Emergence of early alterations in network oscillations and functional connectivity in a tau seeding mouse model of Alzheimer’s disease pathology

Ahnaou, A.; Moechars, D.; Raeymaekers, L.; Biermans, R.; Manyakov, N. V.; Bottelbergs, A.; Wintmolders, C.; Van Kolen, K.; Van De Casteele, T.; Kemp, J. A.; Drinkenburg, W. H.

doi:10.1038/s41598-017-13839-6

Cited by 99Alzheimer's disease research and treatmentsNeural dynamics and brain functionDementia and Cognitive Impairment Research

Emergence of early alterations in network oscillations and functional connectivity in a tau seeding mouse model of Alzheimer’s disease pathology

Open access

Ahnaou, A., Moechars, D., Raeymaekers, L., Biermans, R., Manyakov, N. V., Bottelbergs, A., Wintmolders, C., Van Kolen, K. +3 more·2017·Scientific Reports

DOI 10.1038/s41598-017-13839-6PMC PMC5660172

Open this paper in CoChat — free account Open PDF

Abstract

Synaptic dysfunction and disconnectivity are core deficits in Alzheimer’s disease (AD), preceding clear changes in histopathology and cognitive functioning. Here, the early and late effects of tau pathology induction on functional network connectivity were investigated in P301L mice. Multichannel EEG oscillations were used to compute (1) coherent activity between the prefrontal cortex (PFC) and hippocampus (HPC) CA1-CA3 networks; (2) phase-amplitude cross frequency coupling (PAC) between theta and gamma oscillations, which is instrumental in adequate cognitive functioning; (3) information processing as assessed by auditory evoked potentials and oscillations in the passive oddball mismatch negativity-like (MMN) paradigm. At the end, the density of tau aggregation and GABA parvalbumin (PV+) interneurons were quantified by immunohistochemistry. Early weakening of EEG theta oscillations and coherent activity were revealed between the PFC and HPC CA1 and drastic impairments in theta–gamma oscillations PAC from week 2 onwards, while PV+ interneurons count was not altered. Moreover, the tau pathology disrupted the MMN complex amplitude and evoked gamma oscillations to standard and deviant stimuli suggesting altered memory formation and recall. The induction of intracellular tau aggregation by tau seed injection results in early altered connectivity and strong theta–gamma oscillations uncoupling, which may be exploited as an early electrophysiological signature of dysfunctional neuronal networks.

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.

Integrity signals

Registry

Crossref · 10.1038/s41598-017-13839-6

Cites

88 of 88 references verified0 citation errors · 0 not checkable

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.

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?

This will reduce sensitivity to incoming connections, reducing effective connectivity.
“This will reduce sensitivity to incoming connections, reducing effective connectivity. 51”
From Alzheimer's disease and its progression reduce pyramidal cell gain and connectivity (2025) · cites this paper as [51]
The Discussion (Coherence; page unavailable) reports decreased hippocampal–prefrontal coherence and hypothesizes reduced information transfer in tau-seeded mice. The Discussion (MMN; page unavailable) also reports reduced responses to auditory stimuli. Neither passage says that reduced sensitivity to incoming connections causes a reduction in effective connectivity; the paper assesses functional connectivity through coherence. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Evoked gamma oscillations to auditory stimuli are disrupted in the tau seeding AD-like model.
“Evoked gamma oscillations to auditory stimuli were also disrupted in this model [23].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [23]
In a tau seeding model with AD-like pathology, theta-gamma phase-amplitude coupling is impaired before neuronal loss or maximum tau pathology.
“Theta-gamma oscillation phaseamplitude cross-frequency coupling was impaired prior to neuronal loss or maximum tau pathology in a tau seeding model with AD-like pathology [23].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [23]

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 Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
Alzheimer's disease: Initial report of the purification and characterization of a novel cerebrovascular amyloid protein
Glenner, G. G., & Wong, C. W. (1984) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(84)80190-4 · Cited by 5,404 · see citing works
Alzheimer's Disease Is a Synaptic Failure
Selkoe, D. J. (2002) · Science · doi:10.1126/science.1074069 · Cited by 4,420 · see citing works
Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI
Greicius, M. D., Srivastava, G., Reiss, A. L., & Menon, V. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308627101 · Cited by 3,684 · see citing works
Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology.
Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., & Binder, L. I. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.13.4913 · Cited by 3,676 · see citing works
Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease
Buckner, R. L., Sepulcre, J., Talukdar, T., Krienen, F. M., Liu, H., Hedden, T., Andrews-Hanna, J. R., Sperling, R. A., & Johnson, K. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5062-08.2009 · Cited by 2,862 · see citing works
High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex
Canolty, R. T., Edwards, E., Dalal, S. S., Soltani, M., Nagarajan, S. S., Kirsch, H. E., Berger, M. S., Barbaro, N. M., & Knight, R. T. (2006) · Science · doi:10.1126/science.1128115 · Cited by 2,650 · see citing works
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606 · see citing works
Untitled work
Bloom (2014) · doi:10.1001/jamaneurol.2013.5847 · Cited by 2,194 · see citing works
Transmission and spreading of tauopathy in transgenic mouse brain
Clavaguera, F., Bolmont, T., Crowther, R. A., Abramowski, D., Frank, S., Probst, A., Fraser, G., Stalder, A. K., Beibel, M., Staufenbiel, M., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1901 · Cited by 1,803 · see citing works
Amyloid-β–induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks
Palop, J. J., & Mucke, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2583 · Cited by 1,651 · see citing works
The theta-gamma neural code
Lisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Modulation of Neuronal Interactions Through Neuronal Synchronization
Womelsdorf, T., Schoffelen, J.-M., Oostenveld, R., Singer, W., Desimone, R., Engel, A. K., & Fries, P. (2007) · Science · doi:10.1126/science.1139597 · Cited by 1,367 · see citing works
Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat
Hoover, W. B., & Vertes, R. P. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0150-4 · Cited by 1,365 · see citing works
EEG dynamics in patients with Alzheimer's disease
Jeong, J. (2004) · Clinical Neurophysiology · doi:10.1016/j.clinph.2004.01.001 · Cited by 1,346 · see citing works
Inhibitory Interneuron Deficit Links Altered Network Activity and Cognitive Dysfunction in Alzheimer Model
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., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.046 · Cited by 1,216 · see citing works
Working memory
Baddeley, A. (2010) · Current Biology · doi:10.1016/j.cub.2009.12.014 · Cited by 1,149 · see citing works
Clusters of Hyperactive Neurons Near Amyloid Plaques in a Mouse Model of Alzheimer’s Disease
Busche, M. A., Eichhoff, G., Adelsberger, H., Abramowski, D., Wiederhold, K.-H., Haass, C., Staufenbiel, M., Konnerth, A., & Garaschuk, O. (2008) · Science · doi:10.1126/science.1162844 · Cited by 1,125 · see citing works
Amyloid Deposition Is Associated with Impaired Default Network Function in Older Persons without Dementia
Sperling, R. A., LaViolette, P. S., O'Keefe, K., O'Brien, J., Rentz, D. M., Pihlajamaki, M., Marshall, G., Hyman, B. T., Selkoe, D. J., Hedden, T., et al. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.003 · Cited by 1,027 · see citing works
Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment
Scheff, S. W., Price, D. A., Schmitt, F. A., & Mufson, E. J. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.09.012 · Cited by 1,017 · see citing works
Rapid appearance and local toxicity of amyloid-β plaques in a mouse model of Alzheimer’s disease
Meyer-Luehmann, M., Spires-Jones, T. L., Prada, C., Garcia-Alloza, M., de Calignon, A., Rozkalne, A., Koenigsknecht-Talboo, J., Holtzman, D. M., Bacskai, B. J., & Hyman, B. T. (2008) · Nature · doi:10.1038/nature06616 · Cited by 987 · see citing works
Neuropathologically defined subtypes of Alzheimer's disease with distinct clinical characteristics: a retrospective study
Murray, M. E., Graff-Radford, N. R., Ross, O. A., Petersen, R. C., Duara, R., & Dickson, D. W. (2011) · The Lancet Neurology · doi:10.1016/s1474-4422(11)70156-9 · Cited by 972 · see citing works
Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD
Dickerson, B. C., Salat, D. H., Greve, D. N., Chua, E. F., Rand-Giovannetti, E., Rentz, D. M., Bertram, L., Mullin, K., Tanzi, R. E., Blacker, D., et al. (2005) · Neurology · doi:10.1212/01.wnl.0000171450.97464.49 · Cited by 910 · see citing works
Neuronal activity regulates the regional vulnerability to amyloid-β deposition
Bero, A. W., Yan, P., Roh, J. H., Cirrito, J. R., Stewart, F. R., Raichle, M. E., Lee, J.-M., & Holtzman, D. M. (2011) · Nature Neuroscience · doi:10.1038/nn.2801 · Cited by 880 · see citing works
Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning
Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P. L., Gioanni, Y., Battaglia, F. P., & Wiener, S. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.013 · Cited by 872 · see citing works
Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy
van Vliet, E. A., da Costa Araujo, S., Redeker, S., van Schaik, R., Aronica, E., & Gorter, J. A. (2007) · Brain · doi:10.1093/brain/awl318 · Cited by 775 · see citing works
Seizures and Epileptiform Activity in the Early Stages of Alzheimer Disease
Vossel, K. A., Beagle, A. J., Rabinovici, G. D., Shu, H., Lee, S. E., Naasan, G., Hegde, M., Cornes, S. B., Henry, M. L., Nelson, A., et al. (2013) · JAMA Neurology · doi:10.1001/jamaneurol.2013.136 · Cited by 730 · see citing works
Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia
Sigurdsson, T., Stark, K. L., Karayiorgou, M., Gogos, J. A., & Gordon, J. A. (2010) · Nature · doi:10.1038/nature08855 · Cited by 702 · see citing works
Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L)
Ramsden, M., Kotilinek, L., Forster, C., Paulson, J., McGowan, E., SantaCruz, K., Guimaraes, A., Yue, M., Lewis, J., Carlson, G., et al. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3279-05.2005 · Cited by 702 · see citing works
Synthetic Tau Fibrils Mediate Transmission of Neurofibrillary Tangles in a Transgenic Mouse Model of Alzheimer's-Like Tauopathy
Iba, M., Guo, J. L., McBride, J. D., Zhang, B., Trojanowski, J. Q., & Lee, V. M.-Y. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2642-12.2013 · Cited by 664 · see citing works
Rhythms of the hippocampal network
Colgin, L. L. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.21 · Cited by 654 · see citing works
Incidence and Predictors of Seizures in Patients with Alzheimer's Disease
Amatniek, J. C., Hauser, W. A., del Castillo–Castañeda, C., Jacobs, D. M., Marder, K. S., Bell, K. L., Albert, M., Brandt, J., & Stern, Y. (2006) · Epilepsia · doi:10.1111/j.1528-1167.2006.00554.x · Cited by 592 · see citing works
Seizure‐Promoting Effect of Blood–Brain Barrier Disruption
Marchi, N., Angelov, L., Masaryk, T., Fazio, V. J., Granata, T., Hernandez, N., Hallene, K. L., Diglaw, T., Franic, L. A., Najm, I., et al. (2007) · Epilepsia · doi:10.1111/j.1528-1167.2007.00988.x · Cited by 508 · see citing works
Clinical assessment of social cognitive function in neurological disorders
Henry, J. D., von Hippel, W., Molenberghs, P., Lee, T., & Sachdev, P. S. (2016) · Nature Reviews Neurology · doi:10.1038/nrneurol.2015.229 · Cited by 488 · see citing works
Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer’s disease
Jelić, V., Johansson, S.-E., Almkvist, O., Shigeta, M., Julin, P., Nordberg, A. K., Winblad, B. G., & Wahlund, L. (2000) · Neurobiology of Aging · doi:10.1016/s0197-4580(00)00153-6 · Cited by 471 · see citing works
Neuroimaging correlates of pathologically-defined atypical Alzheimer’s disease
Whitwell, J. L., Dickson, D., Murray, M., Weigand, S., Tosakulwong, N., Senjem, M., Knopman, D., Boeve, B., Parisi, J., Petersen, R., et al. (2012) · Lancet Neurology · doi:10.1016/s1474-4422(12)70200-4 · Cited by 419 · see citing works
Spatial correlation between brain aerobic glycolysis and amyloid-β (Aβ) deposition
Vlassenko, A. G., Vaishnavi, S. N., Couture, L., Sacco, D., Shannon, B. J., Mach, R. H., Morris, J. C., Raichle, M. E., & Mintun, M. A. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010461107 · Cited by 404 · see citing works
Alzheimer-signature MRI biomarker predicts AD dementia in cognitively normal adults
Dickerson, B. C., Stoub, T. R., Shah, R. C., Sperling, R. A., Killiany, R., Albert, M., Hyman, B. T., Blacker, D., & deToledo‐Morrell, L. (2011) · Neurology · doi:10.1212/wnl.0b013e3182166e96 · Cited by 380 · see citing works
Age-related changes in the default mode network are more advanced in Alzheimer disease
Jones, D. T., Machulda, M. M., Vemuri, P., McDade, E. M., Zeng, G., Senjem, M. L., Gunter, J. L., Przybelski, S. A., Avula, R. T., Knopman, D. S., et al. (2011) · Neurology · doi:10.1212/wnl.0b013e318233b33d · Cited by 370 · see citing works
Brain neural synchronization and functional coupling in Alzheimer's disease as revealed by resting state EEG rhythms
Babiloni, C., Lizio, R., Marzano, N., Capotosto, P., Soricelli, A., Triggiani, A. I., Cordone, S., Gesualdo, L., & Percio, C. D. (2015) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2015.02.008 · Cited by 365 · see citing works
Alzheimer’s pathogenesis: is there neuron-to-neuron propagation?
Braak, H., & Tredici, K. D. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0825-z · Cited by 359 · see citing works
What does gamma coherence tell us about inter-regional neural communication?
Buzsáki, G., & Schomburg, E. W. (2015) · Nature Neuroscience · doi:10.1038/nn.3952 · Cited by 314 · see citing works
Generalized Synchronization of MEG Recordings in Alzheimer’s Disease: Evidence for Involvement of the Gamma Band
Stam, C. J., van Walsum, A. V. C., Pijnenburg, Y. A. L., Berendse, H. W., de Munck, J. C., Scheltens, P., & van Dijk, B. W. (2002) · Journal of Clinical Neurophysiology · doi:10.1097/00004691-200212000-00010 · Cited by 302 · see citing works
Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline
O’Brien, J. L., O’Keefe, K., LaViolette, P. S., DeLuca, A. N., Blacker, D., Dickerson, B. C., & Sperling, R. A. (2010) · Neurology · doi:10.1212/wnl.0b013e3181e3966e · Cited by 297 · see citing works
Changed Conformation of Mutant Tau-P301L Underlies the Moribund Tauopathy, Absent in Progressive, Nonlethal Axonopathy of Tau-4R/2N Transgenic Mice
Terwel, D., Lasrado, R., Snauwaert, J., Vandeweert, E., Haesendonck, C. V., Borghgraef, P., & LEUVEN, F. V. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409876200 · Cited by 267 · see citing works
Ammonia triggers neuronal disinhibition and seizures by impairing astrocyte potassium buffering
Thrane, V. R., Thrane, A. S., Wang, F., Cotrina, M. L., Smith, N., Chen, M. J., Xu, Q., Kang, N., Fujita, T., Nagelhus, E. A., et al. (2013) · Nature Medicine · doi:10.1038/nm.3400 · Cited by 265 · see citing works
Alterations in hippocampal network oscillations and theta–gamma coupling arise before Aβ overproduction in a mouse model of A lzheimer's disease
Goutagny, R., Gu, N., Cavanagh, C., Jackson, J., Chabot, J., Quirion, R., Krantic, S. M., & Williams, S. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12233 · Cited by 264 · see citing works
The mismatch negativity: an index of cognitive decline in neuropsychiatric and neurological diseases and in ageing
Näätänen, R., Kujala, T., Kreegipuu, K., Carlson, S., Escera, C., Baldeweg, T., & Ponton, C. W. (2011) · Brain · doi:10.1093/brain/awr064 · Cited by 246 · see citing works
Advanced Alzheimer's Disease Is a Risk Factor for Late-Onset Seizures
Romanelli, M. F., Morris, J. C., Ashkin, K., & Coben, L. A. (1990) · Archives of Neurology · doi:10.1001/archneur.1990.00530080029006 · Cited by 242 · see citing works
Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gamma oscillations in human scalp-recorded EEG
Friese, U., Köster, M., Hassler, U., Martens, U., Trujillo-Barreto, N., & Gruber, T. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.11.002 · Cited by 233 · see citing works
Seizures in Elderly Patients with Dementia
Mendez, M. F., & Lim, G. T. H. (2003) · Drugs & Aging · doi:10.2165/00002512-200320110-00001 · Cited by 219 · see citing works
Intracerebral injection of preformed synthetic tau fibrils initiates widespread tauopathy and neuronal loss in the brains of tau transgenic mice
Peeraer, E., Bottelbergs, A., Van Kolen, K., Stancu, I.-C., Vasconcelos, B., Mahieu, M., Duytschaever, H., Ver Donck, L., Torremans, A., Sluydts, E., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.08.032 · Cited by 214 · see citing works
Self-citation
Pathological Tau Disrupts Ongoing Network Activity
Menkes-Caspi, N., Yamin, H. G., Kellner, V., Spires-Jones, T. L., Cohen, D., & Stern, E. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.025 · Cited by 184 · see citing works
The basolateral amygdala γ‐aminobutyric acidergic system in health and disease
Prager, E. M., Bergstrom, H. C., Wynn, G. H., & Braga, M. F. M. (2015) · Journal of Neuroscience Research · doi:10.1002/jnr.23690 · Cited by 178 · see citing works
Behavioral and EEG changes in male 5xFAD mice
Schneider, F., Baldauf, K., Wetzel, W., & Reymann, K. G. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.05.041 · Cited by 176 · see citing works
Long-Range Neural Synchrony in Behavior
Harris, A. Z., & Gordon, J. A. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034111 · Cited by 165 · see citing works
Electrophysiological changes precede morphological changes to frontal cortical pyramidal neurons in the rTg4510 mouse model of progressive tauopathy
Crimins, J. L., Rocher, A. B., & Luebke, J. I. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-1038-9 · Cited by 137 · see citing works
Brain imaging in the study of Alzheimer's disease
Reiman, E. M., & Jagust, W. J. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.11.075 · Cited by 134 · see citing works
Amyloid β: linking synaptic plasticity failure to memory disruption in Alzheimer’s disease
Ma, T., & Klann, E. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07506.x · Cited by 131 · see citing works
Neuronal network disintegration: common pathways linking neurodegenerative diseases
Ahmed, R. M., Devenney, E. M., Irish, M., Ittner, A., Naismith, S., Ittner, L. M., Rohrer, J. D., Halliday, G. M., Eisen, A., Hodges, J. R., et al. (2016) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-308350 · Cited by 128 · see citing works
Neural circuits underlying the generation of theta oscillations
Pignatelli, M., Beyeler, A., & Leinekugel, X. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.09.007 · Cited by 124 · see citing works
Epileptic Seizures in AD Patients
Larner, A. J. (2009) · NeuroMolecular Medicine · doi:10.1007/s12017-009-8076-z · Cited by 118 · see citing works
Assessing neuronal networks: Understanding Alzheimer's disease
Bokde, A. L. W., Ewers, M., & Hampel, H. J. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.06.004 · Cited by 117 · see citing works
Decreased Rhythmic GABAergic Septal Activity and Memory-Associated θ Oscillations after Hippocampal Amyloid-β Pathology in the Rat
Villette, V., Poindessous‐Jazat, F., Simon, A., Léna, C., Roullot, E., Bellessort, B., Epelbaum, J., Dutar, P., & Stéphan, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6284-09.2010 · Cited by 116 · see citing works
Clinical management of sleep disturbances in Alzheimer's disease: current and emerging strategies
Urrestarazu, E., & Iriarte, J. (2016) · Nature and Science of Sleep · doi:10.2147/nss.s76706 · Cited by 116 · see citing works
Synaptic activity and Alzheimer's disease: a critical update
Tampellini, D. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00423 · Cited by 105 · see citing works
Slowing of Hippocampal Activity Correlates with Cognitive Decline in Early Onset Alzheimer’s Disease. An MEG Study with Virtual Electrodes
Engels, M. M. A., Hillebrand, A., van der Flier, W. M., Stam, C. J., Scheltens, P., & van Straaten, E. C. W. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00238 · Cited by 103 · see citing works
Auditory Sensory Memory and the Cholinergic System: Implications for Alzheimer's Disease
Pekkonen, E., Hirvonen, J., Jääskeläinen, I. P., Kaakkola, S., & Huttunen, J. (2001) · NeuroImage · doi:10.1006/nimg.2001.0805 · Cited by 102 · see citing works
Transgenic mouse models of Alzheimer's disease: How useful have they been for therapeutic development?
Duff, K. (2004) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/3.1.47 · Cited by 98 · see citing works
Accelerated aging of the GABAergic septohippocampal pathway and decreased hippocampal rhythms in a mouse model of Alzheimer's disease
Rubio, S. E., Vega‐Flores, G., Martínez, A., Bosch, C., Pérez‐Mediavilla, A., Río, J. D., Gruart, A., Delgado‐García, J. M., Soriano, E., & Pascual, M. (2012) · The FASEB Journal · doi:10.1096/fj.12-208413 · Cited by 98 · see citing works
Network Disruption and Cerebrospinal Fluid Amyloid-Beta and Phospho-Tau Levels in Mild Cognitive Impairment
Canuet, L., Pusil, S. A., López, M. E., Bajo, R., Pineda‐Pardo, J. A., Cuesta, P., Gálvez, G., Gaztelu, J. M., Lourido, D., García‐Ribas, G., et al. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0704-15.2015 · Cited by 97 · see citing works
EEG and MRI correlates of mild cognitive impairment and Alzheimer's disease
van der Hiele, K., Vein, A. A., van der Welle, A., van der Grond, J., Westendorp, R. G. J., Bollen, E. L. E. M., van Buchem, M. A., van Dijk, J. G., & Middelkoop, H. A. M. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.06.006 · Cited by 88 · see citing works
Age-dependent disruption in hippocampal theta oscillation in amyloid-β overproducing transgenic mice
Scott, L., Feng, J., Kiss, T., Needle, E., Atchison, K. P., Kawabe, T. T., Milici, A. J., Hajós‐Korcsok, É., Riddell, D. R., & Hajós, M. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.12.010 · Cited by 87 · see citing works
A systematic review of the mismatch negativity as an index for auditory sensory memory: From basic research to clinical and developmental perspectives
Bartha, L., Deuster, D., Giordano, V., Zehnhoff‐Dinnesen, A. A., & Dobel, C. (2015) · Psychophysiology · doi:10.1111/psyp.12459 · Cited by 83 · see citing works
Quantitative assessment of possible age-related change in synaptic numbers in the human frontal cortex
Scheff, S. W., PRICE, D. A., & Sparks, D. L. (2001) · Neurobiology of Aging · doi:10.1016/s0197-4580(01)00222-6 · Cited by 82 · see citing works
Mismatch negativity (MMN) amplitude as a biomarker of sensory memory deficit in amnestic mild cognitive impairment
Lindı́n, M., Correa-Jaraba, K. S., Zurrón, M., & Dı́az, F. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00079 · Cited by 72 · see citing works
Theta oscillations are affected by amnestic mild cognitive impairment and cognitive load
Cummins, T. D. R., Broughton, M., & Finnigan, S. (2008) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2008.06.002 · Cited by 70 · see citing works
Delay of cognitive gamma responses in Alzheimer's disease
Başar, E., Emek‐Savaş, D. D., Güntekin, B., & Yener, G. (2016) · NeuroImage Clinical · doi:10.1016/j.nicl.2016.01.015 · Cited by 70 · see citing works
THE NEURAL CODE
Whitfield, I. C. (1978) · Elsevier eBooks · doi:10.1016/b978-0-12-161904-6.50012-9 · Cited by 69 · see citing works
Amplitude differences of evoked alpha and gamma oscillations in two different age groups
Böttger, D., Herrmann, C. S., & von Cramon, D. Y. (2002) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(02)00031-4 · Cited by 67 · see citing works
Cortical EEG oscillations and network connectivity as efficacy indices for assessing drugs with cognition enhancing potential
Ahnaou, A., Huysmans, H., Jacobs, T., & Drinkenburg, W. H. I. M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.08.015 · Cited by 64 · see citing works
Self-citation
Age-dependent reduction of γ oscillations in the mouse hippocampus in vitro
Vreugdenhil, M., & Toescu, E. C. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.025 · Cited by 50 · see citing works
GABAergic Microcircuits in Alzheimer's Disease Models
Villette, V., & Dutar, P. (2016) · Current Alzheimer Research · doi:10.2174/1567205013666160819125757 · Cited by 49 · see citing works
Functional Connectivity in Elderly Controls and AD Patients Using Resting State fMRI: A Pilot Study
Rombouts, S. A. R. B., & Scheltens, P. (2005) · Current Alzheimer Research · doi:10.2174/1567205053585783 · Cited by 38 · see citing works
Gamma oscillatory activity in relation to memory ability in older adults
Park, J. Y., Lee, K. S., An, S. K., Lee, J., Kim, J., Kim, K. H., & Namkoong, K. (2012) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2012.08.002 · Cited by 30 · see citing works
Amyloid Beta Peptide Slows Down Sensory-Induced Hippocampal Oscillations
Peña‐Ortega, F., & Bernal‐Pedraza, R. (2012) · International Journal of Peptides · doi:10.1155/2012/236289 · Cited by 29 · see citing works
Decreased coherence between the two olfactory bulbs in Alzheimer's disease model mice
Liu, Q., Li, A., Gong, L., Zhang, L., Wu, N., & Xu, F. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.04.023 · Cited by 27 · see citing works

Flagged first, then by citations

Research works printed but not linked: 1

[26]Bell K Albert M Brandt J Stern Y Incidence and predictors of seizures in patients with Alzheimer’s disease Epilepsia 2006 47 867 872 10.1111/j.1528-1167.2006.00554.x 16686651 · DOI

Sorted by citations

Sleep as a Potential Biomarker of Tau and β-Amyloid Burden in the Human Brain
Winer, J. R., Mander, B. A., Helfrich, R. F., Maaß, A., Harrison, T. M., Baker, S. L., Knight, R. T., Jagust, W. J., & Walker, M. P. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0503-19.2019 · Cited by 259 · see citing works
Parvalbumin interneuron vulnerability and brain disorders
Ruden, J. B., Dugan, L. L., & Konradi, C. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-020-0778-9 · Cited by 194 · see citing works
Alzheimer’s disease as a synaptopathy: Evidence for dysfunction of synapses during disease progression
Meftah, S., & Gan, J. (2023) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2023.1129036 · Cited by 197 · see citing works
Neural oscillations and brain stimulation in Alzheimer’s disease
Jafari, Z., Kolb, B. E., & Mohajerani, M. H. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101878 · Cited by 176 · see citing works
GSK3β and tau protein in Alzheimer's disease and epilepsy
Toral-Rios, D., Pichardo-Rojas, P. S., Alonso-Vanegas, M., & Campos-Peña, V. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00019 · Cited by 158 · see citing works
Fast-spiking parvalbumin-positive interneurons in brain physiology and Alzheimer’s disease
Hijazi, S., Smit, A. B., & van Kesteren, R. E. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02168-y · Cited by 144 · see citing works
Neuronal Network Excitability in Alzheimer’s Disease: The Puzzle of Similar versus Divergent Roles of Amyloid β and Tau
Kazim, S. F., Seo, J. H., Bianchi, R., Larson, C. S., Sharma, A., Wong, R. K. S., Gorbachev, K., & Pereira, A. C. (2021) · eNeuro · doi:10.1523/eneuro.0418-20.2020 · Cited by 113 · see citing works
Past, Present, and Future of Non-invasive Brain Stimulation Approaches to Treat Cognitive Impairment in Neurodegenerative Diseases: Time for a Comprehensive Critical Review
Sanches, C., Stengel, C., Godard, J., Mertz, J., Teichmann, M., Migliaccio, R., & Valero‐Cabré, A. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.578339 · Cited by 109 · see citing works
Neurophysiological signatures in Alzheimer’s disease are distinctly associated with TAU, amyloid-β accumulation, and cognitive decline
Ranasinghe, K. G., Cha, J., Iaccarino, L., Hinkley, L. B. N., Beagle, A. J., Pham, J. Q., Jagust, W. J., Miller, B. L., Rankin, K. P., Rabinovici, G. D., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aaz4069 · Cited by 106 · see citing works
Neuroprosthetics: from sensorimotor to cognitive disorders
Gupta, A., Vardalakis, N., & Wagner, F. B. (2023) · Communications Biology · doi:10.1038/s42003-022-04390-w · Cited by 108 · see citing works
The Medial Septum as a Potential Target for Treating Brain Disorders Associated With Oscillopathies
Takeuchi, Y., Nagy, A. J., Barcsai, L., Li, Q., Ohsawa, M., Mizuseki, K., & Berényi, A. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.701080 · Cited by 66 · see citing works
Network Medicine for Alzheimer’s Disease and Traditional Chinese Medicine
Jarrell, J. T., Gao, L., Cohen, D. S., & Huang, X. (2018) · Molecules · doi:10.3390/molecules23051143 · Cited by 67 · see citing works
Theta Oscillations Through Hippocampal/Prefrontal Pathway: Importance in Cognitive Performances
Zangbar, H. S., Ghadiri, T., Vafaee, M. S., Kalan, A. E., Fallahi, S., Ghorbani, M., & Shahabi, P. (2020) · Brain Connectivity · doi:10.1089/brain.2019.0733 · Cited by 58 · see citing works
Differential expression of tau species and the association with cognitive decline and synaptic loss in Alzheimer's disease
Saroja, S. R., Sharma, A., Hof, P. R., & Pereira, A. C. (2021) · Alzheimer s & Dementia · doi:10.1002/alz.12518 · Cited by 45 · see citing works
Intracerebral seeding of amyloid-β and tau pathology in mice: Factors underlying prion-like spreading and comparisons with α-synuclein
McAllister, B. B., Lacoursiere, S. G., Sutherland, R. J., & Mohajerani, M. H. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.01.026 · Cited by 47 · see citing works
Functional Neurophysiological Biomarkers of Early-Stage Alzheimer’s Disease: A Perspective of Network Hyperexcitability in Disease Progression
Tok, S., Ahnaou, A., & Drinkenburg, W. H. I. M. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210397 · Cited by 44 · see citing works
Self-citation
Theta and gamma oscillatory dynamics in mouse models of Alzheimer’s disease: A path to prospective therapeutic intervention
Mehak, S. F., Shivakumar, A. B., Kumari, S., Muralidharan, B., & Gangadharan, G. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104628 · Cited by 42 · see citing works
Neurophysiological assessment of neural network plasticity and connectivity: Progress towards early functional biomarkers for disease interception therapies in Alzheimer’s disease
Walsh, C., Drinkenburg, W. H. I. M., & Ahnaou, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.020 · Cited by 35 · see citing works
Self-citation
Spread of pathological human Tau from neurons to oligodendrocytes and loss of high-firing pyramidal neurons in aging mice
Viney, T. J., Sárkány, B., Ozdemir, A. T., Hartwich, K., Schweimer, J. V., Bannerman, D. M., & Somogyi, P. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111646 · Cited by 34 · see citing works
Entorhinal cortex–hippocampal circuit connectivity in health and disease
Hernández‐Frausto, M., & Vivar, C. (2024) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2024.1448791 · Cited by 34 · see citing works
Reduced synchrony in alpha oscillations during life predicts post mortem neurofibrillary tangle density in early‐onset and atypical Alzheimer's disease
Ranasinghe, K. G., Petersen, C., Kudo, K., Mizuiri, D., Rankin, K. P., Rabinovici, G. D., Gorno‐Tempini, M., Seeley, W. W., Spina, S., Miller, B. L., et al. (2021) · Alzheimer s & Dementia · doi:10.1002/alz.12349 · Cited by 33 · see citing works
Mutual Interactions between Brain States and Alzheimer’s Disease Pathology: A Focus on Gamma and Slow Oscillations
Byron, N., Semenova, A., & Sakata, S. (2021) · Biology · doi:10.3390/biology10080707 · Cited by 31 · see citing works
Local and long-range GABAergic circuits in hippocampal area CA1 and their link to Alzheimer’s disease
Hernández‐Frausto, M., Bilash, O. M., Masurkar, A. V., & Basu, J. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1223891 · Cited by 33 · see citing works
Olfactory impairment in men and mice related to aging and amyloid-induced pathology
Tzeng, W.-Y., Figarella, K., & Garaschuk, O. (2021) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-021-02527-0 · Cited by 27 · see citing works
Peripheral nerve stimulation: A neuromodulation-based approach
Luckey, A. M., Adcock, K. S., & Vanneste, S. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105180 · Cited by 27 · see citing works
Brain-Derived Neurotrophic Factor (BDNF) Preserves the Functional Integrity of Neural Networks in the β-Amyloidopathy Model in vitro
Mitroshina, Е. V., Yarkov, R. S., Mishchenko, T. A., Krut’, V. G., Gavrish, M. S., Epifanova, E. A., Babaev, A. A., & Vedunova, M. V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00582 · Cited by 26 · see citing works
EEG Resting-State Functional Networks in Amnestic Mild Cognitive Impairment
Caravaglios, G., Muscoso, E. G., Blandino, V., Maria, G. D., Gangitano, M., Graziano, F., Guajana, F., & Piccoli, T. (2022) · Clinical EEG and Neuroscience · doi:10.1177/15500594221110036 · Cited by 38 · see citing works
Early Electrophysiological Disintegration of Hippocampal Neural Networks in a Novel Locus Coeruleus Tau-Seeding Mouse Model of Alzheimer’s Disease
Ahnaou, A., Walsh, C., Manyakov, N. V., Youssef, S. A., & Drinkenburg, W. H. I. M. (2019) · Neural Plasticity · doi:10.1155/2019/6981268 · Cited by 24 · see citing works
Self-citation
Glycogen synthase kinase-3: The missing link to aberrant circuit function in disorders of cognitive dysfunction?
Manduca, J. D., Thériault, R.-K., & Perreault, M. L. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2020.104819 · Cited by 21 · see citing works
Cortical hyperexcitability in mouse models and patients with amyotrophic lateral sclerosis is linked to noradrenaline deficiency
Scekic‐Zahirovic, J., Benetton, C., Brunet, A., Ye, X., Logunov, E., Douchamps, V., Megat, S., Andry, V., Kan, V. W. Y., Stuart‐Lopez, G., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.adg3665 · Cited by 21 · see citing works
Relationship between default mode network and resting-state electroencephalographic alpha rhythms in cognitively unimpaired seniors and patients with dementia due to Alzheimer’s disease
Babiloni, C., Lopez, S., Noce, G., Ferri, R., Panerai, S., Catania, V., Soricelli, A., Salvatore, M., Nobili, F. M., Arnaldi, D., et al. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad300 · Cited by 20 · see citing works
Sleep, neuronal hyperexcitability, inflammation and neurodegeneration: Does early chronic short sleep trigger and is it the key to overcoming Alzheimer’s disease?
Ahnaou, A., & Drinkenburg, W. H. I. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.039 · Cited by 23 · see citing works
Self-citation
Neurophysiological trajectories in Alzheimer’s disease progression
Kudo, K., Ranasinghe, K. G., Morise, H., Syed, F., Sekihara, K., Rankin, K. P., Miller, B. L., Kramer, J. H., Rabinovici, G. D., Vossel, K. A., et al. (2024) · eLife · doi:10.7554/elife.91044.3 · Cited by 20 · see citing works
The role of aberrant neural oscillations in the hippocampal-medial prefrontal cortex circuit in neurodevelopmental and neurological disorders
Shing, N., Walker, M. C., & Chang, P. (2022) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2022.107683 · Cited by 19 · see citing works
Coherence in event-related EEG oscillations in patients with Alzheimer’s disease dementia and amnestic mild cognitive impairment
Fide, E., Yerlikaya, D., Güntekin, B., Babiloni, C., & Yener, G. (2022) · Cognitive Neurodynamics · doi:10.1007/s11571-022-09920-0 · Cited by 19 · see citing works
Olfactory bulb stimulation mitigates Alzheimer's‐like disease progression
Salimi, M., Nazari, M., Shahsavar, P., Dehghan, S., Javan, M., Mirnajafi‐Zadeh, J., & Raoufy, M. R. (2024) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.70056 · Cited by 19 · see citing works
Phase-Dependent Deep Brain Stimulation: A Review
Kumari, L. S., & Kouzani, A. Z. (2021) · Brain Sciences · doi:10.3390/brainsci11040414 · Cited by 18 · see citing works
Functional Alterations in the Olfactory Neuronal Circuit Occur before Hippocampal Plasticity Deficits in the P301S Mouse Model of Tauopathy: Implications for Early Diagnosis and Translational Research in Alzheimer’s Disease
Ahnaou, A., Rodriguez-Manrique, D., Biermans, R., Embrechts, S., Manyakov, N. V., & Drinkenburg, W. H. I. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155431 · Cited by 18 · see citing works
Self-citation
Decoding expectation and surprise in dementia: the paradigm of music
Benhamou, E., Zhao, S., Sivasathiaseelan, H., Johnson, J. C. S., Requena‐Komuro, M., Bond, R. L., van Leeuwen, J. E. P., Russell, L. L., Greaves, C. V., Nelson, A., et al. (2021) · Brain Communications · doi:10.1093/braincomms/fcab173 · Cited by 15 · see citing works
Do Brain Oscillations Orchestrate Memory?
Luo, W., & Guan, J. (2018) · Brain Science Advances · doi:10.26599/bsa.2018.9050008 · Cited by 16 · see citing works
Pathological and neurophysiological outcomes of seeding human-derived tau pathology in the APP-KI NL-G-F and NL-NL mouse models of Alzheimer’s Disease
Tok, S., Maurin, H., Delay, C., Crauwels, D., Manyakov, N. V., der Elst, W. V., Moechars, D., & Drinkenburg, W. H. I. M. (2022) · Acta Neuropathologica Communications · doi:10.1186/s40478-022-01393-w · Cited by 13 · see citing works
Self-citation
Hyperphosphorylated Tau Relates to Improved Cognitive Performance and Reduced Hippocampal Excitability in the Young rTg4510 Mouse Model of Tauopathy
Xolalpa-Cueva, L., García-Carlos, C. A., Villaseñor-Zepeda, R., Orta-Salazar, E., Díaz-Miranda, S. Y., Peña‐Ortega, F., Perry, G., & Mondragón‐Rodríguez, S. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215186 · Cited by 14 · see citing works
Linking temporal coordination of hippocampal activity to memory function
Etter, G., Carmichael, J. E., & Williams, S. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1233849 · Cited by 12 · see citing works
Understanding Changes in Hippocampal Interneurons Subtypes in the Pathogenesis of Alzheimer's Disease: A Systematic Review
Reid, H. M. O., Chen-Mack, N., Snowden, T. M., & Christie, B. R. (2021) · Brain Connectivity · doi:10.1089/brain.2020.0879 · Cited by 13 · see citing works
Effects of Pharmacological Treatments in Alzheimer’s Disease: Permutation Entropy-Based EEG Complexity Study
Fide, E., Polat, H., Yener, G., & Özerdem, M. S. (2022) · Brain Topography · doi:10.1007/s10548-022-00927-8 · Cited by 12 · see citing works
Low dose of levetiracetam counteracts amyloid β-induced alterations of hippocampal gamma oscillations by restoring fast-spiking interneuron activity
Isla, A. G., Balleza‐Tapia, H., Chu, F., Chen, G., Johansson, J., Nilsson, P., & Fisahn, A. (2023) · Experimental Neurology · doi:10.1016/j.expneurol.2023.114545 · Cited by 12 · see citing works
A Multiscale Closed-Loop Neurotoxicity Model of Alzheimer’s Disease Progression Explains Functional Connectivity Alterations
Cabrera-Álvarez, J., Stefanovski, L., Martin, L., Susi, G., Maestú, F., & Ritter, P. (2024) · eNeuro · doi:10.1523/eneuro.0345-23.2023 · Cited by 11 · see citing works
The role of neuroinflammation in PV interneuron impairments in brain networks; implications for cognitive disorders
Allami, P., Yazdanpanah, N., & Rezaei, N. (2025) · Reviews in the Neurosciences · doi:10.1515/revneuro-2024-0153 · Cited by 11 · see citing works
Mismatch negativity as EEG biomarker supporting CNS drug development: a transnosographic and translational study
Loïodice, S., Drinkenburg, W. H. I. M., Ahnaou, A., McCarthy, A. P., Viardot, G., Cayre, E., Rion, B., Bertaina‐Anglade, V., Mano, M., L’Hostis, P., et al. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01371-1 · Cited by 11 · see citing works
Self-citation
Fast-spiking parvalbumin-positive interneurons: new perspectives of treatment and future challenges in dementia
Zhang, X., Wu, M., Cheng, L., Cao, W., Liu, Z., Yang, S., & Kim, M. S. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02756-6 · Cited by 11 · see citing works
Aging Alters Olfactory Bulb Network Oscillations and Connectivity: Relevance for Aging-Related Neurodegeneration Studies
Ahnaou, A., Rodriguez-Manrique, D., Embrechts, S., Biermans, R., Manyakov, N. V., Youssef, S. A., & Drinkenburg, W. H. I. M. (2020) · Neural Plasticity · doi:10.1155/2020/1703969 · Cited by 11 · see citing works
Self-citation
Progressive tau aggregation does not alter functional brain network connectivity in seeded hTau.P301L mice
Detrez, J. R., Ben-Nejma, I. R. H., Kolen, K. V., Dam, D. V., Deyn, P. P. D., Fransén, E., Verhoye, M., Timmermans, J., Nuydens, R., der Linden, A. V., et al. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105011 · Cited by 10 · see citing works
Inhibitory interneurons in Alzheimer’s disease
Vargová, G., Vogels, T., Kostecká, Z., & Hromádka, T. (2018) · Bratislavské lekárske listy/Bratislava medical journal · doi:10.4149/bll_2018_038 · Cited by 9 · see citing works
Hyperactivity of subicular parvalbumin interneurons drives early amyloid pathology and cognitive deficits in Alzheimer’s disease
Chen, Y., Jiang, B., Zhuang, K., Wang, H., Peng, H., Zhong, B., Xie, W., Chen, K.-W., Zou, T., Wang, Y., et al. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03217-4 · Cited by 9 · see citing works
Traumatic brain injury alterations in the functional connectome are associated with neuroinflammation but not tau in a P30IL tauopathy mouse model
To, X. V., Soni, N., Medeiros, R., Alateeq, K., & Nasrallah, F. A. (2022) · Brain Research · doi:10.1016/j.brainres.2022.147955 · Cited by 8 · see citing works
Odour Retrieval Processing in Mice: Cholinergic Modulation of Oscillatory Coupling in Olfactory Bulb-Piriform Networks
Ahnaou, A., Chave, L., Manyakov, N. V., & Drinkenburg, W. H. I. M. (2021) · Neuropsychobiology · doi:10.1159/000513511 · Cited by 8 · see citing works
Self-citation
Efficacy of preclinical pharmacological interventions against alterations of neuronal network oscillations in Alzheimer's disease: A systematic review
Isla, A. G., Balleza‐Tapia, H., & Fisahn, A. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113743 · Cited by 9 · see citing works
Sleep Biomarkers Help Predict the Development of Alzheimer Disease
Grigg-Damberger, M. M., & Foldvary-Schaefer, N. (2022) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000818 · Cited by 8 · see citing works
Neurophysiological effects of human-derived pathological tau conformers in the APPKM670/671NL.PS1/L166P amyloid mouse model of Alzheimer’s disease
Tok, S., Maurin, H., Delay, C., Crauwels, D., Manyakov, N. V., der Elst, W. V., Moechars, D., & Drinkenburg, W. H. I. M. (2022) · Scientific Reports · doi:10.1038/s41598-022-11582-1 · Cited by 7 · see citing works
Self-citation
Altered low-frequency brain rhythms precede changes in gamma power during tauopathy
Rodrigues, F. R., Papanikolaou, A., Holeniewska, J., Phillips, K. G., Saleem, A. B., & Solomon, S. G. (2022) · iScience · doi:10.1016/j.isci.2022.105232 · Cited by 7 · see citing works
Neuroadaptation in neurodegenerative diseases: compensatory mechanisms and therapeutic approaches
Kopalli, S. R., Behl, T., Baldaniya, L. H., Ballal, S., Joshi, K. K., Arya, R., Chaturvedi, B., Chauhan, A. S., Verma, R. K., Patel, M., et al. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111375 · Cited by 7 · see citing works
Impaired theta and low-gamma directed information flow in the hippocampal-prefrontal circuit underlies working memory deficits in APP/PS1 mice
Ai, H., Zhang, S., Si, C., Liu, T., Zheng, X., Tian, X., & Bai, W. (2025) · Behavioral and Brain Functions · doi:10.1186/s12993-025-00285-y · Cited by 7 · see citing works
Rethinking parvalbumin: From passive marker to active modulator of hippocampal circuits
Zhang, N., Hu, B., Li, X., & Huang, H. (2025) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2025.10.005 · Cited by 7 · see citing works
Next-generation neurotherapeutics: mechanistic insights on monoclonal antibodies in Alzheimer’s disease
Sharma, A., & Singh, T. G. (2025) · Brain Research · doi:10.1016/j.brainres.2025.150047 · Cited by 6 · see citing works
The Effect of the Optogenetic Stimulation of Astrocytes on Neural Network Activity in an In Vitro Model of Alzheimer’s Disease
Mitroshina, Е. V., Kalinina, E. P., Kalyakulina, A., Teplyakova, A. V., & Vedunova, M. V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252212237 · Cited by 6 · see citing works
Septohippocampal cholinergic system at the intersection of stress and cognition: Current trends and translational implications
Kniffin, A. R., Bangasser, D. A., & Parikh, V. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15999 · Cited by 6 · see citing works
Neurophysiological trajectories in Alzheimer’s disease progression
Kudo, K., Ranasinghe, K. G., Morise, H., Syed, F., Sekihara, K., Rankin, K. P., Miller, B. L., Kramer, J. H., Rabinovici, G. D., Vossel, K. A., et al. (2023) · eLife · doi:10.7554/elife.91044 · Cited by 6 · see citing works
Effects of Memantine on the Spontaneous Firing Frequency of Hippocampal CA1 Pyramidal Neurons in Intact and Alzheimer Rat Model: An Electrophysiological Study
Zamani, N., Moazedi, A. A., Khaki, M. R. A., & Boroujeni, M. P. (2021) · Basic and Clinical Neuroscience Journal · doi:10.32598/bcn.2021.1970.1 · Cited by 5 · see citing works
Preliminary Evidence for Perturbation‐Based tACS‐EEG Biomarkers of Gamma Activity in Alzheimer's Disease
Palmisano, A., Pezanko, L. R., Cappon, D., Tatti, E., Macone, J., Koch, G., Smeralda, C. L., Romanella, S. M., Ruffini, G., Rivolta, D., et al. (2025) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.70025 · Cited by 5 · see citing works
Auditory evoked-potential abnormalities in a mouse model of 22q11.2 Deletion Syndrome and their interactions with hearing impairment
Lu, C., & Linden, J. F. (2025) · Translational Psychiatry · doi:10.1038/s41398-024-03218-x · Cited by 3 · see citing works
Early impairments of visually-driven neuronal ensemble dynamics in the rTg4510 tauopathy mouse model
Parka, A., Degel, C., Dreyer, J. K., Richter, U., Hall, B. J., Bastlund, J. F., Laursen, B., Nedergaard, M., Sotty, F., & Botta, P. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106012 · Cited by 4 · see citing works
Aberrant Cortical Activity in 5xFAD Mice in Response to Social and Non-Social Olfactory Stimuli
Kosel, F., Hartley, M. R., & Franklin, T. B. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-230858 · Cited by 4 · see citing works
Age-Related Modifications of Electroencephalogram Coherence in Mice Models of Alzheimer’s Disease and Amyotrophic Lateral Sclerosis
Vorobyov, V., Деев, А. Д., Chaprov, K., Ustyugov, A. A., & Lysikova, E. A. (2023) · Biomedicines · doi:10.3390/biomedicines11041151 · Cited by 5 · see citing works
Low intensity gamma-frequency TMS safely modulates gamma oscillations in probable mild Alzheimer’s dementia: a randomized 2 × 2 crossover pilot study
Mimenza-Alvarado, A. J., Aguilar-Navarro, S. G., Abarca-Jiménez, I. E., Vázquez-Villaseñor, I., Luna-Umanzor, D. I., Dorard, C., & Villafuerte, G. (2025) · Frontiers in Neurology · doi:10.3389/fneur.2025.1566476 · Cited by 3 · see citing works
Alzheimer's disease and its progression reduce pyramidal cell gain and connectivity
Lanskey, J. H., Jafarian, A., Karadag, M., Kocagoncu, E., Williams, R. S., Yadav, P., Quinn, A. J., Pitt, J., Thayanandan, T., Lowe, S., et al. (2025) · Alzheimer's & Dementia · doi:10.1002/alz.70805 · Cited by 2 · see citing works
Unraveling the link: white matter damage, gray matter atrophy and memory impairment in patients with subcortical ischemic vascular disease
Huang, J., Cheng, R., Liu, X., Chen, L., & Luo, T. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1355207 · Cited by 2 · see citing works
Daily rhythms drive dynamism in sleep, oscillations and interneuron firing, while excitatory firing remains stable across 24 h
Ognjanovski, N., Kim, D., Charlett‐Green, E., Goldiez, E., van Koppen, S., Aton, S. J., & Watson, B. O. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16619 · Cited by 2 · see citing works
From stress to Alzheimer’s: A circuit-based framework for prefrontal cognitive dysfunction
Yi, J. H. (2025) · Neuroscience Letters · doi:10.1016/j.neulet.2025.138424 · Cited by 2 · see citing works
GABAergic activity and gamma oscillations in Alzheimer’s disease and mild cognitive impairment: Neuropathology and therapeutic neuromodulatory insights from animal and human studies
Salehinejad, M. A., & Jouzdani, A. F. (2026) · Brain Network Disorders · doi:10.1016/j.bnd.2026.01.002 · Cited by 2 · see citing works
Sex differences in neuronal oscillatory activity and memory in the methylazoxymethanol acetate model of schizophrenia
Albeely, A. M., Williams, O. O. F., Blight, C. R., Thériault, R.-K., & Perreault, M. L. (2024) · Schizophrenia Research · doi:10.1016/j.schres.2024.04.002 · Cited by 3 · see citing works
EEG-based visual deviance detection in freely behaving mice
Kat, R., van den Berg, B., Perenboom, M. J. L., Schenke, M., van den Maagdenberg, A. M. J. M., Bruining, H., Tolner, E. A., & Kas, M. J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118757 · Cited by 2 · see citing works
Neurophysiological trajectories in Alzheimer's disease progressionPreprint
Kudo, K., Ranasinghe, K. G., Morise, H., Syed, F., Sekihara, K., Rankin, K. P., Miller, B. L., Kramer, J. H., Rabinovici, G. D., Vossel, K. A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.18.541379 · Cited by 2 · see citing works
Longitudinal brain-wide recordings reveal early neurophysiological alterations in memory-impaired mice
Eldaly, A. B. M., Agadagba, S. K., Verma, A., Li, K., Lim, L. W., & Chan, L. L.-H. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.12.035 · Cited by 1 · see citing works
Altered low frequency brain rhythms precede changes in gamma power during tauopathyPreprint
Rodrigues, F. R., Papanikolaou, A., Holeniewska, J., Phillips, K. G., Saleem, A. B., & Solomon, S. G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.03.454865 · Cited by 1 · see citing works
Neurophysiological trajectories in Alzheimer’s disease progressionPreprint
Kudo, K., Ranasinghe, K. G., Morise, H., Syed, F., Sekihara, K., Rankin, K. P., Miller, B. L., Kramer, J. H., Rabinovici, G. D., Vossel, K. A., et al. (2024) · eLife · doi:10.7554/elife.91044.2 · Cited by 1 · see citing works
Altered Low Frequency Brain Rhythms Precede Changes in Gamma Power During TauopathyPreprint
Rodrigues, F. R., Papanikolaou, A., Holeniewska, J., Phillips, K. G., Saleem, A. B., & Solomon, S. G. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4112540
Neurophysiological trajectories in Alzheimer’s disease progressionPreprint
Kudo, K., Ranasinghe, K. G., Morise, H., Syed, F., Sekihara, K., Rankin, K. P., Miller, B. L., Kramer, J. H., Rabinovici, G. D., Vossel, K. A., et al. (2023) · eLife · doi:10.7554/elife.91044.1
[A study on the application of cross-frequency coupling characteristics of neural oscillation in the diagnosis of mild cognitive impairment].
Li, X., Wang, K., Jing, J., Yin, L., Zhang, Y., & Xie, P. (2023) · PubMed Central · doi:10.7507/1001-5515.202210020
Author Response: Neurophysiological trajectories in Alzheimer’s disease progression
Kudo, K., Ranasinghe, K. G., Morise, H., Syed, F., Sekihara, K., Rankin, K. P., Miller, B. L., Kramer, J. H., Rabinovici, G. D., Vossel, K. A., et al. (2024) · eLife · doi:10.7554/elife.91044.2.sa3
Effects of 40 Hz Light Flicker Stimulation on Hippocamp-Prefrontal Neural Activity Characteristics During Working Memory Tasks in AD Model Rats
Liu, S., Wang, L., Li, S., & Xu, G. (2025) · Lecture notes in electrical engineering · doi:10.1007/978-981-96-4067-6_7
Dynamics of structural rearrangements in the entorhinal cortex in rats with various neurocognitive disorders after traumatic brain injury
Mizyakina, К. V., Dzyak, L., & Твердохлеб, И. В. (2025) · Reports of Morphology · doi:10.31393/morphology-journal-2025-31(3)-03
Additional file 1 of Pathological and neurophysiological outcomes of seeding human-derived tau pathology in the APP-KI NL-G-F and NL-NL mouse models of Alzheimer’s Disease
Tok, S., Maurin, H., Delay, C., Crauwels, D., Manyakov, N. V., der Elst, W. V., Moechars, D., & Drinkenburg, W. H. I. M. (2022) · Figshare · doi:10.6084/m9.figshare.20147031
Self-citation
Language impairments in neurodegenerative diseases : function, dysfunction and modulation with transcranial stimulation
Sanches, M. C. P. (2019) · doi:10.70675/23d3688fza2a5z4b5czace8z77e89e074aaf
A computational and technological framework to investigate the effects on neural oscillations of hippocampal electrical stimulation for memory disorders
Vardalakis, N. (2024) · theses.fr (ABES) · doi:10.70675/8e4fb18ezbd56z486ez9d11z50ebb4b67126
The light at the end of the tunnel : study of early-stage brain dynamics alterations in Alzheimer’s disease and beneficial effects of light stimulation in the AppNL-F/MAPT mouse model
Aguilera, M. (2024) · theses.fr (ABES) · doi:10.70675/dc614591zf8f9z4a6dzb174za8a482fa3ece
A novel synaptic compartmentalization failure framework for neurodegeneration
Panigrahi, B. (2026) · Journal of Alzheimer s Disease · doi:10.1177/13872877261449379
Basal forebrain parvalbumin neuron dysfunction links network oscillation deficits to hippocampal pathology in Alzheimer’s diseasePreprint
Hwang, E., Shim, H. S., Kim, S. C., Nam, M., Hyeon, S. J., Kim, H.-J., Kim, J. E., Park, H. J., Woo, J., Hwang, E. M., et al. (2026) · Research Square · doi:10.21203/rs.3.rs-10027900/v1
Forty-hertz auditory stimulation restored hippocampal-prefrontal synchrony and attenuated hippocampal hyperexcitability in an STZ-induced Alzheimer's model
Taei, A. A., Karimani, F., Kaveh, N., Khodabakhsh, P., Dehaqani, M. R. A., & Dargahi, L. (2026) · Experimental Neurology · doi:10.1016/j.expneurol.2026.115931
Exploratory analysis of plasma pTau181 and frontal EEG in young male rugby players with cumulative sport-related concussions
Ahn, S., Yuk, K., Bae, H., Ko, S., Seo, J.-W., Zulkifli, N. A. B., Jiang, S., Jamrasi, P., Chung, S. H., Moon, H. Y., et al. (2026) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2026.07.009

ID 388 – Dynamic alterations of brain network oscillations in a Tau seeding mouse model of Alzheimer’s disease
Ahnaou, A., Raeymaekers, L., Biermans, R., Moechars, D., Peeraer, E., Manyakov, N. V., de Casteele, T. V., Kemp, J. A., & Drinkenburg, W. H. I. M. (2016) · Clinical Neurophysiology · doi:10.1016/j.clinph.2015.11.246
Self-citation
Early Electrophysiological Disintegration of Hippocampal Neural Networks in a Novel Locus Coeruleus Tau-Seeding Mouse Model of Alzheimer’s Disease
Ahnaou, A., Walsh, C., Manyakov, N. V., Youssef, S. A., & Drinkenburg, W. H. I. M. (2019) · Neural Plasticity · doi:10.1155/2019/6981268 · Cited by 24 · see citing works
Self-citation
Functional Alterations in the Olfactory Neuronal Circuit Occur before Hippocampal Plasticity Deficits in the P301S Mouse Model of Tauopathy: Implications for Early Diagnosis and Translational Research in Alzheimer’s Disease
Ahnaou, A., Rodriguez-Manrique, D., Biermans, R., Embrechts, S., Manyakov, N. V., & Drinkenburg, W. H. I. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21155431 · Cited by 18 · see citing works
Self-citation
Alterations in hippocampal network oscillations and theta–gamma coupling arise before Aβ overproduction in a mouse model of A lzheimer's disease
Goutagny, R., Gu, N., Cavanagh, C., Jackson, J., Chabot, J., Quirion, R., Krantic, S. M., & Williams, S. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12233 · Cited by 264 · see citing works
P3‐070: Entorhinal TAU Pathology Decouples Hippocampal and Prefrontal Oscillations Without Impairing Associative Memory
Tanninen, S. E., Nouriziabari, B., Morrissey, M. D., Klein, R. L., & Takehara‐Nishiuchi, K. (2016) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2016.06.1728

Authors: Ahnaou, A., Moechars, D., Raeymaekers, L., Biermans, R., Manyakov, N. V., Bottelbergs, A., Wintmolders, C., Van Kolen, K., Van De Casteele, T., Kemp, J. A., & Drinkenburg, W. H.
Affiliations: Janssen (Belgium) (BE)
Corresponding author: Ahnaou, A.
ORCID: Ahnaou, A.
Manyakov, N. V.
Drinkenburg, W. H.
Venue: Scientific Reports
Publisher: Springer Science and Business Media LLC
Published: 2017-10-27
Volume: 7
Issue: 1
Pages: 14189-14189
ISSN: 2045-2322 (ISSN-L)
DOI: 10.1038/s41598-017-13839-6
PMC: PMC5660172
OpenAlex: W2765707864
Cited by: 98
References: 88
Citations by year: 2026: 5 · 2025: 13 · 2024: 14 · 2023: 16 · 2022: 14 · 2021: 18 · 2020: 11 · 2019: 3 · 2018: 3 · 2016: 1
FWCI: 3.44
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Scientific Reports (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Keywords: Alzheimer's disease, tau pathology, tau seeding, EEG oscillations, functional connectivity, prefrontal cortex, hippocampus, parvalbumin interneurons, mismatch negativity, auditory evoked potentials, synaptic dysfunction, memory impairment, network oscillations
MeSH terms: Alzheimer Disease, Animals, Cognition, Disease Models, Animal, Electroencephalography, gamma-Aminobutyric Acid, Hippocampus, Nerve Net, Neurons, tau Proteins, Prefrontal Cortex, Mice

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

Emergence of early alterations in network oscillations and functional connectivity in a tau seeding mouse model of Alzheimer’s disease pathology

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks