Elsevier/Academic Press, New York.
59. Edwards DA, Walter B, Liang P, (1996) Hypothalamic and olfactory control of sexual behavior and partner preference in male rats. Physiol Behav 60: 1347-1354. PubMed: 8916193.
60. Portillo W, Paredes RG, (2004) Sexual incentive motivation, olfactory preference, and activation of the vomeronasal projection pathway by sexually relevant cues in non-copulating and naive male rats. Horm Behav 46: 330-340. doi:10.1016/j.yhbeh.2004.03.001. PubMed: 15325233.
61. Mucignat-Caretta C, Bondí M, Rubini A, Calabrese F, Barbato A, (2009) The olfactory system is affected by steroid aerosol treatment in mice. Am J Physiol Lung Cell Mol Physiol 297: L1073-L1081. doi:10.1152/ajplung.00014.2009. PubMed: 19801453.
62. Badonnel K, Lacroix MC, Monnerie R, Durieux D, Caillol M, et al. (2012) Chronic restricted access to food leading to undernutrition affects rat neuroendocrine status and olfactory-driven behaviors. Horm Behav 62: 120-127. doi:10.1016/j.yhbeh.2012.05.010. PubMed: 22633909.
63. Baunez C, Amalric M, Robbins TW, (2002) Enhanced Food-Related Motivation after Bilateral Lesions of the Subthalamic Nucleus. J Neurosci 22: 562-568. PubMed: 11784803.
64. Peña F, Tapia R, (2000) Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 101: 547-561. doi:10.1016/S0306-4522(00)00400-0. PubMed: 11113304.
65. Peña F, Tapia R, (1999) Relationships among seizures, extracellular amino acid changes, and neurodegeneration induced by 4-aminopyridine in rat hippocampus: a microdialysis and electroencephalographic study. J Neurochem 72: 2006-2014. PubMed: 10217278.
66. Larriva-Sahd J, (2012) Cytological organization of the alpha component of the anterior olfactory nucleus and olfactory limbus. Front Neuroanat 6: 23. PubMed: 22754506.
67. Bacskai BJ, Hickey GA, Skoch J, Kajdasz ST, Wang Y, et al. (2003) Hyman Four-dimensional multiphoton imaging of brain entry, amyloid binding, and clearance of an amyloid-β ligand in transgenic mice. Proc Natl Acad Sci USA 14; 100:: 12462-12467.
68. Luna-Muñoz J, Peralta-Ramirez J, Chávez-Macías L, Harrington CR, Wischik CM, et al. (2008) Thiazin red as a neuropathological tool for the rapid diagnosis of Alzheimer's disease in tissue imprints. Acta Neuropathol 116: 507-515. doi:10.1007/s00401-008-0431-x. PubMed: 18810470.
69. Condello C, Schain A, Grutzendler J, (2011) Multicolor time-stamp reveals the dynamics and toxicity of amyloid deposition. Sci Rep 1: 19. PubMed: 22355538.
70. Gutiérrez-Lerma AI, Ordaz B, Peña-Ortega F, (2013) Amyloid Beta Peptides Differentially Affect Hippocampal Theta Rhythms In Vitro. Int J Pept, 2013(2013); 328140. PubMed: 23878547.
71. Ramírez-Jarquín JO, Lara-Hernández S, López-Guerrero JJ, Aguileta MA, Rivera-Angulo AJ, et al. (2012) Somatostatin modulates generation of inspiratory rhythms and determines asphyxia survival. Peptides 34: 360-372. doi:10.1016/j.peptides.2012.02.011. PubMed: 22386651.
72. Adaya-Villanueva A, Ordaz B, Balleza-Tapia H, Márquez-Ramos A, Peña-Ortega F, (2010) Beta-like hippocampal network activity is differentially affected by amyloid beta peptides. Peptides 31: 1761-1766. doi:10.1016/j.peptides.2010.06.003. PubMed: 20558221.
73. Lagier S, Carleton A, Lledo PM, (2004) Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J Neurosci 24: 4382-4392. doi:10.1523/JNEUROSCI.5570-03.2004. PubMed: 15128852.
74. Lagier S, Panzanelli P, Russo RE, Nissant A, Bathellier B, et al. (2007) GABAergic inhibition at dendrodendritic synapses tunes gamma oscillations in the olfactory bulb. Proc Natl Acad Sci USA 104: 7259-7264. doi:10.1073/pnas.0701846104. PubMed: 17428916.
75. Sassoè-Pognetto M, Panzanelli P, Lagier S, Fritschy JM, Lledo PM, (2009) GABA receptor heterogeneity modulates dendrodendritic inhibition. Ann N Y Acad Sci 1170: 259-263. doi:10.1111/j.1749-6632.2009.03882.x. PubMed: 19686144.
76. Igelström KM, Shirley CH, Heyward PM, (2011) Low-magnesium medium induces epileptiform activity in mouse olfactory bulb slices. J Neurophysiol 106: 2593-2605. doi:10.1152/jn.00601.2011. PubMed: 21832029.
77. Chapman CA, Xu Y, Haykin S, Racine RJ, (1998) Beta-frequency (15-35 Hz) electroencephalogram activities elicited by toluene and electrical stimulation in the behaving rat. Neuroscience 86: 1307-1319. doi:10.1016/S0306-4522(98)00092-X. PubMed: 9697135.
78. Li A, Gong L, Xu F, (2011) Brain-state-independent neural representation of peripheral stimulation in rat olfactory bulb. Proc Natl Acad Sci USA 108: 5087-5092. doi:10.1073/pnas.1013814108. PubMed: 21321196.
79. Selkoe DJ, (1993) Physiological production of the beta-amyloid protein and the mechanism of Alzheimer's disease. Trends Neurosci 16: 403-409. doi:10.1016/0166-2236(93)90008-A. PubMed: 7504355.
80. Hughes JR, Shanmugham S, Wetzel LC, Bellur S, Hughes CA, (1989) The relationship between EEG changes and cognitive functions in dementia: a study in a VA population. Clin Electroencephalogr 20: 77-85. PubMed: 2706793.
81. Schreiter-Gasser U, Gasser T, Ziegler P, (1994) Quantitative EEG analysis in early onset Alzheimer's disease: correlations with severity, clinical characteristics, visual EEG and CCT. Electroencephalogr Clin Neurophysiol 90: 267-272. doi:10.1016/0013-4694(94)90144-9. PubMed: 7512907.
82. Busciglio J, Andersen JK, Schipper HM, Gilad GM, McCarty R, et al. (1998) Stress, aging, and neurodegenerative disorders. Molecular mechanisms. Ann N Y Acad Sci 851: 429-443. doi:10.1111/j.1749-6632.1998.tb09021.x. PubMed: 9668637.
83. Rosenzweig ES, Barnes CA, (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog Neurobiol 69: 143-179. doi:10.1016/S0301-0082(02)00126-0. PubMed: 12758108.
84. Araki T, Kato H, Shuto K, Itoyama Y, (1997) Age-related changes in [3H]nimodipine and [3H]rolipram binding in the rat brain. J Pharm Pharmacol 49: 310-314. doi:10.1111/j.2042-7158.1997.tb06802.x. PubMed: 9231352.
85. Barnes CA, Rao G, Orr G, (2000) Age-related decrease in the Schaffer collateral-evoked EPSP in awake, freely behaving rats. Neural Plast 7: 167-178. doi:10.1155/NP.2000.167. PubMed: 11147459.
86. Thibault O, Landfield PW, (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272: 1017-1020. doi:10.1126/science.272.5264.1017. PubMed: 8638124.
87. Mostany R, Anstey JE, Crump KL, Maco B, Knott G, et al. (2013) Altered Synaptic Dynamics during Normal Brain Aging. J Neurosci 33: 4094-4104. doi:10.1523/JNEUROSCI.4825-12.2013. PubMed: 23447617.
88. Vreugdenhil M, Toescu EC, (2005) Age-dependent reduction of gamma oscillations in the mouse hippocampus in vitro. Neuroscience 132: 1151-1157. doi:10.1016/j.neuroscience.2005.01.025. PubMed: 15857717.
89. Ramirez JM, Tryba AK, Peña F, (2004) Pacemaker neurons and neuronal networks: an integrative view. Curr Opin Neurobiol 14: 665-674. doi:10.1016/j.conb.2004.10.011. PubMed: 15582367.
90. Xing C, Yin Y, Chang R, He X, Xie Z, (2005) A role of insulin-like growth factor 1 in beta amyloid-induced disinhibition of hippocampal neurons. Neurosci Lett: pp. 12-19;384(1-2): 93-7.
91. Nimmrich V, Grimm C, Draguhn A, Barghorn S, Lehmann A, et al. (2008) Amyloid beta oligomers (A beta(1-42) globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J Neurosci 28: 788-797. doi:10.1523/JNEUROSCI.4771-07.2008. PubMed: 18216187.
92. Didier A, Carleton A, Bjaalie JG, Vincent JD, Ottersen OP, et al. (2001) A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb. Proc Natl Acad Sci USA 98: 6441-6446. doi:10.1073/pnas.101126398. PubMed: 11353824.
93. Mori K, Takagi SF, (1978) An intracellular study of dendrodendritic inhibitory synapses on mitral cells in the rabbit olfactory bulb. J Physiol 279: 569-588. PubMed: 671363.
94. Gray CM, Skinner JE, (1988) Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Exp Brain Res 69: 378-386. PubMed: 3345814.
95. Eeckman FH, Freeman WJ, (1990) Correlations between unit firing and EEG in the rat olfactory system. Brain Res 528: 238-244. doi:10.1016/0006-8993(90)91663-2. PubMed: 2271924.
96. Fourcaud-Trocmé N, Courtiol E, Buonviso N, Voegtlin T, (2011) Stability of fast oscillations in the mammalian olfactory bulb: experiments and modeling. J Physiol 105: 59-70. PubMed: 21843638.
97. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, et al. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274: 99-102. doi:10.1126/science.274.5284.99. PubMed: 8810256.
98. Freeman WJ, (1978) Spatial properties of an EEG event in the olfactory bulb and cortex. Electroencephalogr Clin Neurophysiol 44: 586-605. doi:10.1016/0013-4694(78)90126-8. PubMed: 77765.
99. Isaacson JS, Strowbridge BW, (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20: 749-761. doi:10.1016/S0896-6273(00)81013-2. PubMed: 9581766.
100. Rall W, Shepherd GM, Reese TS, Brightman MW, (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14: 44-56. doi:10.1016/0014-4886(66)90023-9. PubMed: 5900523.
101. Cleary J, Hittner JM, Semotuk M, Mantyh P, O'Hare E, (1995) Beta-amyloid(1-40) effects on behavior and memory. Brain Res 682: 69-74. doi:10.1016/0006-8993(95)00323-I. PubMed: 7552329.
102. Giovannelli L, Casamenti F, Scali C, Bartolini L, Pepeu G, (1995) Differential effects of amyloid peptides beta-(1-40) and beta-(25-35) injections into the rat nucleus basalis. Neuroscience 66: 781-792. doi:10.1016/0306-4522(94)00610-H. PubMed: 7651609.
103. O'Hare E, Weldon DT, Mantyh PW, Ghilardi JR, Finke MP, et al. (1999) Delayed behavioral effects following intrahippocampal injection of aggregated A beta (1-42). Brain Res 815: 1-10. doi:10.1016/S0006-8993(98)01002-6. PubMed: 9974116.
104. Nakamura S, Murayama N, Noshita T, Annoura H, Ohno T, (2001) Progressive brain dysfunction following intracerebroventricular infusion of beta(1-42)-amyloid peptide. Brain Res 912: 128-136. doi:10.1016/S0006-8993(01)02704-4. PubMed: 11532428.
105. Stéphan A, Laroche S, Davis S, (2001) Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J Neurosci 21: 5703-5714. PubMed: 11466442.
106. Richardson RL, Kim EM, Shephard RA, Gardiner T, Cleary J, et al. (2002) Behavioural and histopathological analyses of ibuprofen treatment on the effect of aggregated AB(1-42) injections in the rat. Brain Res 954: 1-10. doi:10.1016/S0006-8993(02)03006-8. PubMed: 12393227.
107. Yamada K, Takayanagi M, Kamei H, Nagai T, Dohniwa M, et al. (2005) Effects of memantine and donepezil on amyloid beta-induced memory impairment in a delayed-matching to position task in rats. Behav Brain Res 162: 191-199. doi:10.1016/j.bbr.2005.02.036. PubMed: 15904984.
108. Malm T, Ort M, Tähtivaara L, Jukarainen N, Goldsteins G, et al. (2006) Beta-Amyloid infusion results in delayed and age-dependent learning deficits without role of inflammation or beta-amyloid deposits. Proc Natl Acad Sci USA 103: 8852-8857. doi:10.1073/pnas.0602896103. PubMed: 16723396.
109. Klementiev B, Novikova T, Novitskaya V, Walmod PS, Dmytriyeva O, et al. (2007) A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Abeta25-35. Neuroscience 145: 209-224. doi:10.1016/j.neuroscience.2006.11.060. PubMed: 17223274.
110. Frautschy SA, Yang F, Calderón L, Cole GM, (1996) Rodent models of Alzheimer's disease: Rat A beta infusion approaches to amyloid deposits. Neurobiol Aging 17: 311-321. doi:10.1016/0197-4580(95)02073-X. PubMed: 8744413.
111. Kane MD, Lipinski WJ, Callahan MJ, Bian F, Durham RA, et al. (2000) Evidence for seeding of beta-amyloid by intracerebral infusion of Alzheimer brain extracts in beta-amyloid precursor protein-transgenic mice. J Neurosci 20: 3606-3611. PubMed: 10804202.
112. Langer F, Eisele YS, Fritschi SK, Staufenbiel M, Walker LC, et al. (2011) Soluble Aβ seeds are potent inducers of cerebral β-amyloid deposition. J Neurosci 31: 14488-14495. doi:10.1523/JNEUROSCI.3088-11.2011. PubMed: 21994365.
113. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, 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: 16990547.
114. Eisele YS, Bolmont T, Heikenwalder M, Langer F, Jacobson LH, et al. (2009) Induction of cerebral beta-amyloidosis: intracerebral versus systemic Abeta inoculation. Proc Natl Acad Sci USA 106: 12926-12931. doi:10.1073/pnas.0903200106. PubMed: 19622727.
115. Watts JC, Giles K, Grillo SK, Lemus A, DeArmond SJ, et al. (2011) Bioluminescence imaging of Abeta deposition in bigenic mouse models of Alzheimer's disease. Proc Natl Acad Sci USA 108: 2528-2533. doi:10.1073/pnas.1019034108. PubMed: 21262831.
116. Nobakht M, Hoseini SM, Mortazavi P, Sohrabi I, Esmailzade B, et al. (2011) Neuropathological changes in brain cortex and hippocampus in a rat model of Alzheimer's disease. Iran Biomed J 15: 51-58. PubMed: 21725500.
117. Morales R, Duran-Aniotz C, Castilla J, Estrada LD, Soto C, (2012) De novo induction of amyloid-β deposition in vivo. Mol Psychiatry 17: 1347-1353. doi:10.1038/mp.2011.120. PubMed: 21968933.
118. Zussy C, Brureau A, Delair B, Marchal S, Keller E, et al. (2011) Time-course and regional analyses of the physiopathological changes induced after cerebral injection of an amyloid β fragment in rats. Am J Pathol 179: 315-334. doi:10.1016/j.ajpath.2011.03.021. PubMed: 21703413.
119. Zussy C, Brureau A, Keller E, Marchal S, Blayo C, et al. (2013) Alzheimer's disease related markers, cellular toxicity and behavioral deficits induced six weeks after oligomeric amyloid-β peptide injection in rats. PLOS ONE 8: e53117. doi:10.1371/journal.pone.0053117. PubMed: 23301030.
120. Sigurdsson EM, Lorens SA, Hejna MJ, Dong XW, Lee JM, (1996) Local and distant histopathological effects of unilateral amyloid-beta 25-35 injections into the amygdala of young F344 rats. Neurobiol Aging 17: 893-901. doi:10.1016/S0197-4580(96)00169-8. PubMed: 9363801.
121. Harris JA, Devidze N, Verret L, Ho K, Halabisky B, et al. (2010) Transsynaptic progression of amyloid-β-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 68: 428-441. doi:10.1016/j.neuron.2010.10.020. PubMed: 21040845.