Amyloid beta peptides differentially affect hippocampal theta rhythms in vitro

International Journal of Peptides

Volumn 2013, Issue , 2013, Pages

  Gutiérrez Lerma, Armando I ^a,b   Ordaz, Benito ^a   Peña Ortega, Fernando ^a  

^a INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID BETA PROTEIN[25-35]; CARBACHOL;

ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DELTA RHYTHM; HIPPOCAMPUS THETA RHYTHM; IN VITRO STUDY; MALE; NONHUMAN; OSCILLATION; POWER SPECTRUM; PRIORITY JOURNAL; RAT;

EID: 84880169704     PISSN: 16879767     EISSN: 16879775     Source Type: Journal    
DOI: 10.1155/2013/328140     Document Type: Article

References (100)

1. Hebert L. E., Scherr P. A., Bienias J. L., Bennett D. A., Evans D. A., Alzheimer disease in the US population: prevalence estimates using the 2000 census. Archives of Neurology 2003 60 8 1119 1122 2-s2.0-0042023711 10.1001/archneur.60.8.1119
2. Braak H., Braak E., Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiology of Aging 1997 18 4 351 357 2-s2.0-0030805991 10.1016/S0197-4580(97)00056-0
3. Peña F., Gutiérrez-Lerma A. I., Quiroz-Baez R., Arias C., The role of β -amyloid protein in synaptic function: implications for Alzheimer's disease therapy. Current Neuropharmacology 2006 4 2 149 163 2-s2.0-33646570823 10.2174/157015906776359531
4. Selkoe D. J., Alzheimer's disease is a synaptic failure. Science 2002 298 5594 789 791 2-s2.0-0037174618 10.1126/science.1074069
5. Babiloni C., Pievani M., Vecchio F., Geroldi C., Eusebi F., Fracassi C., Fletcher E., De Carli C., Boccardi M., Rossini P. M., Frisoni G. B., White-matter lesions along the cholinergic tracts are related to cortical sources of eeg rhythms in amnesic mild cognitive impairment. Human Brain Mapping 2009 30 5 1431 1443 2-s2.0-66149102861 10.1002/hbm.20612
6. Klein W. L., Krafft G. A., Finch C. E., Targeting small A β oligomers: the solution to an Alzheimer's disease conundrum? Trends in Neurosciences 2001 24 4 219 224 2-s2.0-0035297712 10.1016/S0166-2236(00)01749-5
7. Ondrejcak T., Klyubin I., Hu N.-W., Barry A. E., Cullen W. K., Rowan M. J., Alzheimer's disease amyloid β -protein and synaptic function. NeuroMolecular Medicine 2010 12 1 13 26 2-s2.0-77952499447 10.1007/s12017-009- 8091-0
8. Peña-Ortega F., Amyloid β -protein and neural network dysfunction. Journal of Neurodegenerative Diseases 2013 2013 8 657470 10.1155/2013/657470
9. Adaya-Villanueva A., Ordaz B., Balleza-Tapia H., Márquez-Ramos A., Peña-Ortega F., β -like hippocampal network activity is differentially affected by amyloid β peptides. Peptides 2010 31 9 1761 1766 2-s2.0-77955654861 10.1016/j.peptides.2010.06.003
10. Iwatsubo T., Odaka A., Suzuki N., Mizusawa H., Nukina N., Ihara Y., Visualization of A β 42(43) and A β 40 in senile plaques with end-specific A β monoclonals: evidence that an initially deposited species is A β 42(43). Neuron 1994 13 1 45 53 2-s2.0-0028169925 10.1016/0896-6273(94)90458-8
11. Güntert A., Döbeli H., Bohrmann B., High sensitivity analysis of amyloid- β peptide composition in amyloid deposits from human and PS2APP mouse brain. Neuroscience 2006 143 2 461 475 2-s2.0-33750825049 10.1016/j.neuroscience.2006.08.027
12. Pike C. J., Walencewicz-Wasserman A. J., Kosmoski J., Cribbs D. H., Glabe C. G., Cotman C. W., Structure-activity analyses of β -amyloid peptides: contributions of the β 25-35 region to aggregation and neurotoxicity. Journal of Neurochemistry 1995 64 1 253 265 2-s2.0-0028981219
13. 26]A β 25-35/40) and fragment presence in the brains of Alzheimer's patients. Journal of Neuroscience Research 2002 70 3 474 483 2-s2.0-0037010292 10.1002/jnr.10391
14. Gruden M. A., Davudova T. B., Mališauskas M., Zamotin V. V., Sewell R. D. E., Voskresenskaya N. I., Kostanyan I. A., Sherstnev V. V., Morozova-Roche L. A., Autoimmune responses to amyloid structures of A β 25-35 peptide and human lysozyme in the serum of patients with progressive Alzheimer's disease. Dementia and Geriatric Cognitive Disorders 2004 18 2 165 171 2-s2.0-4344641184 10.1159/000079197
15. Kaneko I., Morimoto K., Kubo T., Drastic neuronal loss in vivo by β -amyloid racemized at Ser26 residue: conversion of non-toxic [D-Ser26] β -amyloid 1-40 to toxic and proteinase-resistant fragments. Neuroscience 2001 104 4 1003 1011 2-s2.0-0035800012 10.1016/S0306-4522(01)00155-5
16. Yankner B. A., Duffy L. K., Kirschner D. A., Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Science 1990 250 4978 279 282 2-s2.0-0024990330
17. Mattson M. P., Cheng B., Davis D., Bryant K., Lieberburg I., Rydel R. E., β -Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. Journal of Neuroscience 1992 12 2 376 389 2-s2.0-0026570528
18. Sun M.-K., Alkon D. L., Impairment of hippocampal CA1 heterosynaptic transformation and spatial memory by β -amyloid25-35. Journal of Neurophysiology 2002 87 5 2441 2449 2-s2.0-0036082750
19. Peña F., Ordaz B., Balleza-Tapia H., Bernal-Pedraza R., Márquez-Ramos A., Carmona-Aparicio L., Giordano M., β -amyloid protein (25-35) disrupts hippocampal network activity: role of Fyn-kinase. Hippocampus 2010 20 1 78 96 2-s2.0-75149170925 10.1002/hipo.20592
20. Delobette S., Privat A., Maurice T., In vitro aggregation facilitates β -amyloid peptide-(25-35)-induced amnesia in the rat. European Journal of Pharmacology 1997 319 1 1 4 2-s2.0-0031566854
21. Freir D. B., Herron C. E., Nicotine enhances the depressive actions of A β 1-40 on long-term potentiation in the rat hippocampal CA1 region in vivo. Journal of Neurophysiology 2003 89 6 2917 2922 2-s2.0-0038581893 10.1152/jn.00996.2002
22. Freir D. B., Costello D. A., Herron C. E., A β 25-35 -induced depression of long-term potentiation in area CA1 in vivo and in vitro is attenuated by verapamil. Journal of Neurophysiology 2003 89 6 3061 3069 2-s2.0-0037603598 10.1152/jn.00992.2002
23. Grace E. A., Rabiner C. A., Busciglio J., Characterization of neuronal dystrophy induced by fibrillar amyloid β: implications for Alzheimer's disease. Neuroscience 2002 114 1 265 273 2-s2.0-0037130570 10.1016/S0306- 4522(02)00241-5
24. Holscher C., Gengler S., Gault V. A., Harriott P., Mallot H. A., Soluble β -amyloid[25-35] reversibly impairs hippocampal synaptic plasticity and spatial learning. European Journal of Pharmacology 2007 561 1-3 85 90 2-s2.0-33947262557 10.1016/j.ejphar.2007.01.040
25. Maurice T., Lockhart B. P., Privat A., Amnesia induced in mice by centrally administered β -amyloid peptides involves cholinergic dysfunction. Brain Research 1996 706 2 181 193 2-s2.0-0030048606 10.1016/0006-8993(95)01032-7
26. Stepanichev M. Y., Zdobnova I. M., Zarubenko I. I., Moiseeva Y. V., Lazareva N. A., Onufriev M. V., Gulyaeva N. V., A β 25-35 -induced memory impairments correlate with cell loss in rat hippocampus. Physiology and Behavior 2004 80 5 647 655 2-s2.0-1242337336 10.1016/j.physbeh.2003.11.003
27. Tohda C., Matsumoto N., Zou K., Meselhy M. R., Komatsu K., A β 25-35 -induced memory impairment, axonal atrophy, and synaptic loss are ameliorated by MI, A metabolite of protopanaxadiol-type saponins. Neuropsychopharmacology 2004 29 5 860 868 2-s2.0-1942420868 10.1038/sj.npp.1300388
28. Yamaguchi Y., Kawashima S., Effects of amyloid- β -(25-35) on passive avoidance, radial-arm maze learning and choline acetyltransferase activity in the rat. European Journal of Pharmacology 2001 412 3 265 272 2-s2.0-0035793310 10.1016/S0014-2999(01)00730-0
29. Rönicke R., Klemm A., Meinhardt J., Schröder U. H., Fändrich M., Reymann K. G., A Β mediated diminution of MTT reduction-an artefact of single cell culture? PLoS ONE 2008 3 9 2-s2.0-52449104067 10.1371/journal.pone.0003236 e3236
30. Hiruma H., Katakura T., Takahashi S., Ichikawa T., Kawakami T., Glutamate and amyloid β -protein rapidly inhibit fast axonal transport in cultured rat hippocampal neurons by different mechanisms. Journal of Neuroscience 2003 23 26 8967 8977 2-s2.0-0141864562
31. 2+ concentration in cultured rat microglia. European Journal of Pharmacology 1995 288 2 125 130 2-s2.0-0028981610
32. Driver J. E., Racca C., Cunningham M. O., Towers S. K., Davies C. H., Whittington M. A., LeBeau F. E. N., Impairment of hippocampal gamma (γ)-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). European Journal of Neuroscience 2007 26 5 1280 1288 2-s2.0-34548321410 10.1111/j.1460-9568.2007.05705.x
33. Villette V., Poindessous-Jazat F., Simon A., Léna C., Roullot E., Bellessort B., Epelbaum J., Dutar P., Stéphan A., Decreased rhythmic GABAergic septal activity and memory-associated θ oscillations after hippocampal amyloid- β pathology in the rat. Journal of Neuroscience 2010 30 33 10991 11003 2-s2.0-77955860261 10.1523/JNEUROSCI.6284-09.2010
34. Peña-Ortega F., Bernal-Pedraza R., Amyloid β peptide slows down sensory-induced hippocampal oscillations. International Journal of Peptides 2012 2012 8 236289 10.1155/2012/236289
35. Bland B. H., Colom L. V., Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Progress in Neurobiology 1993 41 2 157 208 2-s2.0-0027225382 10.1016/0301-0082(93)90007-F
36. Kahana M. J., Seelig D., Madsen J. R., Theta returns. Current Opinion in Neurobiology 2001 11 6 739 744 2-s2.0-0035660897 10.1016/S0959-4388(01)00278-1
37. Kahana M. J., The cognitive correlates of human brain oscillations. Journal of Neuroscience 2006 26 6 1669 1672 2-s2.0-32544449459 10.1523/JNEUROSCI.3737-05c.2006
38. Klimesch W., EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Research Reviews 1999 29 2-3 169 195 2-s2.0-0032907015 10.1016/S0165-0173(98)00056-3
39. Griffin A. L., Asaka Y., Darling R. D., Berry S. D., Theta-contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behavioral Neuroscience 2004 118 2 403 411 2-s2.0-1842479429 10.1037/0735-7044.118.2.403
40. McNaughton N., Ruan M., Woodnorth M.-A., Restoring theta-like rythmicity in rats restores initial learning in the Morris water maze. Hippocampus 2006 16 12 1102 1110 2-s2.0-33846033919 10.1002/hipo.20235
41. Nakashiba T., Buhl D. L., McHugh T. J., Tonegawa S., Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 2009 62 6 781 787 2-s2.0-67249123597 10.1016/j.neuron.2009.05.013
42. Kahana M. J., Sekuler R., Caplan J. B., Kirschen M., Madsen J. R., Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 1999 399 6738 781 784 2-s2.0-0033600286 10.1038/21645
43. Cornwell B. R., Johnson L. L., Holroyd T., Carver F. W., Grillon C., Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. Journal of Neuroscience 2008 28 23 5983 5990 2-s2.0-44949242629 10.1523/JNEUROSCI.5001-07. 2008
44. Babiloni C., Cassetta E., Binetti G., Tombini M., Del Percio C., Ferreri F., Ferri R., Frisoni G., Lanuzza B., Nobili F., Parisi L., Rodriguez G., Frigerio L., Gurzì M., Prestia A., Vernieri F., Eusebi F., Rossini P. M., Resting EEG sources correlate with attentional span in mild cognitive impairment and Alzheimer's disease. European Journal of Neuroscience 2007 25 12 3742 3757 2-s2.0-34347373077 10.1111/j.1460-9568.2007.05601.x
45. Cummins T. D. R., Broughton M., Finnigan S., Theta oscillations are affected by amnestic mild cognitive impairment and cognitive load. International Journal of Psychophysiology 2008 70 1 75 81 2-s2.0-51249114963 10.1016/j.ijpsycho.2008.06.002
46. Wang J., Ikonen S., Gurevicius K., Van Groen T., Tanila H., Alteration of cortical EEG in mice carrying mutated human APP transgene. Brain Research 2002 943 2 181 190 2-s2.0-0037067796 10.1016/S0006-8993(02)02617-3
47. Wisor J. P., Edgar D. M., Yesavage J., Ryan H. S., Mccormick C. M., Lapustea N., Murphy G. M. Jr., Sleep and circadian abnormalities in a transgenic mouse model of Alzheimer's disease: a role for cholinergic transmission. Neuroscience 2005 131 2 375 385 2-s2.0-13544275103 10.1016/j.neuroscience.2004. 11.018
48. Akay M., Wang K., Akay Y. M., Dragomir A., Wu J., Nonlinear dynamical analysis of carbachol induced hippocampal oscillations in mice. Acta Pharmacologica Sinica 2009 30 6 859 867 2-s2.0-67549150771 10.1038/aps.2009.66
49. Platt B., Drever B., Koss D., Stoppelkamp S., Jyoti A., Plano A., Utan A., Merrick G., Ryan D., Melis V., Wan H., Mingarelli M., Porcu E., Scrocchi L., Welch A., Riedel G., Abnormal cognition, sleep, eeg and brain metabolism in a novel knock-in alzheimer mouse, plb1. PLoS ONE 2011 6 11 2-s2.0-80855156783 10.1371/journal.pone.0027068 e27068
50. Scott L., Feng J., Kiss T., Needle E., Atchison K., Kawabe T. T., Age-dependent disruption in hippocampal theta oscillation in amyloid- β overproducing transgenic mice. Neurobiol Aging 2012 33 e13 e23
51. Colom L. V., Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease. Journal of Neurochemistry 2006 96 3 609 623 2-s2.0-33645105539 10.1111/j.1471-4159.2005.03630.x
52. Shin J., Theta rhythm heterogeneity in humans. Clinical Neurophysiology 2010 121 3 456 457 2-s2.0-75449086510 10.1016/j.clinph.2009.12.008
53. Pálhalmi J., Paulsen O., Freund T. F., Hájos N., Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 2004 47 3 381 389 2-s2.0-3242661823 10.1016/j.neuropharm.2004.04.010
54. Reich C. G., Karson M. A., Karnup S. V., Jones L. M., Alger B. E., Regulation of IPSP theta rhythm by muscarinic receptors and endocannabinoids in hippocampus. Journal of Neurophysiology 2005 94 6 4290 4299 2-s2.0-28044441822 10.1152/jn.00480.2005
55. Cullen K. M., Halliday G. M., Double K. L., Brooks W. S., Creasey H., Broe G. A., Cell loss in the nucleus basalis is related to regional cortical atrophy in Alzheimer's disease. Neuroscience 1997 78 3 641 652 2-s2.0-0030887764 10.1016/S0306-4522(96)00569-6
56. Auld D. S., Kornecook T. J., Bastianetto S., Quirion R., Alzheimer's disease and the basal forebrain cholinergic system: relations to β -amyloid peptides, cognition, and treatment strategies. Progress in Neurobiology 2002 68 3 209 245 2-s2.0-0036810329 10.1016/S0301-0082(02)00079-5
57. Klingner M., Apelt J., Kumar A., Sorger D., Sabri O., Steinbach J., Scheunemann M., Schliebs R., Alterations in cholinergic and non-cholinergic neurotransmitter receptor densities in transgenic Tg2576 mouse brain with β -amyloid plaque pathology. International Journal of Developmental Neuroscience 2003 21 7 357 369 2-s2.0-0242383891 10.1016/j.ijdevneu.2003.08.001
58. Lüth H.-J., Apelt J., Ihunwo A. O., Arendt T., Schliebs R., Degeneration of β -amyloid-associated cholinergic structures in transgenic APPSW mice. Brain Research 2003 977 1 16 22 2-s2.0-0038360763 10.1016/S0006-8993(03)02658-1
59. Ikarashi Y., Harigaya Y., Tomidokoro Y., Kanai M., Ikeda M., Matsubara E., Kawarabayashi T., Kuribara H., Younkin S. G., Maruyama Y., Shoji M., Decreased level of brain acetylcholine and memory disturbance in APPsw mice. Neurobiology of Aging 2004 25 4 483 490 2-s2.0-12144286749 10.1016/S0197- 4580(03)00122-2
60. Ma X., Ye W., Mei Z., Change of cholinergic transmission and memory deficiency induced by injection of β -amyloid protein into NBM of rats. Science in China Series C 2001 44 4 435 442 2-s2.0-0034835219
61. Fang L., Duan J., Ran D., Fan Z., Yan Y., Huang N., Amyloid- β depresses excitatory cholinergic synaptic transmission in Drosophila. Neuroscience Bulletin 2012 28 585 594
62. Balleza-Tapia H., Huanosta-Gutiérrez A., Márquez-Ramos A., Arias N., Peña F., Amyloid β oligomers decrease hippocampal spontaneous network activity in an age-dependent manner. Current Alzheimer Research 2010 7 5 453 462 2-s2.0-78549243744 10.2174/156720510791383859
63. Leão R. N., Colom L. V., Borgius L., Kiehn O., Fisahn A., Medial septal dysfunction by A β -induced KCNQ channel-block in glutamatergic neurons. Neurobiology of Aging 2012 33 2046 2061 2-s2.0-80052409489 10.1016/j.neurobiolaging.2011.07.013
64. Colom L. V., Castañeda M. T., Bañuelos C., Puras G., García-Hernández A., Hernandez S., Mounsey S., Benavidez J., Lehker C., Medial septal β -amyloid 1-40 injections alter septo-hippocampal anatomy and function. Neurobiology of Aging 2010 31 1 46 57 2-s2.0-70449524669 10.1016/j.neurobiolaging.2008.05.006
65. Mugantseva E. A., Podolski I. Y., Animal model of Alzheimer's disease: characteristics of EEG and memory. Central European Journal of Biology 2009 4 4 507 514 2-s2.0-76149104899 10.2478/s11535-009-0054-9
66. β (N-40, N-42) oligomers in normal and Alzheimer disease brains. Journal of Biological Chemistry 1996 271 8 4077 4081 2-s2.0-0029671451 10.1074/jbc.271.8. 4077
67. Klunk W. E., Lopresti B. J., Ikonomovic M. D., Lefterov I. M., Koldamova R. P., Abrahamson E. E., Debnath M. L., Holt D. P., Huang G.-F., Shao L., DeKosky S. T., Price J. C., Mathis C. A., Binding of the positron emission tomography tracer Pittsburgh Compound-B reflects the amount of amyloid- β in Alzheimer's Disease brain but not in transgenic mouse brain. Journal of Neuroscience 2005 25 46 10598 10606 2-s2.0-27944471285 10.1523/JNEUROSCI.2990- 05.2005
68. Matsui T., Ingelsson M., Fukumoto H., Ramasamy K., Kowa H., Frosch M. P., Irizarry M. C., Hyman B. T., Expression of APP pathway mRNAs and proteins in Alzheimer's disease. Brain Research 2007 1161 1 116 123 2-s2.0-34447527687 10.1016/j.brainres.2007.05.050
69. Ikonomovic M. D., Klunk W. E., Abrahamson E. E., Mathis C. A., Price J. C., Tsopelas N. D., Lopresti B. J., Ziolko S., Bi W., Paljug W. R., Debnath M. L., Hope C. E., Isanski B. A., Hamilton R. L., DeKosky S. T., Post-mortem correlates of in vivo PiB-PET amyloid imaging in a typical case of Alzheimer's disease. Brain 2008 131 6 1630 1645 2-s2.0-43849083580 10.1093/brain/awn016
70. Steinerman J. R., Irizarry M., Scarmeas N., Raju S., Brandt J., Albert M., Blacker D., Hyman B., Stern Y., Distinct pools of β -amyloid in Alzheimer disease-affected brain: a clinicopathologic study. Archives of Neurology 2008 65 7 906 912 2-s2.0-47549088485 10.1001/archneur.65.7.906
71. Dewachter I., Van Dorpe J., Smeijers L., Gilis M., Kuipéri C., Laenen I., Caluwaerts N., Moechars D., Checler F., Vanderstichele H., Van Leuven F., Aging increased amyloid peptide and caused amyloid plaques in brain of old APP/V717I transgenic mice by a different mechanism than mutant presenilin1. Journal of Neuroscience 2000 20 17 6452 6458 2-s2.0-0034280437
72. Praticó D., Uryu K., Sung S., Tang S., Trojanowski J. Q., Lee V. M.-Y., Aluminum modulates brain amyloidosis through oxidative stress in APP transgenic mice. The FASEB Journal 2002 16 9 1138 1140 2-s2.0-0036634409
73. Lee J.-Y., Friedman J. E., Angel I., Kozak A., Koh J.-Y., The lipophilic metal chelator DP-109 reduces amyloid pathology in brains of human β -amyloid precursor protein transgenic mice. Neurobiology of Aging 2004 25 10 1315 1321 2-s2.0-4644238758 10.1016/j.neurobiolaging.2004.01.005
74. Jankowsky J. L., Younkin L. H., Gonzales V., Fadale D. J., Slunt H. H., Lester H. A., Younkin S. G., Borchelt D. R., Rodent A β modulates the solubility and distribution of amyloid deposits in transgenic mice. Journal of Biological Chemistry 2007 282 31 22707 22720 2-s2.0-34547960783 10.1074/jbc.M611050200
75. Shinkai Y., Yoshimura M., Morishima-Kawashima M., Ito Y., Shimada H., Yanagisawa K., Ihara Y., Amyloid β -protein deposition in the leptomeninges and cerebral cortex. Annals of Neurology 1997 42 6 899 908 2-s2.0-0031442299 10.1002/ana.410420612
76. Wang J., Dickson D. W., Trojanowski J. Q., Lee V. M.-Y., The levels of soluble versus insoluble brain a β distinguish Alzheimer's disease from normal and pathologic aging. Experimental Neurology 1999 158 2 328 337 2-s2.0-0032837741 10.1006/exnr.1999.7085
77. Fonte J., Miklossy J., Atwood C., Martins R., The severity of cortical Alzheimer's type changes is positively correlated with increased amyloid- β levels: resolubilization of amyloid- β with transition metal ion chelators. Journal of Alzheimer's Disease 2001 3 2 209 219 2-s2.0-0034987999
78. Patton R. L., Kalback W. M., Esh C. L., Kokjohn T. A., Van Vickle G. D., Luehrs D. C., Kuo Y.-M., Lopez J., Brune D., Ferrer I., Masliah E., Newel A. J., Beach T. G., Castaño E. M., Roher A. E., Amyloid- β peptide remnants in AN-1792-immunized Alzheimer's disease patients: a biochemical analysis. American Journal of Pathology 2006 169 3 1048 1063 2-s2.0-33748767945 10.2353/ajpath.2006.060269
79. Bates K. A., Verdile G., Li Q.-X., Ames D., Hudson P., Masters C. L., Martins R. N., Clearance mechanisms of Alzheimer's amyloid- Β peptide: implications for therapeutic design and diagnostic tests. Molecular Psychiatry 2009 14 5 469 486 2-s2.0-67349093525 10.1038/mp.2008.96
80. Gregory G. C., Halliday G. M., What is the dominant a β species in human brain tissue? A review. Neurotoxicity Research 2005 7 1-2 29 41 2-s2.0-15844394507 10.1007/BF03033774
81. Peña F., Alavez-Pérez N., Epileptiform activity induced by pharmacologic reduction of M-current in the developing hippocampus in vitro. Epilepsia 2006 47 1 47 54 2-s2.0-33645020074 10.1111/j.1528-1167.2006.00369.x
82. Fellous J. M., Sejnowski T. J., Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands. Hippocampus 2000 10 187 197
83. Wíniewski K., Car H., (S)-3,5-DHPG: a review. CNS Drug Reviews 2002 8 1 101 116 2-s2.0-0036078428
84. Buzsáki G., Theta oscillations in the hippocampus. Neuron 2002 33 3 325 340 2-s2.0-0037204104 10.1016/S0896-6273(02)00586-X
85. Shin J., Kim D., Bianchi R., Wong R. K. S., Shin H.-S., Genetic dissection of theta rhythm heterogeneity in mice. Proceedings of the National Academy of Sciences of the United States of America 2005 102 50 18165 18170 2-s2.0-29144480496 10.1073/pnas.0505498102
86. Nobili F., Copello F., Vitali P., Prastaro T., Carozzo S., Perego G., Rodriguez G., Timing of disease progression by quantitative EEG in Alzheimer's patients. Journal of Clinical Neurophysiology 1999 16 6 566 573 2-s2.0-0032748821
87. Jyoti A., Plano A., Riedel G., Platt B., EEG, activity, and sleep architecture in a transgenic A β PPswe/PSEN1A246E Alzheimer's disease mouse. Journal of Alzheimer's Disease 2010 22 873 887
88. LaFerla F. M., Green K. N., Oddo S., Intracellular amyloid- β in Alzheimer's disease. Nature Reviews Neuroscience 2007 8 7 499 509 2-s2.0-34250819839 10.1038/nrn2168
89. Verret L., Mann E. O., Hang G. B., Barth A. M. I., 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 3 708 721 2-s2.0-84860334015 10.1016/j.cell.2012.02.046
90. Chen G. J., Xiong Z., Yan Z., A β impairs nicotinic regulation of inhibitory synaptic transmission and interneuron excitability in prefrontal cortex. Molecular Neurodegeneration 2013 8, article 3
91. Rubio S. E., Vega-Flores G., Martinez A., Bosch C., Perez-Mediavilla A., del Rio J., Accelerated aging of the GABAergic septohippocampal pathway and decreased hippocampal rhythms in a mouse model of Alzheimer's disease. The FASEB Journal 2012 26 4458 4467
92. Chapman C. A., Lacaille J.-C., Cholinergic induction of theta-frequency oscillations in hippocampal inhibitory interneurons and pacing of pyramidal cell firing. Journal of Neuroscience 1999 19 19 8637 8645 2-s2.0-0033216128
93. Felder C. C., Muscarinic acetylcholine receptors: signal transduction through multiple effectors. The FASEB Journal 1995 9 8 619 625 2-s2.0-0029013930
94. Huang H.-M., Ou H.-C., Hsieh S.-J., Amyloid β peptide impaired carbachol but not glutamate-mediated phosphoinositide pathways in cultured rat cortical neurons. Neurochemical Research 2000 25 2 303 312 2-s2.0-0034081045 10.1023/A:1007592007956
95. Janickova H., Rudajev V., Zimcik P., Jakubik J., Tanila H., El-Fakahany E. E., Uncoupling of M1 muscarinic receptor/G-protein interaction by amyloid β 1-42. Neuropharmacology 2013 67 272 283
96. Dahlgren K. N., Manelli A. M., Blaine Stine W. Jr., Baker L. K., Krafft G. A., Ladu M. J., Oligomeric and fibrillar species of amyloid- β peptides differentially affect neuronal viability. Journal of Biological Chemistry 2002 277 35 32046 32053 2-s2.0-0037200117 10.1074/jbc.M201750200
97. McGowan E., Pickford F., Kim J., Onstead L., Eriksen J., Yu C., Skipper L., Murphy M. P., Beard J., Das P., Jansen K., DeLucia M., Lin W.-L., Dolios G., Wang R., Eckman C. B., Dickson D. W., Hutton M., Hardy J., Golde T., A β 42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron 2005 47 2 191 199 2-s2.0-22544482926 10.1016/j.neuron.2005.06.030
98. Bitan G., Kirkitadze M. D., Lomakin A., Vollers S. S., Benedek G. B., Teplow D. B., Amyloid β -protein (A β) assembly: A β 40 and A β 42 oligomerize through distinct pathways. Proceedings of the National Academy of Sciences of the United States of America 2003 100 1 330 335 2-s2.0-0037422540 10.1073/pnas.222681699
99. Sandberg A., Luheshi L. M., Söllvander S., De Barros T. P., Macao B., Knowles T. P. J., Biverstål H., Lendel C., Ekholm-Petterson F., Dubnovitsky A., Lannfelt L., Dobson C. M., Härd T., Stabilization of neurotoxic Alzheimer amyloid- β oligomers by protein engineering. Proceedings of the National Academy of Sciences of the United States of America 2010 107 35 15595 15600 2-s2.0-77957257176 10.1073/pnas.1001740107
100. Lin H., Bhatia R., Lal R., Amyloid β protein forms ion channels: implications for Alzheimer's disease pathophysiology. The FASEB Journal 2001 15 13 2433 2444 2-s2.0-0035159553 10.1096/fj.01-0377com Acadiamico