Microglia: A new frontier for synaptic plasticity, learning and memory, and neurodegenerative disease research

Abdipranoto, 2008, The role of neurogenesis in neurodegenerative diseases and its implications for therapeutic development, CNS & Neurological Disorders Drug Targets, 7, 187, 10.2174/187152708784083858

Abdipranoto-Cowley, 2009, Activin A is essential for neurogenesis following neurodegeneration, Stem Cells, 27, 1330, 10.1002/stem.80

Abraham, 1996, Metaplasticity: The plasticity of synaptic plasticity, Trends in Neurosciences, 19, 126, 10.1016/S0166-2236(96)80018-X

Akiyama, 2000, Inflammation and Alzheimer’s disease, Neurobiology of Aging, 21, 383, 10.1016/S0197-4580(00)00124-X

Albensi, 2000, Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity, Synapse, 35, 151, 10.1002/(SICI)1098-2396(200002)35:2<151::AID-SYN8>3.0.CO;2-P

Allen, 2005, Signaling between glia and neurons: Focus on synaptic plasticity, Current Opinion in Neurobiology, 15, 542, 10.1016/j.conb.2005.08.006

Aloe, 1999, Learning abilities, NGF and BDNF brain levels in two lines of TNF-alpha transgenic mice, one characterized by neurological disorders, the other phenotypically normal, Brain Research, 840, 125, 10.1016/S0006-8993(99)01748-5

Alvarez, 2007, Anatomical and physiological plasticity of dendritic spines, Annual Review of Neuroscience, 30, 79, 10.1146/annurev.neuro.30.051606.094222

Araque, 1999, Tripartite synapses: Glia, the unacknowledged partner, Trends in Neuroscience, 22, 208, 10.1016/S0166-2236(98)01349-6

Atwood, 2002, Diversification of synaptic strength: Presynaptic elements, Nature Reviews Neuroscience, 3, 497, 10.1038/nrn876

Bailey, 1996, Toward a molecular definition of long-term memory storage, Proceedings of the National Academy of Sciences, 93, 13445, 10.1073/pnas.93.24.13445

Bannerman, 1995, Distinct components of spatial learning revealed by prior training and NMDA receptor blockade, Nature, 378, 182, 10.1038/378182a0

Barclay, 2002, CD200 and membrane protein interactions in the control of myeloid cells, Trends in Immunology, 23, 285, 10.1016/S1471-4906(02)02223-8

Barker, 2010, Astrocytes and synaptic plasticity, The Neuroscientist, 16, 40, 10.1177/1073858409339215

Bear, 1999, Homosynaptic long-term depression: A mechanism for memory?, Proceedings of the National Academy of Sciences, 96, 9457, 10.1073/pnas.96.17.9457

Beattie, 2002, Control of synaptic strength by glial TNFalpha, Science, 295, 2282, 10.1126/science.1067859

Bennett, 2007, Synaptic P2X7 receptor regenerative-loop hypothesis for depression, Australian and New Zealand Journal of Psychiatry, 41, 563, 10.1080/00048670701399994

Bernardino, 2008, Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures, Stem Cells, 26, 2361, 10.1634/stemcells.2007-0914

Bessis, 2007, Microglial control of neuronal death and synaptic properties, Glia, 55, 233, 10.1002/glia.20459

Beutler, 1994, An evolutionary and functional approach to the TNF receptor/ligand family, Annals of the New York Academy of Sciences, 730, 118, 10.1111/j.1749-6632.1994.tb44244.x

Bianchin, 2010, Nasu–Hakola disease and primary microglial dysfunction, Nature Reviews Neurology, 6, 10.1038/nrneurol.2010.17-c1

Biber, 2007, Neuronal on and off signals control microglia, Trends in Neurosciences, 30, 596, 10.1016/j.tins.2007.08.007

Bitzer-Quintero, 2012, Immune system in the brain: A modulatory role on dendritic spine morphophysiology?, Neural Plasticity, 2012, 348642, 10.1155/2012/348642

Blank, 2013, Microglia as modulators of cognition and neuropsychiatric disorders, Glia, 61, 62, 10.1002/glia.22372

Blinzinger, 1968, Displacement of synaptic terminals from regenerating motoneurons by microglial cells, Z Zellforsch Mikrosk Anat, 85, 145, 10.1007/BF00325030

Bliss, 1993, A synaptic model of memory: Long-term potentiation in the hippocampus, Nature, 361, 31, 10.1038/361031a0

Bliss, 1973, Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path, The Journal of Physiology, 232, 331, 10.1113/jphysiol.1973.sp010273

Boulanger, 2009, Immune proteins in brain development and synaptic plasticity, Neuron, 64, 93, 10.1016/j.neuron.2009.09.001

Bourne, 2007, Do thin spines learn to be mushroom spines that remember?, Current Opinion in Neurobiology, 17, 381, 10.1016/j.conb.2007.04.009

Bourtchuladze, 1994, Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein, Cell, 79, 59, 10.1016/0092-8674(94)90400-6

Brynskikh, 2008, Adaptive immunity affects learning behavior in mice, Brain, Behavior, and Immunity, 22, 861, 10.1016/j.bbi.2007.12.008

Cacci, 2005, Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro, The Journal of Neuroscience Research, 80, 789, 10.1002/jnr.20531

Cajal, 1888, Estructura de los centros nerviosos de las aves, Revista Trimestral de Histología Normal y Patológica, 1, 1

Cajal, 1891, Significación fisiológica de las expansiones protoplásmicas y nerviosas de la sustancia gris, Revista Trimestral de Histología Normal y Patológica, 22, 23

Cajal, 1894, The croonian lecture: la fine structure des centres nerveux, Proceedings of the Royal Society of London, 55, 444, 10.1098/rspl.1894.0063

Cameron, 2010, Inflammation, microglia, and Alzheimer’s disease, Neurobiology of Disease, 37, 503, 10.1016/j.nbd.2009.10.006

Cardona, 2006, Control of microglial neurotoxicity by the fractalkine receptor, Nature Neuroscience, 9, 917, 10.1038/nn1715

Chen, 2004, The role of actin in the regulation of dendritic spine morphology and bidirectional synaptic plasticity, Neuroreport, 15, 829, 10.1097/00001756-200404090-00018

Chen, 2010, Spinal microglial motility is independent of neuronal activity and plasticity in adult mice, Molecular Pain, 6, 19, 10.1186/1744-8069-6-19

Chen, 1997, Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain, Annual Review of Neuroscience, 20, 157, 10.1146/annurev.neuro.20.1.157

Cho, 2008, Role of microglial IKKbeta in kainic acid-induced hippocampal neuronal cell death, Brain, 131, 3019, 10.1093/brain/awn230

Clark, 2010, The roles of TNF in brain dysfunction and disease, Pharmacology & Therapeutics, 128, 519, 10.1016/j.pharmthera.2010.08.007

Clark, 2012, Tumor necrosis factor-induced cerebral insulin resistance in Alzheimer’s disease links numerous treatment rationales, Pharmacological Reviews, 64, 1004, 10.1124/pr.112.005850

Clausen, 1999, Conditional gene targeting in macrophages and granulocytes using LysMcre mice, Transgenic Res, 8, 265, 10.1023/A:1008942828960

Colonnier, 1968, Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study, Brain Research, 9, 268, 10.1016/0006-8993(68)90234-5

Colton, 2009, Heterogeneity of microglial activation in the innate immune response in the brain, Journal of Neuroimmune Pharmacology, 4, 399, 10.1007/s11481-009-9164-4

Combrinck, 2002, Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease, Neuroscience, 112, 7, 10.1016/S0306-4522(02)00030-1

Cooke, 2006, Plasticity in the human central nervous system, Brain, 129, 1659, 10.1093/brain/awl082

Costello, 2011, Long term potentiation is impaired in membrane glycoprotein CD200-deficient mice: A role for Toll-like receptor activation, The Journal of Biological Chemistry, 286, 34722, 10.1074/jbc.M111.280826

Cunningham, 2005, Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration, The Journal of Neuroscience, 25, 9275, 10.1523/JNEUROSCI.2614-05.2005

Damani, 2011, Age-related alterations in the dynamic behavior of microglia, Aging Cell, 10, 263, 10.1111/j.1474-9726.2010.00660.x

Daniel, 2009, Functional heterogeneity at dopamine release sites, The Journal of Neuroscience, 29, 14670, 10.1523/JNEUROSCI.1349-09.2009

Davalos, 2005, ATP mediates rapid microglial response to local brain injury in vivo, Nature Neuroscience, 8, 752, 10.1038/nn1472

Davies, 1987, A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer’s disease, Journal of the Neurological Sciences, 78, 151, 10.1016/0022-510X(87)90057-8

Dityatev, 2011, Molecular signals of plasticity at the tetrapartite synapse, Current Opinion in Neurobiology, 21, 353, 10.1016/j.conb.2010.12.006

Domercq, 2013, Neurotransmitter signaling in the pathophysiology of microglia, Frontiers in Cellular Neuroscience, 7, 49

Elgersma, 1999, Molecular mechanisms of synaptic plasticity and memory, Current Opinion in Neurobiology, 9, 209, 10.1016/S0959-4388(99)80029-4

Engert, 1999, Dendritic spine changes associated with hippocampal long-term synaptic plasticity, Nature, 399, 66, 10.1038/19978

Fagan, T. (2013). Microglia activation—Venusberg meeting Questions M1, M2 Designations. <http://www.alzforum.org/new/detail.asp?id=3426> (Retrieved 15.07.2013).

Farber, 2005, Physiology of microglial cells, Brain Research Reviews, 48, 133, 10.1016/j.brainresrev.2004.12.003

Farber, 2006, Purinergic signaling and microglia, Pflugers Arch, 452, 615, 10.1007/s00424-006-0064-7

Fiala, 1998, Synaptogenesis via dendritic filopodia in developing hippocampal area CA1, The Journal of Neuroscience, 18, 8900, 10.1523/JNEUROSCI.18-21-08900.1998

Fiala, 2002, Dendritic spine pathology: Cause or consequence of neurological disorders?, Brain Research Reviews, 39, 29, 10.1016/S0165-0173(02)00158-3

Finnie, 2012, The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation, Neuroscience & Biobehavioral Reviews, 36, 1667, 10.1016/j.neubiorev.2012.03.008

Fischer, 1995, Complement C1q and C3 mRNA expression in the frontal cortex of Alzheimer’s patients, Journal of Molecular Medicine, 73, 465, 10.1007/BF00202265

Fontainhas, 2011, Microglial morphology and dynamic behavior is regulated by ionotropic glutamatergic and GABAergic neurotransmission, PLoS One, 6, e15973, 10.1371/journal.pone.0015973

Frick, 2013, Microglial dysregulation in psychiatric disease, Clinical and Developmental Immunology, 2013, 10, 10.1155/2013/608654

Fuhrmann, 2010, Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease, Nature Neuroscience, 13, 411, 10.1038/nn.2511

Ganat, 2006, Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo, The Journal of Neuroscience, 26, 8609, 10.1523/JNEUROSCI.2532-06.2006

Garay, 2010, Novel roles for immune molecules in neural development: Implications for neurodevelopmental disorders, Frontiers in Synaptic Neuroscience, 2, 136, 10.3389/fnsyn.2010.00136

Garcia-Lopez, 2010, Dendritic spines and development: Towards a unifying model of spinogenesis–a present day review of Cajal’s histological slides and drawings, Neural Plasticity, 2010, 769207, 10.1155/2010/769207

Gehrmann, 1995, Microglia: Intrinsic immuneffector cell of the brain, Brain Research Reviews, 20, 269, 10.1016/0165-0173(94)00015-H

Gerlai, 1995, Overexpression of a calcium-binding protein, S100 beta, in astrocytes alters synaptic plasticity and impairs spatial learning in transgenic mice, Learning and Memory, 2, 26, 10.1101/lm.2.1.26

Ginhoux, 2010, Fate mapping analysis reveals that adult microglia derive from primitive macrophages, Science, 330, 841, 10.1126/science.1194637

Glezer, 2003, Modulation of the innate immune response by NMDA receptors has neuropathological consequences, The Journal of Neuroscience, 23, 11094, 10.1523/JNEUROSCI.23-35-11094.2003

Golde, 2013, Alzheimer’s disease risk alleles in TREM2 illuminate innate immunity in Alzheimer’s disease, Alzheimer’s Research & Therapy, 5, 24, 10.1186/alzrt178

Goshen, 2007, A dual role for interleukin-1 in hippocampal-dependent memory processes, Psychoneuroendocrinology, 32, 1106, 10.1016/j.psyneuen.2007.09.004

Graeber, 1993, Synaptic stripping in the human facial nucleus, Acta Neuropathologica, 86, 179, 10.1007/BF00334886

Graeber, 2011, Role of microglia in CNS inflammation, FEBS Letters, 585, 3798, 10.1016/j.febslet.2011.08.033

Gray, 1959, Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study, Journal of Anatomy, 93, 420

Griffin, 2006, The age-related attenuation in long-term potentiation is associated with microglial activation, Journal of Neurochemistry, 99, 1263, 10.1111/j.1471-4159.2006.04165.x

Grutzendler, 2002, Long-term dendritic spine stability in the adult cortex, Nature, 420, 812, 10.1038/nature01276

Guerreiro, 2013, TREM2 variants in Alzheimer’s disease, New England Journal of Medicine, 368, 117, 10.1056/NEJMoa1211851

Han, 2013, Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice, Cell Stem Cell, 12, 342, 10.1016/j.stem.2012.12.015

Hanisch, 2002, Microglia as a source and target of cytokines, Glia, 40, 140, 10.1002/glia.10161

Haynes, 2006, The P2Y12 receptor regulates microglial activation by extracellular nucleotides, Nature Neuroscience, 9, 1512, 10.1038/nn1805

Hebb, 1949

Hoek, 2000, Down-regulation of the macrophage lineage through interaction with OX2 (CD200), Science, 290, 1768, 10.1126/science.290.5497.1768

Holtmaat, 2009, Experience-dependent structural synaptic plasticity in the mammalian brain, Nature Reviews Neuroscience, 10, 647, 10.1038/nrn2699

Holtmaat, 2005, Transient and persistent dendritic spines in the neocortex in vivo, Neuron, 45, 279, 10.1016/j.neuron.2005.01.003

Hulme, 2013, Emerging roles of metaplasticity in behaviour and disease, Trends in Neurosciences, 36, 353, 10.1016/j.tins.2013.03.007

Iosif, 2008, Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1, Journal of Cerebral Blood Flow & Metabolism, 28, 1574, 10.1038/jcbfm.2008.47

Iosif, 2006, Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis, The Journal of Neuroscience, 26, 9703, 10.1523/JNEUROSCI.2723-06.2006

Ishii, 2008, Expression of nonclassical Class I major histocompatibility genes defines a tripartite organization of the mouse vomeronasal system, The Journal of Neuroscience, 28, 2332, 10.1523/JNEUROSCI.4807-07.2008

Johnston, 1992, NMDA-receptor-independent long-term potentiation, Annual Reviews Physiology, 54, 489, 10.1146/annurev.ph.54.030192.002421

Jonsson, T., Stefansson, H., Ph, D. Ss, Jonsdottir, I., Jonsson, P. V., Snaedal, J., Stefansson, K. (2012). Variant of TREM2 Associated with the Risk of Alzheimer’s Disease. New England Journal of Medicine.

Kaindl, 2012, Activation of microglial N-methyl-D-aspartate receptors triggers inflammation and neuronal cell death in the developing and mature brain, Annals of Neurology, 72, 536, 10.1002/ana.23626

Kaindl, 2008, Microglia express functional NMDA receptors: A novel finding and a promise for innovative treatment of excitotoxic and inflammatory brain disease, Neuropediatrics, 39, V23, 10.1055/s-0029-1215736

Kalla, 2001, Journal of Comparative Neurology, 436, 182, 10.1002/cne.1060

Kandel, 2001, The molecular biology of memory storage: A dialogue between genes and synapses, Science, 294, 1030, 10.1126/science.1067020

Kandel, 2009, The biology of memory: A forty-year perspective, The Journal of Neuroscience, 29, 12748, 10.1523/JNEUROSCI.3958-09.2009

Kasai, 2010, Structural dynamics of dendritic spines in memory and cognition, Trends in Neurosciences, 33, 121, 10.1016/j.tins.2010.01.001

Katz, 1996, Synaptic activity and the construction of cortical circuits, Science, 274, 1133, 10.1126/science.274.5290.1133

Kawakami, 2013, Visualizing hippocampal neurons with in vivo two-photon microscopy using a 1030nm picosecond pulse laser, Scientific Reports, 3, 1014, 10.1038/srep01014

Kettenmann, 2007, Neuroscience: The brain’s garbage men, Nature, 446, 987, 10.1038/nature05713

Kettenmann, 2011, Physiology of microglia, Physiological Reviews, 91, 461, 10.1152/physrev.00011.2010

Kettenmann, 2013, Microglia: New roles for the synaptic stripper, Neuron, 77, 10, 10.1016/j.neuron.2012.12.023

Kierdorf, 2013, Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways, Nature Neuroscience, 16, 273, 10.1038/nn.3318

Kitamura, 1978, Initial response of silver-impregnated “resting microglia” to stab wounding in rabbit hippocampus, Acta Neuropathologica, 44, 31, 10.1007/BF00691636

Klemann, 2011, The gray area between synapse structure and function—Gray’s synapse types I and II revisited, Synapse, 65, 1222, 10.1002/syn.20962

Kopec, 2006, Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation, The Journal of Neuroscience, 26, 2000, 10.1523/JNEUROSCI.3918-05.2006

Krabbe, 2013, Functional impairment of microglia coincides with Beta-amyloid deposition in mice with Alzheimer-like pathology, PLoS One, 8, e60921, 10.1371/journal.pone.0060921

Krause, D. L., & Muller, N. (2010). Neuroinflammation, microglia and implications for anti-inflammatory treatment in Alzheimer’s disease. International Journal of Alzheimer’s Disease.

Kreutzberg, 1996, Microglia: A sensor for pathological events in the CNS, Trends in Neurosciences, 19, 312, 10.1016/0166-2236(96)10049-7

Kubota, 2009, Tumor necrosis factor receptor-associated protein 1 regulates cell adhesion and synaptic morphology via modulation of N-cadherin expression, Journal of Neurochemistry, 110, 496, 10.1111/j.1471-4159.2009.06099.x

Kurpius, 2007, Purines induce directed migration and rapid homing of microglia to injured pyramidal neurons in developing hippocampus, Glia, 55, 873, 10.1002/glia.20509

Kurpius, 2006, Early activation, motility, and homing of neonatal microglia to injured neurons does not require protein synthesis, Glia, 54, 58, 10.1002/glia.20355

Lai, 2012, Opposite effects of fear conditioning and extinction on dendritic spine remodelling, Nature, 483, 87, 10.1038/nature10792

Lang, 2004, Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation, Proceedings of the National Academy of Sciences, 101, 16665, 10.1073/pnas.0407581101

Lawson, 1990, Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain, Neuroscience, 39, 151, 10.1016/0306-4522(90)90229-W

Lawson, 1992, Turnover of resident microglia in the normal adult mouse brain, Neuroscience, 48, 405, 10.1016/0306-4522(92)90500-2

Lee, 2002, Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD, Neuron, 36, 661, 10.1016/S0896-6273(02)01024-3

Linden, 1995, Long-term synaptic depression, Annual Review of Neuroscience, 18, 319, 10.1146/annurev.ne.18.030195.001535

Lukiw, 2007, Micro-RNA speciation in fetal, adult and Alzheimer’s disease hippocampus, Neuroreport, 18, 297, 10.1097/WNR.0b013e3280148e8b

Luscher, 2012, NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD), Cold Spring Harbor Perspectives in Biology, 4, 10.1101/cshperspect.a005710

Luscher, 1999, Role of AMPA receptor cycling in synaptic transmission and plasticity, Neuron, 24, 649, 10.1016/S0896-6273(00)81119-8

Lynch, 1977, Heterosynaptic depression: A postsynaptic correlate of long-term potentiation, Nature, 266, 737, 10.1038/266737a0

Lyons, 2009, Fractalkine-induced activation of the phosphatidylinositol-3 kinase pathway attentuates microglial activation in vivo and in vitro, Journal of Neurochemistry, 110, 1547, 10.1111/j.1471-4159.2009.06253.x

Maezawa, 2010, Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate, The Journal of Neuroscience, 30, 5346, 10.1523/JNEUROSCI.5966-09.2010

Majewska, 2006, Remodeling of synaptic structure in sensory cortical areas in vivo, The Journal of Neuroscience, 26, 3021, 10.1523/JNEUROSCI.4454-05.2006

Maletic-Savatic, 1999, Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity, Science, 283, 1923, 10.1126/science.283.5409.1923

Mallat, 1994, Brain macrophages: Neurotoxic or neurotrophic effector cells?, Journal of Leukocyte Biology, 56, 416, 10.1002/jlb.56.3.416

Man, 2000, Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization, Neuron, 25, 649, 10.1016/S0896-6273(00)81067-3

Maren, 1996, N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats, Behavioral Neuroscience, 110, 1365, 10.1037/0735-7044.110.6.1365

Martin, 2000, Synaptic plasticity and memory: An evaluation of the hypothesis, Annual Review of Neuroscience, 23, 649, 10.1146/annurev.neuro.23.1.649

Masliah, 1994, Synaptic and neuritic alterations during the progression of Alzheimer’s disease, Neuroscience Letters, 174, 67, 10.1016/0304-3940(94)90121-X

Massey, 2007, Long-term depression: Multiple forms and implications for brain function, Trends in Neurosciences, 30, 176, 10.1016/j.tins.2007.02.005

Matsuzaki, 2004, Structural basis of long-term potentiation in single dendritic spines, Nature, 429, 761, 10.1038/nature02617

Mayford, 1996, Control of memory formation through regulated expression of a CaMKII transgene, Science, 274, 1678, 10.1126/science.274.5293.1678

Mayford, 1999, Genetic approaches to memory storage, Trends in Genetics, 15, 463, 10.1016/S0168-9525(99)01846-6

Mayford, 2012, Synapses and memory storage, Cold Spring Harbor Perspectives in Biology, 4, 10.1101/cshperspect.a005751

McGeer, 2003, Inflammatory processes in Alzheimer’s disease, Progress in Neuro-Psychopharmacology and Biological Psychiatry, 27, 741, 10.1016/S0278-5846(03)00124-6

McKercher, 1996, Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities, The EMBO Journal, 15, 5647, 10.1002/j.1460-2075.1996.tb00949.x

Miller, 1981, Maturation of rat visual cortex. II. A combined Golgi-electron microscope study of pyramidal neurons, The Journal of Comparative Neurology, 203, 555, 10.1002/cne.902030402

Mittelbronn, 2001, Local distribution of microglia in the normal adult human central nervous system differs by up to one order of magnitude, Acta Neuropathologica, 101, 249, 10.1007/s004010000284

Mizrahi, 2004, High-resolution in vivo imaging of hippocampal dendrites and spines, The Journal of Neuroscience, 24, 3147, 10.1523/JNEUROSCI.5218-03.2004

Mobley, 2012, Use of Cre-lox technology to analyze integrin functions in astrocytes, Methods Mol Biol, 814, 555, 10.1007/978-1-61779-452-0_37

Monji, 2009, Cytokines and schizophrenia: Microglia hypothesis of schizophrenia, Psychiatry and Clinical Neurosciences, 63, 257, 10.1111/j.1440-1819.2009.01945.x

Moran, 2004, The facial nerve axotomy model, Brain Research Reviews, 44, 154, 10.1016/j.brainresrev.2003.11.004

Mozzachiodi, 2010, More than synaptic plasticity: Role of nonsynaptic plasticity in learning and memory, Trends in Neurosciences, 33, 17, 10.1016/j.tins.2009.10.001

Mulkey, 1992, Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus, Neuron, 9, 967, 10.1016/0896-6273(92)90248-C

Munn, 2000, Microglia dysfunction in schizophrenia: An integrative theory, Medical Hypotheses, 54, 198, 10.1054/mehy.1999.0018

Nagerl, 2004, Bidirectional activity-dependent morphological plasticity in hippocampal neurons, Neuron, 44, 759, 10.1016/j.neuron.2004.11.016

Nedergaard, 2012, Artifact versus reality—How astrocytes contribute to synaptic events, Glia, 60, 1013, 10.1002/glia.22288

Neumann, 2007, Essential role of the microglial triggering receptor expressed on myeloid cells-2 (TREM2) for central nervous tissue immune homeostasis, Journal of Neuroimmunology, 184, 92, 10.1016/j.jneuroim.2006.11.032

Nimchinsky, 2002, Structure and function of dendritic spines, Annual Review of Physiology, 64, 313, 10.1146/annurev.physiol.64.081501.160008

Nimmerjahn, 2012, Two-photon imaging of microglia in the mouse cortex in vivo, Cold Spring Harbor Protocols, 2012, 10.1101/pdb.prot069294

Nimmerjahn, 2005, Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo, Science, 308, 1314, 10.1126/science.1110647

Nolte, 1996, Complement 5a controls motility of murine microglial cells in vitro via activation of an inhibitory G-protein and the rearrangement of the actin cytoskeleton, Neuroscience, 73, 1091, 10.1016/0306-4522(96)00106-6

Norden, 2013, Review: Microglia of the aged brain: Primed to be activated and resistant to regulation, Neuropathology and Applied Neurobiology, 39, 19, 10.1111/j.1365-2990.2012.01306.x

Oberheim, 2012, Heterogeneity of astrocytic form and function, Methods in Molecular Biology, 814, 23, 10.1007/978-1-61779-452-0_3

Oemichen, 1978, Mononuclear phagocytes in the central nervous system. Origin, mode of distribution, and function of progressive microglia, perivascular cells of intracerebral vessels, free subarachnoidal cells, and epiplexus cells, Schriftenreihe Neurologie, 21, 1

Ogoshi, 2005, Tumor necrosis-factor-alpha (TNF-α) induces rapid insertion of Ca2+-permeable α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA)/kainate (Ca-A/K) channels in a subset of hippocampal pyramidal neurons, Experimental Neurology, 193, 384, 10.1016/j.expneurol.2004.12.026

Okun, 2012, Evidence for a developmental role for TLR4 in learning and memory, PLoS One, 7, e47522, 10.1371/journal.pone.0047522

Ottersen, 1997, Molecular organization of cerebellar glutamate synapses, Progress in Brain Research, 114, 97, 10.1016/S0079-6123(08)63360-9

Pan, 1997, Tumor necrosis factor-alpha: A neuromodulator in the CNS, Neuroscience and Biobehavioral Reviews, 21, 603, 10.1016/S0149-7634(96)00047-4

Pannasch, 2013, Emerging role for astroglial networks in information processing: From synapse to behavior, Trends in Neurosciences, 36, 405, 10.1016/j.tins.2013.04.004

Paolicelli, 2011, Synaptic pruning by microglia is necessary for normal brain development, Science, 333, 1456, 10.1126/science.1202529

Pascual, 2012, Microglia activation triggers astrocyte-mediated modulation of excitatory neurotransmission, Proceedings of the National Academy of Sciences, 109, E197, 10.1073/pnas.1111098109

Pearce, 2004, Sir Charles Scott Sherrington (1857–1952) and the synapse, Journal of Neurology, Neurosurgery & Psychiatry, 75, 544, 10.1136/jnnp.2003.017921

Penzes, 2011, Dendritic spine pathology in neuropsychiatric disorders, Nature Neuroscience, 14, 285, 10.1038/nn.2741

Perea, 2009, Tripartite synapses: Astrocytes process and control synaptic information, Trends in Neurosciences, 32, 421, 10.1016/j.tins.2009.05.001

Perry, 2007, Systemic infections and inflammation affect chronic neurodegeneration, Nature Reviews Immunology, 7, 161, 10.1038/nri2015

Perry, 2010, Microglia in neurodegenerative disease, Nature Reviews Neurology, 6, 193, 10.1038/nrneurol.2010.17

Perry, 2010, The role of microglia in synaptic stripping and synaptic degeneration: A revised perspective, ASN Neuro, 2, e00047, 10.1042/AN20100024

Peters, 1970, The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines, American Journal of Anatomy, 127, 321, 10.1002/aja.1001270402

Petersen, 2004, Diverse microglial motility behaviors during clearance of dead cells in hippocampal slices, Glia, 46, 195, 10.1002/glia.10362

Pocock, 2007, Neurotransmitter receptors on microglia, Trends in Neurosciences, 30, 527, 10.1016/j.tins.2007.07.007

Ponomarev, 2011, MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-[alpha]-PU.1 pathway, Nature Medicine, 17, 64, 10.1038/nm.2266

Ransohoff, 2010, The myeloid cells of the central nervous system parenchyma, Nature, 468, 253, 10.1038/nature09615

Ransohoff, 2009, Microglial physiology: Unique stimuli, specialized responses, Annual Review of Immunology, 27, 119, 10.1146/annurev.immunol.021908.132528

Redondo, 2011, Making memories last: The synaptic tagging and capture hypothesis, Nature Reviews Neuroscience, 12, 17, 10.1038/nrn2963

Rivest, 2009, Regulation of innate immune responses in the brain, Nature Reviews Immunology, 9, 429, 10.1038/nri2565

Rochefort, 2012, Dendritic spines: From structure to in vivo function, EMBO Reports, 13, 699, 10.1038/embor.2012.102

Rogers, 2011, CX3CR1 deficiency leads to impairment of hippocampal cognitive function and synaptic plasticity, The Journal of Neuroscience, 31, 16241, 10.1523/JNEUROSCI.3667-11.2011

Romo-González, 2012, Central nervous system: A modified immune surveillance circuit?, Brain, Behavior, and Immunity, 26, 823, 10.1016/j.bbi.2012.01.016

Saijo, 2011, Microglial cell origin and phenotypes in health and disease, Nature Reviews Immunology, 11, 775, 10.1038/nri3086

Sanders, 2012, Elimination of dendritic spines with long-term memory is specific to active circuits, The Journal of Neuroscience, 32, 12570, 10.1523/JNEUROSCI.1131-12.2012

Santello, 2012, TNFalpha in synaptic function: Switching gears, Trends in Neurosciences, 35, 638, 10.1016/j.tins.2012.06.001

Sauer, 1998, Inducible gene targeting in mice using the Cre/lox system, Methods, 14, 381, 10.1006/meth.1998.0593

Schafer, 2012, Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner, Neuron, 74, 691, 10.1016/j.neuron.2012.03.026

Schafer, 2013, The “quad-partite” synapse: Microglia-synapse interactions in the developing and mature CNS, Glia, 61, 24, 10.1002/glia.22389

Scheff, 2003, Synaptic pathology in Alzheimer’s disease: A review of ultrastructural studies, Neurobiology of Aging, 24, 1029, 10.1016/j.neurobiolaging.2003.08.002

Scheff, 2007, Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment, Neurology, 68, 1501, 10.1212/01.wnl.0000260698.46517.8f

Scheff, 2006, Hippocampal synaptic loss in early Alzheimer’s disease and mild cognitive impairment, Neurobiology of Aging, 27, 1372, 10.1016/j.neurobiolaging.2005.09.012

Schiefer, 1999, Microglial motility in the rat facial nucleus following peripheral axotomy, Journal of Neurocytology, 28, 439, 10.1023/A:1007048903862

Schoch, 2006, Molecular organization of the presynaptic active zone, Cell and Tissue Research, 326, 379, 10.1007/s00441-006-0244-y

Selkoe, 2002, Alzheimer’s disease is a synaptic failure, Science, 298, 789, 10.1126/science.1074069

Sheng, 2011

Sheng, 2001

Sierra, 2010, Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis, Cell Stem Cell, 7, 483, 10.1016/j.stem.2010.08.014

Silva, 1998, Creb and memory, Annual Review of Neuroscience, 21, 127, 10.1146/annurev.neuro.21.1.127

Silva, 1992, Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice, Science, 257, 206, 10.1126/science.1321493

Siskova, 2010, Morphological and functional abnormalities in mitochondria associated with synaptic degeneration in prion disease, The American Journal of Pathology, 177, 1411, 10.2353/ajpath.2010.091037

Snyder, 2005, Regulation of NMDA receptor trafficking by amyloid-beta, Nature Neuroscience, 8, 1051, 10.1038/nn1503

Sogn, 2013, Rare contacts between synapses and microglial processes containing high levels of Iba1 and actin – A postembedding immunogold study in the healthy rat brain, The European Journal of Neuroscience, 10.1111/ejn.12213

Stellwagen, 2005, Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-α, The Journal of Neuroscience, 25, 3219, 10.1523/JNEUROSCI.4486-04.2005

Stellwagen, 2006, Synaptic scaling mediated by glial TNF-alpha, Nature, 440, 1054, 10.1038/nature04671

Stence, 2001, Dynamics of microglial activation: A confocal time-lapse analysis in hippocampal slices, Glia, 33, 256, 10.1002/1098-1136(200103)33:3<256::AID-GLIA1024>3.0.CO;2-J

Stevens, 2007, The classical complement cascade mediates CNS synapse elimination, Cell, 131, 1164, 10.1016/j.cell.2007.10.036

Streit, 2005, Microglia and neuroprotection: Implications for Alzheimer’s disease, Brain Research Brain Research Reviews, 48, 234, 10.1016/j.brainresrev.2004.12.013

Streit, 2009, Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer’s disease, Acta Neuropathologica, 118, 475, 10.1007/s00401-009-0556-6

Streit, 2004, Microglia and neuroinflammation: A pathological perspective, Journal of Neuroinflammation, 1, 14, 10.1186/1742-2094-1-14

Streit, 2004, Dystrophic microglia in the aging human brain, Glia, 45, 208, 10.1002/glia.10319

Streit, 1999, Reactive microgliosis, Progress in Neurobiology, 57, 563, 10.1016/S0301-0082(98)00069-0

Streit, 2010, The brain’s aging immune system, Aging and Disease, 1, 254

Streit, 2012, Alzheimer’s disease, neuroprotection, and CNS immunosenescence, Frontiers in Pharmacology, 3, 138, 10.3389/fphar.2012.00138

Takahashi, 2005, Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2, The Journal of Experimental Medicine, 201, 647, 10.1084/jem.20041611

Tang, 2001, Total regional and global number of synapses in the human brain neocortex, Synapse, 41, 258, 10.1002/syn.1083

Tashiro, 2003, Structure and molecular organization of dendritic spines, Histology and Histopathology, 18, 617

Terry, 1991, Physical basis of cognitive alterations in alzheimer’s disease: Synapse loss is the major correlate of cognitive impairment, Annals of Neurology, 30, 572, 10.1002/ana.410300410

Thomas, 1992, Brain macrophages: Evaluation of microglia and their functions, Brain Research Reviews, 17, 61, 10.1016/0165-0173(92)90007-9

Thrash, 2009, Developmental regulation of TREM2 and DAP12 expression in the murine CNS: Implications for Nasu–Hakola disease, Neurochemical Research, 34, 38, 10.1007/s11064-008-9657-1

Tonelli, 2005, Tumor necrosis factor alpha, interleukin-1 beta, interleukin-6 and major histocompatibility complex molecules in the normal brain and after peripheral immune challenge, Neurological Research, 27, 679, 10.1179/016164105X49463

Trapp, 2007, Evidence for synaptic stripping by cortical microglia, Glia, 55, 360, 10.1002/glia.20462

Tremblay, 2010, Microglial interactions with synapses are modulated by visual experience, PLoS Biology, 8, e1000527, 10.1371/journal.pbio.1000527

Tremblay, 2011, A role for microglia in synaptic plasticity?, Communicative & Integrative Biology, 4, 220, 10.4161/cib.4.2.14506

Tremblay, 2012, Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices, Glia, 60, 541, 10.1002/glia.22287

Tsien, 1996, The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory, Cell, 87, 1327, 10.1016/S0092-8674(00)81827-9

Tsien, R. Y. (2013). Very long-term memories may be stored in the pattern of holes in the perineuronal net. Proceedings of the National Academy of Sciences of the United States of America.

Tuppo, 2005, The role of inflammation in Alzheimer’s disease, The International Journal of Biochemistry & Cell Biology, 37, 289, 10.1016/j.biocel.2004.07.009

Turnbull, 2006, Cutting edge: TREM-2 attenuates macrophage activation, Journal of Immunology, 177, 3520, 10.4049/jimmunol.177.6.3520

Turrigiano, 2008, The self-tuning neuron: synaptic scaling of excitatory synapses, Cell, 135, 422, 10.1016/j.cell.2008.10.008

van Rossum, 2004, Microglia, Metabolic Brain Disease, 19, 393, 10.1023/B:MEBR.0000043984.73063.d8

Vissel, 2001, A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux, Nature Neuroscience, 4, 587, 10.1038/88404

Vissel, 2001, The role of RNA editing of kainate receptors in synaptic plasticity and seizures, Neuron, 29, 217, 10.1016/S0896-6273(01)00192-1

Wake, 2009, Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals, The Journal of Neuroscience, 29, 3974, 10.1523/JNEUROSCI.4363-08.2009

Walker, 2009, Decreased expression of CD200 and CD200 receptor in Alzheimer’s disease: A potential mechanism leading to chronic inflammation, Experimental Neurology, 215, 5, 10.1016/j.expneurol.2008.09.003

Walsh, 2004, Deciphering the molecular basis of memory failure in Alzheimer’s disease, Neuron, 44, 181, 10.1016/j.neuron.2004.09.010

Wersinger, 2002, Inflammation and Parkinson’s disease, Current Drug Targets Inflammation and Allergy, 1, 221, 10.2174/1568010023344580

Williamson, 2011, Microglia and memory: Modulation by early-life infection, The Journal of Neuroscience, 31, 15511, 10.1523/JNEUROSCI.3688-11.2011

Wilms, 2007, Inflammation in Parkinson’s diseases and other neurodegenerative diseases: Cause and therapeutic implications, Current Pharmaceutical Design, 13, 1925, 10.2174/138161207780858429

Wiltgen, 2010, A role for calcium-permeable AMPA receptors in synaptic plasticity and learning, PLoS One, 5, 10.1371/journal.pone.0012818

Winder, 1998, Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin, Cell, 92, 25, 10.1016/S0092-8674(00)80896-X

Wolf, Y., Yona, S., Kim, K-W., & Jung, S. (2013). Microglia, seen from the CX3CR1 angle. Frontiers in Cellular Neuroscience, 7.

Wong, 2013, Microglial aging in the healthy CNS: Phenotypes, drivers, and rejuvenation, Frontiers in Cellular Neuroscience, 7, 22, 10.3389/fncel.2013.00022

Wright, 2013, Neuroinflammation and neuronal loss precede abeta plaque deposition in the hAPP-J20 mouse model of Alzheimer’s disease, PLoS One, 8, e59586, 10.1371/journal.pone.0059586

Wu, 2008, Resting microglial motility is independent of synaptic plasticity in mammalian brain, Journal of Neurophysiology, 99, 2026, 10.1152/jn.01210.2007

Wyss-Coray, 2012, Inflammation in Alzheimer disease—A brief review of the basic science and clinical literature, Cold Spring Harbor Perspectives in Medicine, 2, 10.1101/cshperspect.a006346

Xiao, 2001, Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors, Neuropharmacology, 41, 664, 10.1016/S0028-3908(01)00134-4

Xu, 2007, Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex, Nature Neuroscience, 10, 549, 10.1038/nn1883

Yamada, 2008, Reduced synaptic activity precedes synaptic stripping in vagal motoneurons after axotomy, Glia, 56, 1448, 10.1002/glia.20711

Yang, 2009, Stably maintained dendritic spines are associated with lifelong memories, Nature, 462, 920, 10.1038/nature08577

Yirmiya, 2011, Immune modulation of learning, memory, neural plasticity and neurogenesis, Brain, Behavior, and Immunity, 25, 181, 10.1016/j.bbi.2010.10.015

Yuste, 2001, On the function of dendritic spines, Neuroscientist, 7, 387, 10.1177/107385840100700508

Zhang, 2013, Hypothalamic programming of systemic ageing involving IKK-beta, NF-kappaB and GnRH, Nature, 497, 211, 10.1038/nature12143

Zhou, 2004, Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses, Neuron, 44, 749, 10.1016/j.neuron.2004.11.011

Zuo, 2005, Development of long-term dendritic spine stability in diverse regions of cerebral cortex, Neuron, 46, 181, 10.1016/j.neuron.2005.04.001