Diminished perisomatic GABAergic terminals on cortical neurons adjacent to amyloid plaques
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One of the main pathological hallmarks of Alzheimer's disease (AD) is the accumulation of plaques in the cerebral cortex, which may appear either in the neuropil or in direct association with neuronal somata. Since different axonal systems innervate the dendritic (mostly glutamatergic) and perisomatic (mostly GABAergic) regions of neurons, the accumulation of plaques in the neuropil or associated with the soma might produce different alterations to synaptic circuits. We have used a variety of conventional light, confocal and electron microscopy techniques to study their relationship with neuronal somata in the cerebral cortex from AD patients and APP/PS1 transgenic mice. The main finding was that the membrane surfaces of neurons (mainly pyramidal cells) in contact with plaques lack GABAergic perisomatic synapses. Since these perisomatic synapses are thought to exert a strong influence on the output of pyramidal cells, their loss may lead to the hyperactivity of the neurons in contact with plaques. These results suggest that plaques modify circuits in a more selective manner than previously thought.
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The course such diseases take is highly variable as the neuropathological changes are not homogenous, neither among patients nor in different regions of the brain of the same patient, giving rise to variation in the alterations to cortical circuits.
“In addition, the course such diseases take is highly variable as the neuropathological changes are not homogenous, neither among patients nor in different regions of the brain of the same patient, giving rise to variation in the alterations to cortical circuits (Garcia-Marin et al., 2009; Blazquez-Llorca et al., 2010).”
From The influence of phospho-tau on dendritic spines of cortical pyramidal neurons in patients with Alzheimer’s disease (2013) · cites this paper as Garcia-Marin et al., 2009
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Cites
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123 · see citing works
Triple-Transgenic Model of Alzheimer’s Disease with Plaques and Tangles
Oddo, S., Caccamo, A., Shepherd, J. D., Murphy, M. P., Golde, T. E., Kayed, R., Metherate, R., Mattson, M. P., Akbari, Y., & LaFerla, F. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00434-3 · Cited by 4,126 · see citing works
Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease
Gómez-Isla, T., Price, J. L., McKeel Jr., D. W., Morris, J. C., Growdon, J. H., & Hyman, B. T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-14-04491.1996 · Cited by 1,796 · see citing works
Intraneuronal Aβ42 Accumulation in Human Brain
Gouras, G. K., Tsai, J., Naslund, J., Vincent, B., Edgar, M., Checler, F., Greenfield, J. P., Haroutunian, V., Buxbaum, J. D., Xu, H., et al. (2000) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64700-1 · Cited by 991 · 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
Colonnier, M. (1968) · Brain Research · doi:10.1016/0006-8993(68)90234-5 · Cited by 946 · see citing works
IRIZARRY, M. C., MCNAMARA, M., FEDORCHAK, K., HSIAO, K., & HYMAN, B. T. (1997) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199709000-00002 · Cited by 649 · see citing works
Spires, T. L., Meyer-Luehmann, M., Stern, E. A., McLean, P. J., Skoch, J., Nguyen, P. T., Bacskai, B. J., & Hyman, B. T. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1879-05.2005 · Cited by 550 · see citing works
D'Andrea, M. R., Nagele, R. G., Wang, H., Peterson, P. A., & Lee, D. H. S. (2001) · Histopathology · doi:10.1046/j.1365-2559.2001.01082.x · Cited by 390 · see citing works
The Development of Amyloid β Protein Deposits in the Aged Brain
Thal, D. R., Capetillo-Zarate, E., Del Tredici, K., & Braak, H. (2006) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2006.6.re1 · Cited by 234 · see citing works
Lighting the chandelier: new vistas for axo-axonic cells
Howard, A., Tamas, G., & Soltesz, I. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.04.004 · Cited by 167 · see citing works
Flagged first, then by citations
Research works printed but not linked: 84
- Allsop D. Haga S. I. Haga C. Ikeda S. I. Mann D. M. Ishii T. (1989). Early senile plaques in Down's syndrome brains show a close relationship with cell bodies of neurons. Neuropathol. Appl. Neurobiol. 15, 531– 542 10.1111/j.1365-2990.1989.tb01252.x 2559339 · DOI
- Amatniek J. C. Hauser W. A. Castillo-Castaneda C. Jacobs D. M. Marder K. Bell K. Albert M. Brandt J. Stern Y. (2006). Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47, 867– 872 10.1111/j.1528-1167.2006.00554.x 16686651 · DOI
- Armstrong R. A. (1995). Factors determining the morphology of beta-amyloid (A beta) deposits in Down's syndrome. Neurodegeneration 4, 179– 186 10.1006/neur.1995.0022 7583682 · DOI
- Arnold S. E. Hyman B. T. Flory J. Damasio A. R. Van Hoesen G. W. (1991). The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cereb. Cortex 1, 103– 116 10.1093/cercor/1.1.103 1822725 · DOI · Paper page
- Bancher C. Brunner C. Lassmann H. Budka H. Jellinger K. Wiche G. Seitelberger F. Grundke-Iqbal I. Iqbal K. Wisniewski H. M. (1989). Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res. 477, 90– 99 10.1016/0006-8993(89)91396-6 2495152 · DOI · Paper page
- Bell K. F. de Kort G. J. Steggerda S. Shigemoto R. Ribeiro-da-Silva A. Cuello A. C. (2003). Structural involvement of the glutamatergic presynaptic boutons in a transgenic mouse model expressing early onset amyloid pathology. Neurosci. Lett. 353, 143– 147 10.1016/j.neulet.2003.09.027 14664921 · DOI
- Blinzinger K. Kreutzberg G. (1968). Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch. Mikrosk. Anat. 85, 145– 157 10.1007/BF00325030 5706753 · DOI
- Brady D. R. Mufson E. J. (1997). Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseased brain. Neuroscience 80, 1113– 1125 10.1016/S0306-4522(97)00068-7 9284064 · DOI · Paper page
- Brendza R. P. Holtzman D. M. (2006). Amyloid-beta immunotherapies in mice and men. Alzheimer Dis. Assoc. Disord. 20, 118– 123 10.1097/01.wad.0000213810.89681.a5 16772748 · DOI
- Brendza R. P. O'Brien C. Simmons K. McKeel D. W. Bales K. R. Paul S. M. Olney J. W. Sanes J. R. Holtzman D. M. (2003). PDAPP; YFP double transgenic mice: a tool to study amyloid-beta associated changes in axonal, dendritic, and synaptic structures. J. Comp. Neurol. 456, 375– 383 10.1002/cne.10536 12532409 · DOI
- Busche M. A. Eichhoff G. Adelsberger H. Abramowski D. Wiederhold K. H. Haass C. Staufenbiel M. Konnerth A. Garaschuk O. (2008). Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321, 1686– 1689 10.1126/science.1162844 18802001 · DOI · Paper page
- Chagnac-Amitai Y. Connors B. W. (1989). Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61, 747– 758 2542471
- Cobb S. R. Buhl E. H. Halasy K. Paulsen O. Somogyi P. (1995). Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75– 78 10.1038/378075a0 7477292 · DOI · Paper page
- Coleman P. Federoff H. Kurlan R. (2004). A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 63, 1155– 1162 15477531
- Cummings B. J. Su J. H. Cotman C. W. White R. Russell M. J. (1993). Beta-amyloid accumulation in aged canine brain: a model of early plaque formation in Alzheimer's disease. Neurobiol. Aging 14, 547– 560 10.1016/0197-4580(93)90038-D 8295657 · DOI
- De Felice F. G. Wu D. Lambert M. P. Fernandez S. J. Velasco P. T. Lacor P. N. Bigio E. H. Jerecic J. Acton P. J. Shughrue P. J. Chen-Dodson E. Kinney G. G. Klein W. L. (2008). Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol. Aging 29, 1334– 1347 10.1016/j.neurobiolaging.2007.02.029 17403556 PMC3142933 · DOI · Paper page
- DeFelipe J. (1999). Chandelier cells and epilepsy. Brain 122, 1807– 1822 10.1093/brain/122.10.1807 10506085 · DOI
- DeFelipe J. (2002). Cortical interneurons: from Cajal to 2001. Prog. Brain Res. 136, 215– 238 10.1016/S0079-6123(02)36019-9 12143384 · DOI
- DeFelipe J. Alonso-Nanclares L. Arellano J. I. Ballesteros-Yáñez I. Benavides-Piccione R. Munoz A. (2007). Specializations of the cortical microstructure of humans. In Evolution of the Nervous Systems: A Comprehensive Reference, Vol. 4. Primates Kaas J. H. Preuss T. M., eds (Amsterdam, Elsevier), pp. 167– 190
- DeFelipe J. Fairen A. (1993). A simple and reliable method for correlative light and electron microscopic studies. J. Histochem. Cytochem. 41, 769– 772 8468459
- DeFelipe J. Fariñas I. (1992). The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39, 563– 607 10.1016/0301-0082(92)90015-7 1410442 · DOI · Paper page
- Delaere P. Duyckaerts C. He Y. Piette F. Hauw J. J. (1991). Subtypes and differential laminar distributions of beta A4 deposits in Alzheimer's disease: relationship with the intellectual status of 26 cases. Acta Neuropathol. 81, 328– 335 10.1007/BF00305876 1711758 · DOI
- Dickson D. W. (1997). The pathogenesis of senile plaques. J. Neuropathol. Exp. Neurol. 56, 321– 339 10.1097/00005072-199704000-00001 9100663 · DOI · Paper page
- Duyckaerts C. Hauw J. J. Bastenaire F. Piette F. Poulain C. Rainsard V. Javoy-Agid F. Berthaux P. (1986). Laminar distribution of neocortical senile plaques in senile dementia of the Alzheimer type. Acta Neuropathol. (Berl.) 70, 249– 256 10.1007/BF00686079 3766125 · DOI
- Eriksen J. L. Janus C. G. (2007). Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav. Genet. 37, 79– 100 10.1007/s10519-006-9118-z 17072762 · DOI · Paper page
- Esiri M. M. Hyman B. T. Beyreuther K. Masters C. L. (1997). Aging and dementia. In Greenfield's Neuropathology, Graham D. I. Lantos P. I., eds (London, Arnold), pp. 153– 233
- Ferrer I. Soriano E. Tunon T. Fonseca M. Guionnet N. (1991). Parvalbumin immunoreactive neurons in normal human temporal neocortex and in patients with Alzheimer's disease. J. Neurol. Sci. 106, 135– 141 10.1016/0022-510X(91)90250-B 1802961 · DOI
- Fonseca M. Soriano E. Ferrer I. Martinez A. Tunon T. (1993). Chandelier cell axons identified by parvalbumin-immunoreactivity in the normal human temporal cortex and in Alzheimer's disease. Neuroscience 55, 1107– 1116 10.1016/0306-4522(93)90324-9 8232900 · DOI
- Glenner G. G. Wong C. W. (1984). Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885– 890 10.1016/S0006-291X(84)80190-4 6375662 · DOI · Paper page
- Glezer I. I. Hof P. R. Leranth C. Morgane P. J. (1993). Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. Cereb. Cortex 3, 249– 272 10.1093/cercor/3.3.249 8324371 · DOI
- Goedert M. Wischik C. M. Crowther R. A. Walker J. E. Klug A. (1988). Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc. Natl. Acad. Sci. U.S.A. 85, 4051– 4055 10.1073/pnas.85.11.4051 3131773 PMC280359 · DOI · Paper page
- Götz J. Deters N. Doldissen A. Bokhari L. Ke Y. Wiesner A. Schonrock N. Ittner L. M. (2007). A decade of tau transgenic animal models and beyond. Brain Pathol. 17, 91– 103 10.1111/j.1750-3639.2007.00051.x 17493043 PMC8095624 · DOI
- Gray E. G. (1959). Electron microscopy of synaptic contacts on dendritic spines of the cerebral cortex. Nature 183, 1592– 1594 10.1038/1831592a0 13666826 · DOI
- Grundke-Iqbal I. Iqbal K. Tung Y.C. Quinlan M. Wisniewski H. M. Binder L. I. (1986). Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U.S.A. 83, 4913– 4917 10.1073/pnas.83.13.4913 3088567 PMC323854 · DOI · Paper page
- Hof P. R. Cox K. Young W. G. Celio M. R. Rogers J. Morrison J. H. (1991). Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 50, 451– 462 10.1097/00005072-199107000-00006 2061713 · DOI
- Hof P. R. Young W. G. Bloom F. E. Belichenko P. V. Celio M. R. (2000a). Comparative Cytoarchitectonic Atlas of the C57BL/6 AND 129/SV Mouse Brains. Amsterdam, Elsevier Science B.V
- Hof P. R. Glezer I. I. Nimchinsky E. A. Erwin J. M. (2000b). Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from primates, cetaceans, and artiodactyls. Brain Behav. Evol. 55, 300– 310 10.1159/000006665 10971015 · DOI
- Ihara Y. Nukina N. Miura R. Ogawara M. (1986). Phosphorylated tau protein is integrated into paired helical filaments in Alzheimer's disease. J. Biochem. (Tokyo) 99, 1807– 1810 2427509
- Irizarry M. C. Soriano F. McNamara M. Page K. J. Schenk D. Games D. Hyman B. T. (1997b). Abeta deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J. Neurosci. 17, 7053– 7059 9278541 PMC6573263
- Jaffar S. Counts S. E. Ma S. Y. Dadko E. Gordon M. N. Morgan D. Mufson E. J. (2001). Neuropathology of mice carrying mutant APP(swe) and/or PS1(M146L) transgenes: alterations in the p75(NTR) cholinergic basal forebrain septohippocampal pathway. Exp. Neurol. 170, 227– 243 10.1006/exnr.2001.7710 11476589 · DOI
- Kemper T. (1984). Neuroanatomical and neuropathological changes in normal aging and dementia. In Clinical Neurology of Aging, Albert M. L., ed. (New York, Oxford University Press), pp. 9– 52
- Kidd M. (1964). Alzheimer's Disease – an electron microscopical study. Brain 87, 307– 320 10.1093/brain/87.2.307 14188276 · DOI
- Kirkpatrick J. B. (1985). Non-random distribution of senile plaques in cerebral cortex. J. Neuropathol. Exp. Neurol. 44, 325– 331 10.1097/00005072-198505000-00081 · DOI
- Klausberger T. Marton L. F. Baude A. Roberts J. D. Magill P. J. Somogyi P. (2004). Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat. Neurosci. 7, 41– 47 10.1038/nn1159 14634650 · DOI · Paper page
- Knafo S. Alonso-Nanclares L. Gonzalez-Soriano J. Merino-Serrais P. Fernaud-Espinosa I. Ferrer I. DeFelipe J. (2009a). Widespread changes in dendritic spines in a model of Alzheimer's disease. Cereb. Cortex 19, 586– 592 10.1093/cercor/bhn111 18632740 · DOI · Paper page
- Knafo S. Venero C. Merino-Serrais P. Fernaud-Espinosa I. Gonzalez-Soriano J. Ferrer I. Santpere G. DeFelipe J. (2009b). Morphological alterations to neurons of the amygdala and impaired fear conditioning in a transgenic mouse model of Alzheimer's disease. J. Pathol. 219, 41– 51 10.1002/path.2565 19449368 · DOI
- Kosik K. S. Joachim C. L. Selkoe D. J. (1986). Microtubule-associated protien tau (τ) is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 83, 4044– 4048 10.1073/pnas.83.11.4044 2424016 PMC323662 · DOI
- Kuchibhotla K. V. Lattarulo C. R. Hyman B. T. Bacskai B. J. (2009). Synchronous hyperactivity and intercellular calcium waves in astrocytes in Alzheimer mice. Science 323, 1211– 1215 10.1126/science.1169096 19251629 PMC2884172 · DOI · Paper page
- Kuljis R. O. Tikoo R. K. (1997). Discontinuous distribution of senile plaques within striate cortex hypercolumns in Alzheimer's disease. Vis. Res. 37, 3573– 3591 10.1016/S0042-6989(96)00177-0 9425532 · DOI
- Lewis D. A. Campbell M. J. Terry R. D. Morrison J. H. (1987). Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices. J. Neurosci. 7, 1799– 1808 2439665 PMC6568896
- Lippa C. F. Hamos J. E. Pulaski-Salo D. DeGennaro L. J. Drachman D. A. (1992). Alzheimer's disease and aging: effects on perforant pathway perikarya and synapses. Neurobiol. Aging 13, 405– 411 10.1016/0197-4580(92)90115-E 1625770 · DOI
- Lowe S. L. Francis P. T. Procter A. W. Palmer A. M. Davison A. N. Bowen D. M. (1988). Gamma-aminobutyric acid concentration in brain tissue at two stages of Alzheimer's disease. Brain 111, 785– 799 10.1093/brain/111.4.785 3401683 · DOI
- Luse S. A. Smith K. R. (1964). The ultrastructure of senile plaques. Am. J. Path. 44, 553– 563 5877505 PMC1907027
- Masters C. L. Simms G. Weinman N. A. Multhaup G. McDonald B. L. Beyreuther K. (1985). Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. U.S.A. 82, 4245– 4249 10.1073/pnas.82.12.4245 3159021 PMC397973 · DOI · Paper page
- McGowan E. Eriksen J. Hutton M. (2006). A decade of modeling Alzheimer's disease in transgenic mice. Trends Genet. 22, 281– 289 10.1016/j.tig.2006.03.007 16567017 · DOI · Paper page
- Merchan-Perez A. Rodriguez J. R. Ribak C. E. DeFelipe J. (2009). The proximity of excitatory and inhibitory perisomatic axon terminals provides the basis for putative cortical nonsynaptic interactions. Proc. Natl. Acad. Sci. U.S.A. 106, 9878– 9883 10.1073/pnas.0900330106 19487685 PMC2701041 · DOI
- Mikkonen M. Alafuzoff I. Tapiola T. Soininen H. Miettinen R. (1999). Subfield- and layer-specific changes in parvalbumin, calretinin and calbindin-D28K immunoreactivity in the entorhinal cortex in Alzheimer's disease. Neuroscience 92, 515– 532 10.1016/S0306-4522(99)00047-0 10408601 · DOI
- Miles R. Toth K. Gulyas A. I. Hajos N. Freund T. F. (1996). Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815– 823 10.1016/S0896-6273(00)80101-4 8607999 · DOI · Paper page
- Minelli A. Alonso-Nanclares L. Edwards R. H. DeFelipe J. Conti F. (2003). Postnatal development of the vesicular GABA transporter in rat cerebral cortex. Neuroscience 117, 337– 346 10.1016/S0306-4522(02)00864-3 12614674 · DOI
- Minelli A. Brecha N. C. Karschin C. DeBiasi S. Conti F. (1995). GAT-1, a high-affinity GABA plasma membrane transporter, is localized to neurons and astroglia in the cerebral cortex. J. Neurosci. 15, 7734– 7746 7472524 PMC6578038
- Moran L. B. Graeber M. B. (2004). The facial nerve axotomy model. Brain Res. Brain Res. Rev. 44, 154– 178 10.1016/j.brainresrev.2003.11.004 15003391 · DOI
- Nägga K. Bogdanovic N. Marcusson J. (1999). GABA transporters (GAT-1) in Alzheimer's disease. J. Neural Transm. 106, 1141– 1149 10.1007/s007020050230 10651110 · DOI
- Pappolla M. A. Omar R. A. Vinters H. V. (1991). Image analysis microspectroscopy shows that neurons participate in the genesis of a subset of early primitive (diffuse) senile plaques. Am. J. Pathol. 139, 599– 607 1716046 PMC1886230
- Pearson R. C. Esiri M. M. Hiorns R. W. Wilcock G. K. Powell T. P. (1985). Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 82, 4531– 4534 10.1073/pnas.82.13.4531 3859874 PMC391136 · DOI · Paper page
- Preuss T. M. (2006). Who's afraid of Homo sapiens? J. Biomed. Discov. Collab. 1, 17 10.1186/1747-5333-1-17 17134486 PMC1764430 · DOI
- Price J. L. Morris J. C. (2004). So what if tangles precede plaques? Neurobiol. Aging 25, 721– 723 10.1016/j.neurobiolaging.2003.12.017 15165694 · DOI
- Radde R. Duma C. Goedert M. Jucker M. (2008). The value of incomplete mouse models of Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging 35, S70– S74 10.1007/s00259-007-0704-y 18270700 · DOI
- Rafalowska J. Barcikowska M. Wen G. Y. Wisniewski H. M. (1988). Laminar distribution of neuritic plaques in normal aging, Alzheimer's disease and Down's syndrome. Acta Neuropathol. (Berl.) 77, 21– 25 10.1007/BF00688238 2977047 · DOI
- Reinikainen K. J. Paljarvi L. Huuskonen M. Soininen H. Laakso M. Riekkinen P. J. (1988). A post-mortem study of noradrenergic, serotonergic and GABAergic neurons in Alzheimer's disease. J. Neurol. Sci. 84, 101– 116 10.1016/0022-510X(88)90179-7 2452858 · DOI
- Ren M. Yoshimura Y. Takada N. Horibe S. Komatsu Y. (2007). Specialized inhibitory synaptic actions between nearby neocortical pyramidal neurons. Science 316, 758– 761 10.1126/science.1135468 17478724 · DOI
- Ribak C. E. (1978). Aspinous and sparsely-spinous stellate neurons in the visual cortex of rats contain glutamic acid decarboxylase. J. Neurocytol. 7, 461– 478 10.1007/BF01173991 690673 · DOI
- Rissman R. A. De Blas A. L. Armstrong D. M. (2007). GABA(A) receptors in aging and Alzheimer's disease. J. Neurochem. 103, 1285– 1292 (Review). 10.1111/j.1471-4159.2007.04832.x 17714455 · DOI
- Rogers J. Morrison J. H. (1985). Quantitative morphology and regional and laminar distributions of senile plaques in Alzheimer's disease. J. Neurosci. 5, 2801– 2808 4045553 PMC6565139
- Solodkin A. Veldhuizen S. D. Van Hoesen G. W. (1996). Contingent vulnerability of entorhinal parvalbumin-containing neurons in Alzheimer's disease. J. Neurosci. 16, 3311– 3321 8627368 PMC6579156
- Takahashi R. H. Milner T. A. Li F. Nam E. E. Edgar M. A. Yamaguchi H. Beal M. F. Xu H. Greengard P. Gouras G. K. (2002). Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am. J. Pathol. 161, 1869– 1879 12414533 PMC1850783
- Terry R. D. Gonatas N. K. Weiss M. (1964). Ultrastructural studies in Alzheimer's presenile dementia. Am. J. Path. 44, 269– 297 14119171 PMC1906996
- Terry R. D. Katzman R. (1983). Senile dementia of the Alzheimer type. Ann. Neurol. 14, 497– 506 10.1002/ana.410140502 6139975 · DOI
- Thal D. R. Holzer M. Rub U. Waldmann G. Gunzel S. Zedlick D. Schober R. (2000). Alzheimer-related tau-pathology in the perforant path target zone and in the hippocampal stratum oriens and radiatum correlates with onset and degree of dementia. Exp. Neurol. 163, 98– 110 10.1006/exnr.2000.7380 10785448 · DOI
- Thal D. R. Rub U. Orantes M. Braak H. (2002). Phases of A betadeposition in the human brain and its relevance for the development of AD. Neurology 58, 1791– 1800 12084879
- Tsai J. Grutzendler J. Duff K. Gan W. B. (2004). Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat. Neurosci. 7, 1181– 1183 10.1038/nn1335 15475950 · DOI · Paper page
- Velez-Pardo C. Arellano J. I. Cardona-Gomez P. Jimenez Del Rio M. Lopera F. DeFelipe J. (2004). CA1 hippocampal neuronal loss in familial Alzheimer's disease presenilin-1 E280A mutation is related to epilepsy. Epilepsia 45, 751– 756 10.1111/j.0013-9580.2004.55403.x 15230697 · DOI
- Wisniewski H. M. Wen G. Y. Kim K. S. (1989). Comparison of four staining methods on the detection of neuritic plaques. Acta Neuropathol. 78, 22– 27 10.1007/BF00687398 2472039 · DOI
- Yan X. X. Cariaga W. A. Ribak C. E. (1997). Immunoreactivity for GABA plasma membrane transporter, GAT-1, in the developing rat cerebral cortex: transient presence in the somata of neocortical and hippocampal neurons. Dev. Brain Res. 99, 1– 19 10.1016/S0165-3806(96)00192-7 9088561 · DOI
- Young A. B. (1987). Cortical amino acidergic pathways in Alzheimer's disease. J. Neural Transm. Suppl. 24, 147– 152 (Review). 2824688
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- Authors
- Garcia-Marin, V.
- Venue
- Frontiers in Neuroanatomy
- Publisher
- Frontiers Media SA
- Published
- 2009
- Volume
- 3
- Pages
- 28-28
- ISSN
- 1662-5129 (ISSN-L)
- PMC
- PMC2784678
- OpenAlex
- W2153628730
- Cited by
- 136
- References
- 11
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 16 · 2023: 8 · 2022: 13 · 2021: 16 · 2020: 12 · 2019: 16 · 2018: 7 · 2017: 9 · 2016: 4 · 2015: 7 · 2014: 4 · 2013: 5 · 2012: 6
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- other-oa
- Locations
- Frontiers in Neuroanatomy (publishedVersion, other-oa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, cc-by)
- Funders
- “la Caixa” Foundation
- Ministerio de Ciencia y Tecnología
- Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CB06/05/0066)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, amyloid plaques, GABAergic synapses, cortical pyramidal neurons, APP/PS1 mice, neuronal hyperactivity, cerebral cortex
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.
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