1.
Werneburg, S., Feinberg, P. A., Johnson, K. M. & Schafer, D. P. A microglia-cytokine axis to modulate synaptic connectivity and function. Curr. Opin. Neurobiol. 47, 138–145 (2017).
CAS
PubMed
PubMed Central
Article
Google Scholar
2.
Li, Y., Du, X. F., Liu, C. S., Wen, Z. L. & Du, J. L. Reciprocal regulation between resting microglial dynamics and neuronal activity in vivo. Dev. Cell 23, 1189–1202 (2012).
CAS
PubMed
Article
PubMed Central
Google Scholar
3.
Eyo, U. B. et al. Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. J. Neurosci. 34, 10528–10540 (2014).
PubMed
PubMed Central
Article
CAS
Google Scholar
4.
Akiyoshi, R. et al. Microglia enhance synapse activity to promote local network synchronization. eNeuro 5, ENEURO.0088-18.2018 (2018).
PubMed
PubMed Central
Article
Google Scholar
5.
Kato, G. et al. Microglial contact prevents excess depolarization and rescues neurons from excitotoxicity. eNeuro 3, ENEURO.0004-16.2016 (2016).
PubMed
PubMed Central
Article
Google Scholar
6.
Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S. & Nabekura, J. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974–3980 (2009).
CAS
PubMed
PubMed Central
Article
Google Scholar
7.
Peng, J. et al. Microglial P2Y12 receptor regulates ventral hippocampal CA1 neuronal excitability and innate fear in mice. Mol. Brain 12, 71 (2019).
PubMed
PubMed Central
Article
CAS
Google Scholar
8.
Cserép, C. et al. Microglia monitor and protect neuronal function through specialized somatic purinergic junctions. Science 367, 528–537 (2020).
ADS
PubMed
Article
CAS
PubMed Central
Google Scholar
9.
Bernier, L. P. et al. Nanoscale surveillance of the brain by microglia via cAMP-regulated filopodia. Cell Rep. 27, 2895–2908.e4 (2019).
CAS
PubMed
Article
PubMed Central
Google Scholar
10.
Madry, C. et al. Microglial ramification, surveillance, and interleukin-1β release are regulated by the two-pore domain K+ channel THIK-1. Neuron 97, 299–312.e6 (2018).
CAS
PubMed
PubMed Central
Article
Google Scholar
11.
Liu, Y. U. et al. Neuronal network activity controls microglial process surveillance in awake mice via norepinephrine signaling. Nat. Neurosci. 22, 1771–1781 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
12.
Stowell, R. D. et al. Noradrenergic signaling in the wakeful state inhibits microglial surveillance and synaptic plasticity in the mouse visual cortex. Nat. Neurosci. 22, 1782–1792 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
13.
Elmore, M. R. P. et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron 82, 380–397 (2014).
CAS
PubMed
PubMed Central
Article
Google Scholar
14.
Bozzi, Y. & Borrelli, E. The role of dopamine signaling in epileptogenesis. Front. Cell. Neurosci. 7, 157 (2013).
PubMed
PubMed Central
Article
CAS
Google Scholar
15.
Chitu, V., Gokhan, Ş., Nandi, S., Mehler, M. F. & Stanley, E. R. Emerging roles for CSF-1 receptor and its ligands in the nervous system. Trends Neurosci. 39, 378–393 (2016).
CAS
PubMed
PubMed Central
Article
Google Scholar
16.
Kana, V. et al. CSF-1 controls cerebellar microglia and is required for motor function and social interaction. J. Exp. Med. 216, 2265–2281 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
17.
Easley-Neal, C., Foreman, O., Sharma, N., Zarrin, A. A. & Weimer, R. M. CSF1R ligands IL-34 and CSF1 are differentially required for microglia development and maintenance in white and gray matter brain regions. Front. Immunol. 10, 2199 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
18.
Saunders, A. et al. Molecular diversity and specializations among the cells of the adult mouse brain. Cell 174, 1015–1030.e16 (2018).
CAS
PubMed
PubMed Central
Article
Google Scholar
19.
Wenzel, M., Hamm, J. P., Peterka, D. S. & Yuste, R. Acute focal seizures start as local synchronizations of neuronal ensembles. J. Neurosci. 39, 8562–8575 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
20.
Pankratov, Y., Lalo, U., Verkhratsky, A. & North, R. A. Vesicular release of ATP at central synapses. Pflugers Arch. 452, 589–597 (2006).
CAS
PubMed
Article
Google Scholar
21.
Pascual, O. et al. Neurobiology: astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113–116 (2005).
ADS
CAS
PubMed
Article
Google Scholar
22.
Corkrum, M. et al. Dopamine-evoked synaptic regulation in the nucleus accumbens requires astrocyte activity. Neuron 105, 1036–1047.e5 (2020).
CAS
PubMed
Article
Google Scholar
23.
Beamer, E., Conte, G. & Engel, T. ATP release during seizures—a critical evaluation of the evidence. Brain Res. Bull. 151, 65–73 (2019).
CAS
PubMed
Article
Google Scholar
24.
Haynes, S. E. et al. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat. Neurosci. 9, 1512–1519 (2006).
CAS
PubMed
Article
Google Scholar
25.
Ayata, P. et al. Epigenetic regulation of brain region-specific microglia clearance activity. Nat. Neurosci. 21, 1049–1060 (2018).
CAS
PubMed
PubMed Central
Article
Google Scholar
26.
Madry, C. et al. Effects of the ecto-ATPase apyrase on microglial ramification and surveillance reflect cell depolarization, not ATP depletion. Proc. Natl Acad. Sci. USA 115, E1608–E1617 (2018).
CAS
PubMed
Article
PubMed Central
Google Scholar
27.
Dissing-Olesen, L. et al. Activation of neuronal NMDA receptors triggers transient ATP-mediated microglial process outgrowth. J. Neurosci. 34, 10511–10527 (2014).
PubMed
PubMed Central
Article
CAS
Google Scholar
28.
Robson, S. C., Sévigny, J. & Zimmermann, H. The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal. 2, 409–430 (2006).
CAS
PubMed
PubMed Central
Article
Google Scholar
29.
Lanser, A. J. et al. Disruption of the ATP/adenosine balance in CD39−/− mice is associated with handling-induced seizures. Immunology 152, 589–601 (2017).
CAS
PubMed
PubMed Central
Article
Google Scholar
30.
Dunwiddie, T. V. & Masino, S. A. The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24, 31–55 (2001).
CAS
PubMed
Article
PubMed Central
Google Scholar
31.
Zimmermann, H., Zebisch, M. & Sträter, N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal. 8, 437–502 (2012).
CAS
PubMed
PubMed Central
Article
Google Scholar
32.
Flagmeyer, I., Haas, H. L. & Stevens, D. R. Adenosine A1 receptor-mediated depression of corticostriatal and thalamostriatal glutamatergic synaptic potentials in vitro. Brain Res. 778, 178–185 (1997).
CAS
PubMed
Article
PubMed Central
Google Scholar
33.
Yabuuchi, K. et al. Role of adenosine A1 receptors in the modulation of dopamine D1 and adenosine A2A receptor signaling in the neostriatum. Neuroscience 141, 19–25 (2006).
CAS
PubMed
Article
PubMed Central
Google Scholar
34.
Trusel, M. et al. Coordinated regulation of synaptic plasticity at striatopallidal and striatonigral neurons orchestrates motor control. Cell Rep. 13, 1353–1365 (2015).
CAS
PubMed
Article
PubMed Central
Google Scholar
35.
Zhou, S. et al. Pro-inflammatory effect of downregulated CD73 expression in EAE astrocytes. Front. Cell. Neurosci. 13, 233 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
36.
Bateup, H. S. et al. Cell type-specific regulation of DARPP-32 phosphorylation by psychostimulant and antipsychotic drugs. Nat. Neurosci. 11, 932–939 (2008).
CAS
PubMed
PubMed Central
Article
Google Scholar
37.
Wendeln, A. C. et al. Innate immune memory in the brain shapes neurological disease hallmarks. Nature 556, 332–338 (2018).
ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
38.
Süß, P. et al. Chronic peripheral inflammation causes a region-specific myeloid response in the central nervous system. Cell Rep. 30, 4082–4095.e6 (2020).
PubMed
Article
CAS
PubMed Central
Google Scholar
39.
Krasemann, S. et al. The TREM2–APOE pathway drives the transcriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity 47, 566–581.e9 (2017).
CAS
PubMed
PubMed Central
Article
Google Scholar
40.
Mildner, A., Huang, H., Radke, J., Stenzel, W. & Priller, J. P2Y12 receptor is expressed on human microglia under physiological conditions throughout development and is sensitive to neuroinflammatory diseases. Glia 65, 375–387 (2017).
PubMed
Article
PubMed Central
Google Scholar
41.
Palop, J. J. et al. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer’s disease. Neuron 55, 697–711 (2007).
CAS
PubMed
PubMed Central
Article
Google Scholar
42.
Lam, A. D. et al. Silent hippocampal seizures and spikes identified by foramen ovale electrodes in Alzheimer’s disease. Nat. Med. 23, 678–680 (2017).
CAS
PubMed
PubMed Central
Article
Google Scholar
43.
Wohleb, E. S., Franklin, T., Iwata, M. & Duman, R. S. Integrating neuroimmune systems in the neurobiology of depression. Nat. Rev. Neurosci. 17, 497–511 (2016).
CAS
PubMed
Article
PubMed Central
Google Scholar
44.
Spangenberg, E. E. et al. Eliminating microglia in Alzheimer’s mice prevents neuronal loss without modulating amyloid-β pathology. Brain 139, 1265–1281 (2016).
PubMed
PubMed Central
Article
Google Scholar
45.
Bejar, R., Yasuda, R., Krugers, H., Hood, K. & Mayford, M. Transgenic calmodulin-dependent protein kinase II activation: dose-dependent effects on synaptic plasticity, learning, and memory. J. Neurosci. 22, 5719–5726 (2002).
CAS
PubMed
PubMed Central
Article
Google Scholar
46.
Alexander, G. M. et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63, 27–39 (2009).
CAS
PubMed
PubMed Central
Article
Google Scholar
47.
Stanley, S. et al. Profiling of glucose-sensing neurons reveals that ghrh neurons are activated by hypoglycemia. Cell Metab. 18, 596–607 (2013).
CAS
PubMed
Article
PubMed Central
Google Scholar
48.
Parkhurst, C. N. et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell 155, 1596–1609 (2013).
CAS
PubMed
PubMed Central
Article
Google Scholar
49.
Wang, Y. et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13, 753–760 (2012).
CAS
PubMed
PubMed Central
Article
Google Scholar
50.
Tronche, F. et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat. Genet. 23, 99–103 (1999).
CAS
PubMed
Article
PubMed Central
Google Scholar
51.
Harris, S. E. et al. Meox2Cre-mediated disruption of CSF-1 leads to osteopetrosis and osteocyte defects. Bone 50, 42–53 (2012).
CAS
PubMed
Article
PubMed Central
Google Scholar
52.
Rothweiler, S. et al. Selective deletion of ENTPD1/CD39 in macrophages exacerbates biliary fibrosis in a mouse model of sclerosing cholangitis. Purinergic Signal. 15, 375–385 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
53.
Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).
CAS
PubMed
Article
PubMed Central
Google Scholar
54.
Scammell, T. E. et al. Focal deletion of the adenosine A1 receptor in adult mice using an adeno-associated viral vector. J. Neurosci. 23, 5762–5770 (2003).
CAS
PubMed
PubMed Central
Article
Google Scholar
55.
Thompson, L. F. et al. Crucial role for ecto-5′-nucleotidase (CD73) in vascular leakage during hypoxia. J. Exp. Med. 200, 1395–1405 (2004).
CAS
PubMed
PubMed Central
Article
Google Scholar
56.
André, P. et al. P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. J. Clin. Invest. 112, 398–406 (2003).
PubMed
PubMed Central
Article
Google Scholar
57.
Oakley, H. et al. Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129–10140 (2006).
CAS
PubMed
PubMed Central
Article
Google Scholar
58.
Casanova, E. et al. A CamKIIα iCre BAC allows brain-specific gene inactivation. Genesis 31, 37–42 (2001).
CAS
PubMed
Article
PubMed Central
Google Scholar
59.
Doyle, J. P. et al. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135, 749–762 (2008).
CAS
PubMed
PubMed Central
Article
Google Scholar
60.
Heiman, M. et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738–748 (2008).
CAS
PubMed
PubMed Central
Article
Google Scholar
61.
von Schimmelmann, M. et al. Polycomb repressive complex 2 (PRC2) silences genes responsible for neurodegeneration. Nat. Neurosci. 19, 1321–1330 (2016).
Article
CAS
Google Scholar
62.
Kim, D. & Salzberg, S. L. TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol. 12, R72 (2011).
CAS
PubMed
PubMed Central
Article
Google Scholar
63.
Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).
CAS
PubMed
PubMed Central
Article
Google Scholar
64.
Purushothaman, I. & Shen, L. SPEctRA: a scalable pipeline for RNA -seq ana lysis. https://zenodo.org/record/60547#.X1khQDNKjIU (2016).
65.
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
PubMed
PubMed Central
Article
CAS
Google Scholar
66.
Liddelow, S. A. et al. Neurotoxic reactive astrocytes are induced by activated microglia. Nature 541, 481–487 (2017).
ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
67.
Hickman, S. E. et al. The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16, 1896–1905 (2013).
CAS
PubMed
PubMed Central
Article
Google Scholar
68.
Howe, E. A., Sinha, R., Schlauch, D. & Quackenbush, J. RNA-seq analysis in MeV. Bioinformatics 27, 3209–3210 (2011).
CAS
PubMed
PubMed Central
Article
Google Scholar
69.
Chen, E. Y. et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128 (2013).
PubMed
PubMed Central
Article
Google Scholar
70.
Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44 (W1), W90−W97 (2016).
CAS
PubMed
PubMed Central
Article
Google Scholar
71.
Gokce, O. et al. Cellular taxonomy of the mouse striatum as revealed by single-cell RNA-seq. Cell Rep. 16, 1126–1137 (2016).
CAS
PubMed
PubMed Central
Article
Google Scholar
72.
Bohlen, C. J., Bennett, F. C. & Bennett, M. L. Isolation and culture of microglia. Curr. Protoc. Immunol. 125, e70 (2019).
PubMed
Article
CAS
PubMed Central
Google Scholar
73.
Butovsky, O. et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci. 17, 131–143 (2014).
CAS
PubMed
Article
PubMed Central
Google Scholar
74.
Gabriel, L. R., Wu, S. & Melikian, H. E. Brain slice biotinylation: an ex vivo approach to measure region-specific plasma membrane protein trafficking in adult neurons. J. Vis. Exp. 86, e51240 (2014).
Google Scholar
75.
Crupi, M. J. F., Richardson, D. S. & Mulligan, L. M. Cell surface biotinylation of receptor tyrosine kinases to investigate intracellular trafficking. Methods Mol. Biol. 1233, 91–102 (2015).
PubMed
Article
PubMed Central
Google Scholar
76.
Sullivan, J. M. et al. Autism-like syndrome is induced by pharmacological suppression of BET proteins in young mice. J. Exp. Med. 212, 1771–1781 (2015).
CAS
PubMed
PubMed Central
Article
Google Scholar
77.
Pnevmatikakis, E. A. & Giovannucci, A. NoRMCorre: an online algorithm for piecewise rigid motion correction of calcium imaging data. J. Neurosci. Methods 291, 83–94 (2017).
CAS
PubMed
Article
PubMed Central
Google Scholar
78.
Pachitariu, M. et al. Suite2p: beyond 10,000 neurons with standard two-photon microscopy. Preprint at https://www.biorxiv.org/content/10.1101/061507v2 (2016).
79.
Yoder, N. C. peakfinder(x0, sel, thresh, extrema, includeEndpoints, interpolate). https://www.mathworks.com/matlabcentral/fileexchange/25500-peakfinder-x0-sel-thresh-extrema-includeendpoints-interpolate (Matlab Central File Exchange, 2016).
80.
Klaus, A. et al. The spatiotemporal organization of the striatum encodes action space. Neuron 95, 1171–1180.e7 (2017).
CAS
PubMed
PubMed Central
Article
Google Scholar
81.
Barbera, G. et al. Spatially compact neural clusters in the dorsal striatum encode locomotion relevant information. Neuron 92, 202–213 (2016).
CAS
PubMed
PubMed Central
Article
Google Scholar
82.
Kato, D. et al. in Microglia. Methods in Molecular Biology (eds. Garaschuk, O. & Verkhratsky A.) (Humana, 2019).
83.
Thévenaz, P., Ruttimann, U. E. & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27–41 (1998).
ADS
PubMed
Article
PubMed Central
Google Scholar
84.
Ting, J. T. et al. Preparation of acute brain slices using an optimized N-methyl-d-glucamine protective recovery method. J. Vis. Exp. 132, e53825 (2018).
Google Scholar
85.
Fieblinger, T. et al. Cell type-specific plasticity of striatal projection neurons in parkinsonism and L-DOPA-induced dyskinesia. Nat. Commun. 5, 5316 (2014).
ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
86.
Graves, S. M. & Surmeier, D. J. Delayed spine pruning of direct pathway spiny projection neurons in a mouse model of parkinson’s disease. Front. Cell. Neurosci. 13, 32 (2019).
CAS
PubMed
PubMed Central
Article
Google Scholar
87.
Wong, J. M. T. et al. Benzoyl chloride derivatization with liquid chromatography-mass spectrometry for targeted metabolomics of neurochemicals in biological samples. J. Chromatogr. A 1446, 78–90 (2016).
CAS
PubMed
PubMed Central
Article
Google Scholar
88.
Gangarossa, G. et al. Convulsant doses of a dopamine D1 receptor agonist result in Erk-dependent increases in Zif268 and Arc/Arg3.1 expression in mouse dentate gyrus. PLoS One 6, e19415 (2011).
ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
89.
Bunch, L. & Krogsgaard-Larsen, P. Subtype selective kainic acid receptor agonists: discovery and approaches to rational design. Med. Res. Rev. 29, 3–28 (2009).
CAS
PubMed
Article
PubMed Central
Google Scholar
90.
Willoughby, J. O., Mackenzie, L., Medvedev, A. & Hiscock, J. J. Distribution of Fos-positive neurons in cortical and subcortical structures after picrotoxin-induced convulsions varies with seizure type. Brain Res. 683, 73–87 (1995).
CAS
PubMed
Article
PubMed Central
Google Scholar
91.
Sipe, G. O. et al. Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex. Nat. Commun. 7, 10905 (2016).
ADS
CAS
PubMed
PubMed Central
Article
Google Scholar
92.
Racine, R. J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281–294 (1972).
CAS
PubMed
Article
PubMed Central
Google Scholar
93.
Silverman, J. L., Yang, M., Lord, C. & Crawley, J. N. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 11, 490–502 (2010).
CAS
PubMed
PubMed Central
Article
Google Scholar
94.
Langfelder, P. et al. Integrated genomics and proteomics define huntingtin CAG length-dependent networks in mice. Nat. Neurosci. 19, 623–633 (2016).
CAS
PubMed
PubMed Central
Article
Google Scholar
95.
Wang, Y. et al. TREM2 lipid sensing sustains the microglial response in an Alzheimer’s disease model. Cell 160, 1061–1071 (2015).
CAS
PubMed
PubMed Central
Article
Google Scholar
96.
Keren-Shaul, H. et al. A unique microglia type associated with restricting development of Alzheimer’s disease. Cell 169, 1276–1290.e17 (2017).
CAS
PubMed
Article
PubMed Central
Google Scholar
97.
Sousa, C. et al. Single-cell transcriptomics reveals distinct inflammation-induced microglia signatures. EMBO Rep. 19, e46171 (2018).
PubMed
PubMed Central
Article
CAS
Google Scholar