Cited by 71Alzheimer's disease research and treatmentsNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

Altered Theta Oscillations and Aberrant Cortical Excitatory Activity in the 5XFAD Model of Alzheimer’s Disease

Open access
Siwek, Magdalena Elisabeth, Müller, Ralf, Henseler, Christina, Trog, Astrid, Lundt, Andreas, Wormuth, Carola, Broich, Karl, Ehninger, Dan +2 more·2015·Neural Plasticity

Abstract

Alzheimer’s disease (AD) is an age-related neurodegenerative disorder characterized by impairment of memory function. The 5XFAD mouse model was analyzed and compared with wild-type (WT) controls for aberrant cortical excitability and hippocampal theta oscillations by using simultaneous video-electroencephalogram (EEG) monitoring. Seizure staging revealed that 5XFAD mice exhibited cortical hyperexcitability whereas controls did not. In addition, 5XFAD mice displayed a significant increase in hippocampal theta activity from the light to dark phase during nonmotor activity. We also observed a reduction in mean theta frequency in 5XFAD mice compared to controls that was again most prominent during nonmotor activity. Transcriptome analysis of hippocampal probes and subsequent qPCR validation revealed an upregulation of Plcd4 that might be indicative of enhanced muscarinic signalling. Our results suggest that 5XFAD mice exhibit altered cortical excitability, hippocampal dysrhythmicity, and potential changes in muscarinic signaling.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1155/2015/781731

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 98 · Cited by 71

Research works printed but not linked: 88

  1. [1]Scott L. Feng J. Kiss T. Age-dependent disruption in hippocampal theta oscillation in amyloid-β overproducing transgenic mice Neurobiology of Aging 2012 33 7 1481.e13 1481.e23 10.1016/j.neurobiolaging.2011.12.010 2-s2.0-84861114070 22227005 · DOI
  2. [2]Yamaguchi H. Hirai S. Morimatsu M. Shoji M. Nakazato Y. Diffuse type of senile plaques in the cerebellum of Alzheimer-type dementia demonstrated by β protein immunostain Acta Neuropathologica 1989 77 3 314 319 10.1007/bf00687584 2-s2.0-0024561561 2466390 · DOI
  3. [3]Selkoe D. J. Alzheimer's disease is a synaptic failure Science 2002 298 5594 789 791 10.1126/science.1074069 2-s2.0-0037174618 12399581 · DOI · Paper page
  4. [4]Selkoe D. J. Schenk D. Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics Annual Review of Pharmacology and Toxicology 2003 43 545 584 2-s2.0-0001181116 10.1146/annurev.pharmtox.43.100901.140248 12415125 · DOI
  5. [5]Ashe K. H. Learning and memory in transgenic mice modeling Alzheimer's disease Learning and Memory 2001 8 6 301 308 10.1101/lm.43701 2-s2.0-0035674312 11773429 · DOI · Paper page
  6. [6]Eriksen J. L. Janus C. G. Plaques, tangles, and memory loss in mouse models of neurodegeneration Behavior Genetics 2007 37 1 79 100 10.1007/s10519-006-9118-z 2-s2.0-33846466652 17072762 · DOI · Paper page
  7. [7]Glenner G. G. Wong C. W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein Biochemical and Biophysical Research Communications 1984 120 3 885 890 2-s2.0-0021256895 10.1016/s0006-291x(84)80190-4 6375662 · DOI · Paper page
  8. [8]Glenner G. G. Wong C. W. Quaranta V. Eanes E. D. The amyloid deposits in Alzheimer's disease: their nature and pathogenesis Applied Pathology 1984 2 6 357 369 2-s2.0-0021572660 6242724
  9. [9]Ohno M. Cole S. L. Yasvoina M. BACE1 gene deletion prevents neuron loss and memory deficits in 5XFAD APP/PS1 transgenic mice Neurobiology of Disease 2007 26 1 134 145 10.1016/j.nbd.2006.12.008 2-s2.0-33947247360 17258906 PMC1876698 · DOI · Paper page
  10. [10]Duff K. Suleman F. Transgenic mouse models of Alzheimer's disease: how useful have they been for therapeutic development? Briefings in Functional Genomics & Proteomics 2004 3 1 47 59 10.1093/bfgp/3.1.47 2-s2.0-11344294035 15163359 · DOI
  11. [11]Torres-Aleman I. Toward a comprehensive neurobiology of IGF-I Developmental Neurobiology 2010 70 5 384 396 10.1002/dneu.20778 2-s2.0-77949741721 20186710 · DOI
  12. [12]Devi L. Ohno M. Deletion of the eIF2α kinase GCN2 fails to rescue the memory decline associated with Alzheimer's disease PLoS ONE 2013 8 10 e77335 10.1371/journal.pone.0077335 2-s2.0-84885398154 PMC3795630 24146979 · DOI
  13. [13]Sinha S. Anderson J. P. Barbour R. Purification and cloning of amyloid precursor protein β-secretase from human brain Nature 1999 402 6761 537 540 2-s2.0-0033518251 10.1038/990114 10591214 · DOI · Paper page
  14. [14]Vassar R. Bennett B. D. Babu-Khan S. β-Secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE Science 1999 286 5440 735 741 10.1126/science.286.5440.735 2-s2.0-0033595706 10531052 · DOI · Paper page
  15. [16]Ohno M. Sametsky E. A. Younkin L. H. BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease Neuron 2004 41 1 27 33 10.1016/s0896-6273(03)00810-9 2-s2.0-0346055155 14715132 · DOI · Paper page
  16. [17]Crouzin N. Baranger K. Cavalier M. Area-specific alterations of synaptic plasticity in the 5XFAD mouse model of Alzheimer's disease: dissociation between somatosensory cortex and hippocampus PLoS ONE 2013 8 9 e74667 2-s2.0-84884254543 10.1371/journal.pone.0074667 PMC3775744 24069328 · DOI
  17. [19]Rockenstein E. M. McConlogue L. Tan H. Power M. Masliah E. Mucke L. Levels and alternative splicing of amyloid β protein precursor (APP) transcripts in brains of APP transgenic mice and humans with Alzheimer's disease The Journal of Biological Chemistry 1995 270 47 28257 28267 10.1074/jbc.270.47.28257 2-s2.0-0028875687 7499323 · DOI
  18. [20]Goutagny R. Krantic S. Hippocampal oscillatory activity in Alzheimer's disease: toward the identification of early biomarkers? Aging and Disease 2013 4 3 134 140 23730529 PMC3660123
  19. [22]Casas C. Sergeant N. Itier J.-M. Massive CA1/2 neuronal loss with intraneuronal and N-terminal truncated Abeta42 accumulation in a novel Alzheimer transgenic model The American Journal of Pathology 2004 165 4 1289 1300 10.1016/s0002-9440(10)63388-3 2-s2.0-4644276796 15466394 PMC1618627 · DOI · Paper page
  20. [24]Kaczorowski C. C. Disterhoft J. F. Memory deficits are associated with impaired ability to modulate neuronal excitability in middle-aged mice Learning and Memory 2009 16 6 362 366 2-s2.0-66349124196 10.1101/lm.1365609 19470651 PMC2704100 · DOI
  21. [26]Kim K. H. Moon M. Yu S.-B. Mook-Jung I. Kim J.-I. RNA-Seq analysis of frontal cortex and cerebellum from 5XFAD mice at early stage of disease pathology Journal of Alzheimer's Disease 2012 29 4 793 808 10.3233/JAD-2012-111793 2-s2.0-84860124906 22507954 · DOI
  22. [27]Blanchet P. J. Antipsychotic drug-induced movement disorders Canadian Journal of Neurological Sciences 2003 30 supplement 1 S101 S107 10.1017/s0317167100003309 2-s2.0-0037349634 12691483 · DOI
  23. [28]Martino D. Giovannoni G. Antibasal ganglia antibodies and their relevance to movement disorders Current Opinion in Neurology 2004 17 4 425 432 10.1097/01.wco.0000137532.76491.19 2-s2.0-4043083344 15247537 · DOI
  24. [29]Palop J. J. Chin J. Mucke L. A network dysfunction perspective on neurodegenerative diseases Nature 2006 443 7113 768 773 10.1038/nature05289 2-s2.0-33750339228 17051202 · DOI
  25. [31]Palop J. J. Chin J. Roberson E. D. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease Neuron 2007 55 5 697 711 10.1016/j.neuron.2007.07.025 2-s2.0-34548264782 17785178 PMC8055171 · DOI · Paper page
  26. [32]Buzsáki G. Theta oscillations in the hippocampus Neuron 2002 33 3 325 340 2-s2.0-0037204104 10.1016/S0896-6273(02)00586-X 11832222 · DOI · Paper page
  27. [33]Colom L. V. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease Journal of Neurochemistry 2006 96 3 609 623 10.1111/j.1471-4159.2005.03630.x 2-s2.0-33645105539 16405497 · DOI
  28. [34]Chin J. Scharfman H. E. Shared cognitive and behavioral impairments in epilepsy and Alzheimer's disease and potential underlying mechanisms Epilepsy and Behavior 2013 26 3 343 351 10.1016/j.yebeh.2012.11.040 2-s2.0-84875263668 23321057 PMC3924321 · DOI
  29. [35]Minkeviciene R. Rheims S. Dobszay M. B. Amyloid induced neuronal hyperexcitability triggers progressive epilepsy-induced neuronal hyperexcitability triggers progressive epilepsy The Journal of Neuroscience 2009 29 11 3453 3462 10.1523/jneurosci.5215-08.2009 2-s2.0-63849180498 19295151 PMC6665248 · DOI
  30. [36]Verret L. Mann E. O. Hang G. B. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model Cell 2012 149 3 708 721 10.1016/j.cell.2012.02.046 2-s2.0-84860334015 22541439 PMC3375906 · DOI · Paper page
  31. [37]Mendez M. F. Lim G. T. H. Seizures in elderly patients with dementia: epidemiology and management Drugs and Aging 2003 20 11 791 803 10.2165/00002512-200320110-00001 2-s2.0-0141761520 12964886 · DOI
  32. [38]Larner A. J. Epileptic seizures in AD patients NeuroMolecular Medicine 2010 12 1 71 77 10.1007/s12017-009-8076-z 2-s2.0-77952510145 19557550 · DOI
  33. [39]Scarmeas N. Honig L. S. Choi H. Seizures in Alzheimer disease: who, when, and how common? Archives of Neurology 2009 66 8 992 997 2-s2.0-68549089091 10.1001/archneurol.2009.130 19667221 PMC2768279 · DOI
  34. [40]Morrison J. H. Hof P. R. Life and death of neurons in the aging brain Science 1997 278 5337 412 419 10.1126/science.278.5337.412 2-s2.0-0030698871 9334292 · DOI · Paper page
  35. [41]Price J. L. Ko A. I. Wade M. J. Tsou S. K. McKeel D. W. Morris J. C. Neuron number in the entorhinal cortex and CA1 in preclinical alzheimer disease Archives of Neurology 2001 58 9 1395 1402 10.1001/archneur.58.9.1395 2-s2.0-0034849725 11559310 · DOI · Paper page
  36. [42]Terry R. D. Masliah E. Salmon D. P. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Annals of Neurology 1991 30 4 572 580 10.1002/ana.410300410 2-s2.0-0025987048 1789684 · DOI · Paper page
  37. [44]Romanelli M. F. Morris J. C. Ashkin K. Coben L. A. Advanced Alzheimer's disease is a risk factor for late-onset seizures Archives of Neurology 1990 47 8 847 850 10.1001/archneur.1990.00530080029006 2-s2.0-0024996068 2375689 · DOI
  38. [45]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 10.1016/s0301-0082(02)00079-5 2-s2.0-0036810329 12450488 · DOI
  39. [46]Cullen K. M. Perivascular astrocytes within Alzheimer's disease plaques NeuroReport 1997 8 8 1961 1966 10.1097/00001756-199705260-00033 2-s2.0-0030847015 9223085 · DOI
  40. [47]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 15275827 · DOI
  41. [48]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 10.1152/jn.00480.2005 2-s2.0-28044441822 16093334 · DOI
  42. [49]Gutiérrez-Lerma A. I. Ordaz B. Peña-Ortega F. Amyloid beta peptides differentially affect hippocampal theta rhythms in vitro International Journal of Peptides 2013 2013 11 328140 10.1155/2013/328140 2-s2.0-84880169704 PMC3708430 23878547 · DOI
  43. [50]Ikarashi Y. Harigaya Y. Tomidokoro Y. Decreased level of brain acetylcholine and memory disturbance in APPsw mice Neurobiology of Aging 2004 25 4 483 490 10.1016/s0197-4580(03)00122-2 2-s2.0-12144286749 15013569 · DOI
  44. [51]Klingner M. Apelt J. Kumar A. 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 10.1016/j.ijdevneu.2003.08.001 2-s2.0-0242383891 14599482 · DOI
  45. [52]Kordower J. H. Chu Y. Stebbins G. T. Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment Annals of Neurology 2001 49 2 202 213 10.1002/1531-8249(20010201)49:260;202::aid-ana4062;3.3.co;2-v 11220740 · DOI
  46. [53]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 12788508 · DOI
  47. [54]Babiloni C. Frisoni G. B. Pievani M. White matter vascular lesions are related to parietal-to-frontal coupling of EEG rhythms in mild cognitive impairment Human Brain Mapping 2008 29 12 1355 1367 10.1002/hbm.20467 2-s2.0-55849121761 17979121 PMC6870662 · DOI
  48. [55]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 10.1016/j.ijpsycho.2008.06.002 2-s2.0-51249114963 18652854 · DOI
  49. [56]Peña-Ortega F. Bernal-Pedraza R. Amyloid beta peptide slows down sensory-induced hippocampal oscillations International Journal of Peptides 2012 2012 8 236289 10.1155/2012/236289 2-s2.0-84879191897 PMC3350957 22611415 · DOI
  50. [57]Babiloni C. Cassetta E. Binetti G. Resting EEG sources correlate with attentional span in mild cognitive impairment and Alzheimer's disease European Journal of Neuroscience 2007 25 12 3742 3757 10.1111/j.1460-9568.2007.05601.x 2-s2.0-34347373077 17610594 · DOI
  51. [58]Weiergräber M. Henry M. Hescheler J. Smyth N. Schneider T. Electrocorticographic and deep intracerebral EEG recording in mice using a telemetry system Brain Research Protocols 2005 14 3 154 164 2-s2.0-15944418924 10.1016/j.brainresprot.2004.12.006 15795169 · DOI
  52. [59]Kramer K. Kinter L. B. Evaluation and applications of radiotelemetry in small laboratory animals Physiological Genomics 2003 13 3 197 205 10.1152/physiolgenomics.00164.2002 2-s2.0-0038387496 12746464 · DOI
  53. [60]Kronland-Martinet R. Morlet J. Grossmann A. Analysis of sound patterns through wavelet transforms International Journal of Pattern Recognition and Artificial Intelligence 1987 1 2 273 302 10.1142/s0218001487000205 · DOI
  54. [61]Montgomery S. M. Buzsáki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance Proceedings of the National Academy of Sciences of the United States of America 2007 104 36 14495 14500 10.1073/pnas.0701826104 2-s2.0-35448999715 17726109 PMC1964875 · DOI
  55. [62]Müller R. Struck H. Ho M. S. P. Atropine-sensitive hippocampal theta oscillations are mediated by Cav2.3 R-type Ca2+ channels Neuroscience 2012 205 125 139 10.1016/j.neuroscience.2011.12.032 2-s2.0-84858002841 22240250 · DOI
  56. [63]Huang D. W. Sherman B. T. Lempicki R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nature Protocols 2009 4 1 44 57 10.1038/nprot.2008.211 2-s2.0-61449172037 19131956 · DOI · Paper page
  57. [64]Huang D. W. Sherman B. T. Lempicki R. A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Research 2009 37 1 1 13 10.1093/nar/gkn923 2-s2.0-58549112996 19033363 PMC2615629 · DOI · Paper page
  58. [65]Schmittgen T. D. Livak K. J. Analyzing real-time PCR data by the comparative CT method Nature Protocols 2008 3 6 1101 1108 10.1038/nprot.2008.73 2-s2.0-44949231424 18546601 · DOI · Paper page
  59. [66]Hochberg Y. A sharper Bonferroni procedure for multiple tests of significance Biometrika 1988 75 4 800 802 2-s2.0-33645762226 10.1093/biomet/75.4.800 MR995126 · DOI · Paper page
  60. [68]Jelic V. Johansson S.-E. Almkvist O. Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer's disease Neurobiology of Aging 2000 21 4 533 540 10.1016/s0197-4580(00)00153-6 2-s2.0-0034622247 10924766 · DOI
  61. [69]van der Hiele K. Vein A. A. van der Welle A. EEG and MRI correlates of mild cognitive impairment and Alzheimer's disease Neurobiology of Aging 2007 28 9 1322 1329 10.1016/j.neurobiolaging.2006.06.006 2-s2.0-34447572927 16854500 · DOI
  62. [70]Czigler B. Csikós D. Hidasi Z. Quantitative EEG in early Alzheimer's disease patients—power spectrum and complexity features International Journal of Psychophysiology 2008 68 1 75 80 10.1016/j.ijpsycho.2007.11.002 2-s2.0-40849142223 18093675 · DOI
  63. [71]Moretti V. D. Pievani M. Geroldi C. EEG markers discriminate among different subgroup of patients with mild cognitive impairment American Journal of Alzheimer's Disease and Other Dementias 2010 25 1 58 73 10.1177/1533317508329814 2-s2.0-77749277377 PMC10845572 19204371 · DOI
  64. [72]Noebels J. A perfect storm: converging paths of epilepsy and Alzheimer's dementia intersect in the hippocampal formation Epilepsia 2011 52 supplement 1 39 46 10.1111/j.1528-1167.2010.02909.x 2-s2.0-78651278360 PMC3058398 21214538 · DOI
  65. [74]Lalonde R. Dumont M. Staufenbiel M. Strazielle C. Neurobehavioral characterization of APP23 transgenic mice with the SHIRPA primary screen Behavioural Brain Research 2005 157 1 91 98 2-s2.0-11144294808 10.1016/j.bbr.2004.06.020 15617775 · DOI
  66. [75]Moechars D. Lorent K. de Strooper B. Dewachter I. Van Leuven F. Expression in brain of amyloid precursor protein mutated in the α-secretase site causes disturbed behavior, neuronal degeneration and premature death in transgenic mice The EMBO Journal 1996 15 6 1265 1274 2-s2.0-0029917041 8635459 PMC450029
  67. [76]Kumar V. B. Farr S. A. Flood J. F. Site-directed antisense oligonucleotide decreases the expression of amyloid precursor protein and reverses deficits in learning and memory in aged SAMP8 mice Peptides 2000 22 12 1769 1775 2-s2.0-0034867485 11150636
  68. [77]Steinbach J. P. Müller U. Leist M. Li Z.-W. Nicotera P. Aguzzi A. Hypersensitivity to seizures in β-amyloid precursor protein deficient mice Cell Death & Differentiation 1998 5 10 858 866 10.1038/sj.cdd.4400391 2-s2.0-0031731261 10203685 · DOI
  69. [78]Hu Y.-S. Xu P. Pigino G. Brady S. T. Larson J. Lazarov O. Complex environment experience rescues impaired neurogenesis, enhances synaptic plasticity, and attenuates neuropathology in familial Alzheimer's disease-linked APPswe/PS1ΔE9 mice The FASEB Journal 2010 24 6 1667 1681 2-s2.0-77953506502 10.1096/fj.09-136945 20086049 PMC4050966 · DOI
  70. [79]Pandis D. Scarmeas N. Seizures in alzheimer disease: clinical and epidemiological data Epilepsy Currents 2012 12 5 184 187 10.5698/1535-7511-12.5.184 2-s2.0-84870314387 23118603 PMC3482722 · DOI
  71. [80]de Lanerolle N. C. Kim J. H. Robbins R. J. Spencer D. D. Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy Brain Research 1989 495 2 387 395 10.1016/0006-8993(89)90234-5 2-s2.0-0024412565 2569920 · DOI
  72. [81]Sutula T. Cascino G. Cavazos J. Parada I. Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe Annals of Neurology 1989 26 3 321 330 10.1002/ana.410260303 2-s2.0-0024444281 2508534 · DOI
  73. [82]Minkeviciene R. Ihalainen J. Malm T. Age-related decrease in stimulated glutamate release and vesicular glutamate transporters in APP/PS1 transgenic and wild-type mice Journal of Neurochemistry 2008 105 3 584 594 10.1111/j.1471-4159.2007.05147.x 2-s2.0-42449107478 18042177 · DOI
  74. [83]Jin K. Peel A. L. Mao X. O. Increased hippocampal neurogenesis in Alzheimer's disease Proceedings of the National Academy of Sciences of the United States of America 2004 101 1 343 347 2-s2.0-0346458659 10.1073/pnas.2634794100 14660786 PMC314187 · DOI · Paper page
  75. [84]Amatniek J. C. Hauser W. A. DelCastillo-Castaneda C. Incidence and predictors of seizures in patients with Alzheimer's disease Epilepsia 2006 47 5 867 872 10.1111/j.1528-1167.2006.00554.x 2-s2.0-33745258377 16686651 · DOI
  76. [85]Westmark C. J. Westmark P. R. Beard A. M. Hildebrandt S. M. Malter J. S. Seizure susceptibility and mortality in mice that over-express amyloid precursor protein International Journal of Clinical and Experimental Pathology 2008 1 2 157 168 18784809 PMC2480559
  77. [86]Womelsdorf T. Schoffelen J.-M. Oostenveld R. Modulation of neuronal interactions through neuronal synchronization Science 2007 316 5831 1609 1612 10.1126/science.1139597 2-s2.0-34250856329 17569862 · DOI · Paper page
  78. [87]McNaughton N. Ruan M. Woodnorth M.-A. Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze Hippocampus 2006 16 12 1102 1110 10.1002/hipo.20235 2-s2.0-33846033919 17068783 · DOI
  79. [88]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 10.1073/pnas.0505498102 2-s2.0-29144480496 16330775 PMC1306792 · DOI
  80. [89]Bland B. H. Trepel C. Oddie S. D. Kirk I. J. Intraseptal microinfusion of muscimol: effects on hippocampal formation theta field activity and phasic Theta-ON cell discharges Experimental Neurology 1996 138 2 286 297 10.1006/exnr.1996.0067 2-s2.0-0029937821 8620927 · DOI
  81. [90]Berry S. D. Rinaldi P. C. Thompson R. F. Verzeano M. Analysis of temporal relations among units and slow waves in rabbit hippocampus Brain Research Bulletin 1978 3 5 509 518 10.1016/0361-9230(78)90080-1 2-s2.0-0018124084 122716 · DOI
  82. [91]Jeewajee A. Lever C. Burton S. O'Keefe J. Burgess N. Environmental novelty is signaled by reduction of the hippocampal theta frequency Hippocampus 2008 18 4 340 348 10.1002/hipo.20394 2-s2.0-42149170120 18081172 PMC2678674 · DOI
  83. [92]Felder C. C. Muscarinic acetylcholine receptors: signal transduction through multiple effectors The FASEB Journal 1995 9 8 619 625 2-s2.0-0029013930 7768353
  84. [93]Huang H.-M. Ou H.-C. Hsieh S.-J. Amyloid beta peptide impaired carbachol but not glutamate-mediated phosphoinositide pathways in cultured rat cortical neurons Neurochemical Research 2000 25 2 303 312 10.1023/A:1007592007956 2-s2.0-0034081045 10786716 · DOI
  85. [94]Kuzmiski J. B. Barr W. Zamponi G. W. MacVicar B. A. Topiramate inhibits the initiation of plateau potentials in CA1 neurons by depressing R-type calcium channels Epilepsia 2005 46 4 481 489 10.1111/j.0013-9580.2005.35304.x 2-s2.0-16344368695 15816941 · DOI
  86. [95]Tai C. Kuzmiski J. B. MacVicar B. A. Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons The Journal of Neuroscience 2006 26 23 6249 6258 10.1523/jneurosci.1009-06.2006 2-s2.0-33745621938 16763032 PMC6675200 · DOI
  87. [96]Shin J. Gireesh G. Kim S.-W. Phospholipase C β4 in the medial septum controls cholinergic theta oscillations and anxiety behaviors The Journal of Neuroscience 2009 29 49 15375 15385 10.1523/jneurosci.3126-09.2009 2-s2.0-71849097133 20007462 PMC6666097 · DOI
  88. [97]Jansen R. Timmerman J. Loos M. Novel candidate genes associated with hippocampal oscillations PLoS ONE 2011 6 10 e26586 10.1371/journal.pone.0026586 2-s2.0-80055107941 PMC3204991 22066001 · DOI

Authors
Siwek, M. E., Müller, R., Henseler, C., Trog, A., Lundt, A., Wormuth, C., Broich, K., Ehninger, D., Weiergräber, M., & Papazoglou, A.
Affiliations
  • Federal Institute for Drugs and Medical Devices (DE)
  • University of Cologne (DE)
  • University of Bonn (DE)
  • German Center for Neurodegenerative Diseases (DE)
Corresponding author
Weiergräber, Marco
Venue
Neural Plasticity
Publisher
Wiley
Published
2015
Volume
2015
Pages
1-17
ISSN
  • 1687-5443 (ISSN-L)
  • 2090-5904
OpenAlex
W1996001613
Cited by
71
References
98
Citations by year
2026: 2 · 2025: 3 · 2024: 11 · 2023: 6 · 2022: 9 · 2021: 11 · 2020: 6 · 2019: 6 · 2018: 5 · 2017: 7 · 2016: 4 · 2015: 1
FWCI
4.17
Type
journal article
Language
en
Open access
Locations
  • Neural Plasticity (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • DZNE Pub (submittedVersion, other-oa)
Funders
Federal Institute for Drugs and Medical Devices
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
Alzheimer's disease, 5xFAD mice, hippocampal theta oscillations, cortical excitability, cortical hyperexcitability, circadian rhythm, theta frequency, muscarinic signaling, hippocampal transcriptome
MeSH terms
Alzheimer Disease, Animals, Cerebral Cortex, Disease Models, Animal, Electroencephalography, Female, Hippocampus, Male, Mice, Transgenic, Motor Activity, Seizures, Theta Rhythm, Gene Expression, Amyloid beta-Protein Precursor, Mice, Presenilin-1

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review