Neuroplasticity in stroke recovery. The role of microglia in engaging and modifying synapses and networks
Open accessAbstract
Neuroplasticity after ischaemic injury involves both spontaneous rewiring of neural networks and circuits as well as functional responses in neurogenic niches. These events involve complex interactions with activated microglia, which evolve in a dynamic manner over time. Although the exact mechanisms underlying these interactions remain poorly understood, increasing experimental evidence suggests a determining role of pro‐ and anti‐inflammatory microglial activation profiles in shaping both synaptogenesis and neurogenesis. While the inflammatory response of microglia was thought to be detrimental, a more complex profile of the role of microglia in tissue remodelling is emerging. Experimental evidence suggests that microglia in response to injury can rapidly modify neuronal activity and modulate synaptic function, as well as be beneficial for the proliferation and integration of neural progenitor cells (NPC s) from endogenous neurogenic niches into functional networks thereby supporting stroke recovery. The manner in which microglia contribute towards sculpting neural synapses and networks, both in terms of activity‐dependent and homeostatic plasticity, suggests that microglia‐mediated pro‐ and/or anti‐inflammatory activity may significantly contribute towards spontaneous neuronal plasticity after ischaemic lesions. In this review, we first introduce some of the key cellular and molecular mechanisms underlying neuroplasticity in stroke and then proceed to discuss the crosstalk between microglia and endogenous neuroplasticity in response to brain ischaemia with special focus on the engagement of synapses and neural networks and their implications for grey matter integrity and function in stroke repair.
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Microglia are postulated to degrade PNNs in some disease states, probably via increased extracellular proteases.
“it has been postulated that microglia mediate the degradation of PNNs in certain disease states, likely through enhanced production of extracellular proteases”
From Microglial depletion prevents extracellular matrix changes and striatal volume reduction in a model of Huntington's disease (2020) · cites this paper as Sandvig et al., 2018
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1 retracted
Bialas, A. R., & Stevens, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3560 · Cited by 519 · see citing works
RetractedHeart Disease and Stroke Statistics—2017 Update: A Report From the American Heart Association
Benjamin, E. J., Blaha, M. J., Chiuve, S. E., Cushman, M., Das, S. R., Deo, R., de Ferranti, S. D., Floyd, J., Fornage, M., Gillespie, C., et al. (2017) · Circulation · doi:10.1161/cir.0000000000000485 · Cited by 12,591 · see citing works
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984 · see citing works
Heart Disease and Stroke Statistics—2016 Update: A Report From the American Heart Association
Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., Das, S. R., de Ferranti, S., Després, J.-P., Fullerton, H. J., et al. (2016) · Circulation · doi:10.1161/cir.0000000000000350 · Cited by 6,596 · see citing works
Alternative activation of macrophages
Gordon, S. (2003) · Nature Reviews Immunology · doi:10.1038/nri978 · Cited by 6,189 · see citing works
Heart Disease and Stroke Statistics—2015 Update: A Report From the American Heart Association
Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., de Ferranti, S., Després, J.-P., Fullerton, H. J., Howard, V. J., et al. (2015) · Circulation · doi:10.1161/cir.0000000000000152 · Cited by 5,797 · see citing works
Fate Mapping Analysis Reveals That Adult Microglia Derive from Primitive Macrophages
Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., Mehler, M. F., Conway, S. J., Ng, L. G., Stanley, E. R., et al. (2010) · Science · doi:10.1126/science.1194637 · Cited by 5,175 · see citing works
Synaptic Pruning by Microglia Is Necessary for Normal Brain Development
Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T. A., Guiducci, E., Dumas, L., et al. (2011) · Science · doi:10.1126/science.1202529 · Cited by 4,244 · see citing works
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
ATP mediates rapid microglial response to local brain injury in vivo
Davalos, D., Grutzendler, J., Yang, G., Kim, J. V., Zuo, Y., Jung, S., Littman, D. R., Dustin, M. L., & Gan, W.-B. (2005) · Nature Neuroscience · doi:10.1038/nn1472 · Cited by 3,913 · see citing works
Microglia: Active sensor and versatile effector cells in the normal and pathologic brain
Hanisch, U.-K., & Kettenmann, H. (2007) · Nature Neuroscience · doi:10.1038/nn1997 · Cited by 3,676 · see citing works
Kettenmann, H., Hanisch, U.-K., Noda, M., & Verkhratsky, A. (2011) · Physiological Reviews · doi:10.1152/physrev.00011.2010 · Cited by 3,547 · see citing works
The Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313 · see citing works
Neuronal replacement from endogenous precursors in the adult brain after stroke
Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., & Lindvall, O. (2002) · Nature Medicine · doi:10.1038/nm747 · Cited by 2,799 · see citing works
Alternative Activation of Macrophages: An Immunologic Functional Perspective
Martinez, F. O., Helming, L., & Gordon, S. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132532 · Cited by 2,745 · see citing works
Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4106-4114.2000 · Cited by 2,632 · see citing works
Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor
Parkhurst, C. N., Yang, G., Ninan, I., Savas, J. N., Yates, J. R., Lafaille, J. J., Hempstead, B. L., Littman, D. R., & Gan, W.-B. (2013) · Cell · doi:10.1016/j.cell.2013.11.030 · Cited by 2,599 · see citing works
The immunology of stroke: from mechanisms to translation
Iadecola, C., & Anrather, J. (2011) · Nature Medicine · doi:10.1038/nm.2399 · Cited by 2,596 · see citing works
Identification of a unique TGF-β–dependent molecular and functional signature in microglia
Butovsky, O., Jedrychowski, M. P., Moore, C. S., Cialic, R., Lanser, A. J., Gabriely, G., Koeglsperger, T., Dake, B., Wu, P. M., Doykan, C. E., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3599 · Cited by 2,543 · see citing works
Homeostatic plasticity in the developing nervous system
Turrigiano, G. G., & Nelson, S. B. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1327 · Cited by 2,485 · see citing works
The Glial Nature of Embryonic and Adult Neural Stem Cells
Kriegstein, A., & Alvarez-Buylla, A. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135600 · Cited by 2,475 · see citing works
Critical period plasticity in local cortical circuits
Hensch, T. K. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1787 · Cited by 2,323 · see citing works
Transcriptional regulation of macrophage polarization: enabling diversity with identity
Lawrence, T., & Natoli, G. (2011) · Nature Reviews Immunology · doi:10.1038/nri3088 · Cited by 2,284 · see citing works
Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain
Lawson, L. J., Perry, V. H., Dri, P., & Gordon, S. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90229-w · Cited by 2,045 · see citing works
Elmore, M. R. P., Najafi, A. R., Koike, M. A., Dagher, N. N., Spangenberg, E. E., Rice, R. A., Kitazawa, M., Matusow, B., Nguyen, H., West, B. L., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.040 · Cited by 1,968 · see citing works
Nathan, C. F., Murray, H. W., Wiebe, M. E., & Rubin, B. Y. (1983) · The Journal of experimental medicine · doi:10.1084/jem.158.3.670 · Cited by 1,962 · see citing works
Synaptic scaling mediated by glial TNF-α
Stellwagen, D., & Malenka, R. C. (2006) · Nature · doi:10.1038/nature04671 · Cited by 1,715 · see citing works
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679 · see citing works
Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S., & Nabekura, J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4363-08.2009 · Cited by 1,619 · see citing works
Inflammation is detrimental for neurogenesis in adult brain
Ekdahl, C. T., Claasen, J.-H., Bonde, S., Kokaia, Z., & Lindvall, O. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2234031100 · Cited by 1,559 · see citing works
Microglial interactions with synapses are modulated by visual experience
Tremblay, M.-È., Lowery, R. L., & Majewska, A. K. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000527 · Cited by 1,542 · see citing works
Control of microglial neurotoxicity by the fractalkine receptor
Cardona, A. E., Pioro, E. P., Sasse, M. E., Kostenko, V., Cardona, S. M., Dijkstra, I. M., Huang, D., Kidd, G., Dombrowski, S., Dutta, R., et al. (2006) · Nature Neuroscience · doi:10.1038/nn1715 · Cited by 1,531 · see citing works
The microglial sensome revealed by direct RNA sequencing
Hickman, S. E., Kingery, N. D., Ohsumi, T. K., Borowsky, M. L., Wang, L.-C., Means, T. K., & El Khoury, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3554 · Cited by 1,511 · see citing works
Hu, X.-M., Li, P.-Y., Guo, Y., Wang, H., Leak, R., Chen, S., Gao, Y.-Q., & Chen, J. (2012) · Stroke · doi:10.1161/strokeaha.112.659656 · Cited by 1,445 · see citing works
Harrison, J. K., Jiang, Y., Chen, S., Xia, Y., Maciejewski, D., McNamara, R. K., Streit, W. J., Salafranca, M. N., Adhikari, S., Thompson, D. A., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10896 · Cited by 1,176 · see citing works
Microglia: new roles for the synaptic stripper
Kettenmann, H., Kirchhoff, F., & Verkhratsky, A. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.023 · Cited by 1,173 · see citing works
Imitola, J., Raddassi, K., Park, K. I., Müeller, F.-J., Nieto, M., Teng, Y. D., Frenkel, D., Li, J., Sidman, R. L., Walsh, C. A., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408258102 · Cited by 1,056 · see citing works
Fitch, M. T., & Silver, J. (2008) · Experimental Neurology · doi:10.1016/j.expneurol.2007.05.014 · Cited by 1,007 · see citing works
Butovsky, O., Ziv, Y., Schwartz, A., Landa, G., Talpalar, A. E., Pluchino, S., Martino, G., & Schwartz, M. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.10.006 · Cited by 923 · see citing works
Polydendrocytes (NG2 cells): multifunctional cells with lineage plasticity
Nishiyama, A., Komitova, M., Suzuki, R., & Zhu, X. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2495 · Cited by 865 · see citing works
IL-1β is an essential mediator of the antineurogenic and anhedonic effects of stress
Koo, J. W., & Duman, R. S. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708092105 · Cited by 862 · see citing works
Brain inflammation and adult neurogenesis: The dual role of microglia
Ekdahl, C. T., Kokaia, Z., & Lindvall, O. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.052 · Cited by 801 · see citing works
Layer V cortical neurons require microglial support for survival during postnatal development
Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., & Yamashita, T. (2013) · Nature Neuroscience · doi:10.1038/nn.3358 · Cited by 781 · see citing works
Turnover of resident microglia in the normal adult mouse brain
Lawson, L. J., Perry, V. H., & Gordon, S. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90500-2 · Cited by 709 · see citing works
Neurogenesis in the Hypothalamus of Adult Mice: Potential Role in Energy Balance
Kokoeva, M. V., Yin, H., & Flier, J. S. (2005) · Science · doi:10.1126/science.1115360 · Cited by 704 · see citing works
Spatiotemporal Dynamics of Cortical Sensorimotor Integration in Behaving Mice
Férézou, I., Haiss, F., Gentet, L. J., Aronoff, R., Weber, B., & Petersen, C. C. H. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.007 · Cited by 692 · see citing works
The bright side of the glial scar in CNS repair
Rolls, A., Shechter, R., & Schwartz, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2591 · Cited by 674 · see citing works
Microglia: Dynamic Mediators of Synapse Development and Plasticity
Wu, Y., Dissing-Olesen, L., MacVicar, B. A., & Stevens, B. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.08.008 · Cited by 661 · see citing works
How widespread is adult neurogenesis in mammals?
Gould, E. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2147 · Cited by 658 · see citing works
Neurotransmitter receptors on microglia
Pocock, J. M., & Kettenmann, H. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.07.007 · Cited by 650 · see citing works
Porta, C., Rimoldi, M., Raes, G., Brys, L., Ghezzi, P., Di Liberto, D., Dieli, F., Ghisletti, S., Natoli, G., De Baetselier, P., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0809784106 · Cited by 627 · see citing works
Reciprocal Regulation between Resting Microglial Dynamics and Neuronal Activity In Vivo
Li, Y., Du, X.-F., Liu, C., Wen, Z., & Du, J. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.10.027 · Cited by 553 · see citing works
Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex
Sipe, G. O., Lowery, Tremblay, M.-È., Kelly, E. A., Lamantia, C. E., & Majewska, A. K. (2016) · Nature Communications · doi:10.1038/ncomms10905 · Cited by 512 · see citing works
Eyo, U. B., Peng, J., Swiatkowski, P., Mukherjee, A., Bispo, A., & Wu, L.-J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0416-14.2014 · Cited by 509 · see citing works
Morrison, H. W., & Filosa, J. A. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-4 · Cited by 506 · see citing works
Perego, C., Fumagalli, S., & Simoni, M. G. D. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-174 · Cited by 504 · see citing works
Pathophysiology and therapy of experimental stroke
Hossmann, K.-A. (2006) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-006-9008-1 · Cited by 475 · see citing works
Madry, C., Kyrargyri, V., Arancibia-Cárcamo, I. L., Jolivet, R., Kohsaka, S., Bryan, R. M., & Attwell, D. (2018) · Neuron · doi:10.1016/j.neuron.2017.12.002 · Cited by 464 · see citing works
Thored, P., Wood, J., Arvidsson, A., Cammenga, J., Kokaia, Z., & Lindvall, O. (2007) · Stroke · doi:10.1161/strokeaha.107.488445 · Cited by 421 · see citing works
Actions of TNF‐α on glutamatergic synaptic transmission in the central nervous system
Pickering, M., Cumiskey, D., & O'Connor, J. J. (2005) · Experimental Physiology · doi:10.1113/expphysiol.2005.030734 · Cited by 411 · see citing works
Regulation of microglial activation in stroke
Zhao, S.-C., Ma, L.-S., Chu, Z., Xu, H., Wu, W.-Q., & Liu, F. (2017) · Acta Pharmacologica Sinica · doi:10.1038/aps.2016.162 · Cited by 411 · see citing works
The soft mechanical signature of glial scars in the central nervous system
Moeendarbary, E., Weber, I. P., Sheridan, G. K., Koser, D. E., Soleman, S., Haenzi, B., Bradbury, E. J., Fawcett, J. W., & Franze, K. (2017) · Nature Communications · doi:10.1038/ncomms14787 · Cited by 408 · see citing works
Structure of IRF-1 with bound DNA reveals determinants of interferon regulation
Escalante, C. R., Yie, J., Thanos, D., & Aggarwal, A. K. (1998) · Nature · doi:10.1038/34224 · Cited by 397 · see citing works
Sandvig, A., Berry, M., Barrett, L. B., Butt, A. M., & Logan, A. (2004) · Glia · doi:10.1002/glia.10315 · Cited by 378 · see citing works
Self-citationStructural and functional recovery from early monocular deprivation in adult rats
Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N., & Maffei, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602657103 · Cited by 367 · see citing works
Microglia and ischemic stroke: a double-edged sword.
Patel, A. R., Ritzel, R. M., McCullough, L. D., & Liu, F. (2013) · Europe PMC (PubMed Central) · Cited by 355 · see citing works
Cortical Reorganization After Stroke
Grefkes, C., & Ward, N. (2013) · The Neuroscientist · doi:10.1177/1073858413491147 · Cited by 346 · see citing works
Fontainhas, A. M., Wang, M., Liang, K. J., Chen, S., Mettu, P., Damani, M., Fariss, R. N., Li, W., & Wong, W. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0015973 · Cited by 334 · see citing works
Hermann, D. M., & Chopp, M. (2012) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70039-x · Cited by 333 · see citing works
Recovery recapitulates ontogeny
Cramer, S. C., & Chopp, M. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01562-9 · Cited by 326 · see citing works
Microglial displacement of inhibitory synapses provides neuroprotection in the adult brain
Chen, Z., Jalabi, W., Hu, W., Park, H.-J., Gale, J. T., Kidd, G. J., Bernatowicz, R., Gossman, Z. C., Chen, J. T., Dutta, R., et al. (2014) · Nature Communications · doi:10.1038/ncomms5486 · Cited by 319 · see citing works
Schiene, K., Bruehl, C., Zilles, K., Qü, M., Hagemann, G., Kraemer, M., & Witte, O. W. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199609000-00014 · Cited by 309 · see citing works
Effects of aging and sensory loss on glial cells in mouse visual and auditory cortices
Tremblay, M., Zettel, M. L., Ison, J. R., Allen, P. D., & Majewska, A. K. (2012) · Glia · doi:10.1002/glia.22287 · Cited by 309 · see citing works
Activation of Neuronal NMDA Receptors Triggers Transient ATP-Mediated Microglial Process Outgrowth
Dissing-Olesen, L., LeDue, J. M., Rungta, R. L., Hefendehl, J. K., Choi, H. B., & MacVicar, B. A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0405-14.2014 · Cited by 286 · see citing works
Microglia provide neuroprotection after ischemia
Neumann, J. H. L., Gunzer, M., Gutzeit, H. O., Ullrich, O., Reymann, K. G., & Dinkel, K. (2006) · The FASEB Journal · doi:10.1096/fj.05-4882fje · Cited by 284 · see citing works
Ben‐Hur, T., Menachem-Zidon, O. B., Furer, V. L., Einstein, O., Mizrachi‐Kol, R., & Grigoriadis, N. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00218-5 · Cited by 283 · see citing works
Innate Immunity in the CNS: Redefining the Relationship between the CNS and Its Environment
Lampron, A., ElAli, A., & Rivest, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.005 · Cited by 282 · see citing works
Arcuri, C., Mecca, C., Bianchi, R., Giambanco, I., & Donato, R. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00191 · Cited by 279 · see citing works
Hydrogels derived from central nervous system extracellular matrix
Medberry, C. J., Crapo, P. M., Siu, B. F., Carruthers, C. A., Wolf, M. T., Nagarkar, S. P., Agrawal, V., Jones, K. E., Kelly, J., Johnson, S. A., et al. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.10.062 · Cited by 278 · see citing works
RIGOR Guidelines: Escalating STAIR and STEPS for Effective Translational Research
Lapchak, P. A., Zhang, J. H., & Noble‐Haeusslein, L. J. (2012) · Translational Stroke Research · doi:10.1007/s12975-012-0209-2 · Cited by 272 · see citing works
Alia, C., Spalletti, C., Lai, S., Panarese, A., Lamola, G., Bertolucci, F., Vallone, F., Garbo, A. D., Chisari, C., Micera, S., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00076 · Cited by 256 · see citing works
The Ischemic Environment Drives Microglia and Macrophage Function
Fumagalli, S., Perego, C., Pischiutta, F., Zanier, E. R., & Simoni, M. G. D. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00081 · Cited by 245 · see citing works
Martino, G., Pluchino, S., Bonfanti, L., & Schwartz, M. (2011) · Physiological Reviews · doi:10.1152/physrev.00032.2010 · Cited by 240 · see citing works
van Meer, M. P. A., Otte, W. M., van der Marel, K., Nijboer, C. H. A., Kavelaars, A., van der Sprenkel, J. W. B., Viergever, M. A., & Dijkhuizen, R. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3662-11.2012 · Cited by 234 · see citing works
Zhang, J., Malik, A., Choi, H. B., Ko, R. W. Y., Dissing-Olesen, L., & MacVicar, B. A. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.043 · Cited by 234 · see citing works
Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex
Arnò, B., Grassivaro, F., Rossi, C., Bergamaschi, A., Castiglioni, V., Furlan, R., Greter, M., Favaro, R., Comı, G., Becher, B., et al. (2014) · Nature Communications · doi:10.1038/ncomms6611 · Cited by 233 · see citing works
Persistent inflammation alters the function of the endogenous brain stem cell compartment
Pluchino, S., Muzio, L., Imitola, J., Deleidi, M., Alfaro‐Cervelló, C., Salani, G., Porcheri, C., Brambilla, E., Cavasinni, F., Bergamaschi, A., et al. (2008) · Brain · doi:10.1093/brain/awn198 · Cited by 227 · see citing works
Microglia and ischemic stroke: a double-edged sword
Sang, Y., Zou, X., & Zhang, Y. (2019) · Int J Immunol · doi:10.3760/cma.j.issn.1673-4394.2019.01.013 · Cited by 227 · see citing works
A distinct population of microglia supports adult neurogenesis in the subventricular zone
Ribeiro Xavier, A. L., Kress, B. T., Goldman, S. A., Lacerda de Menezes, J. R., & Nedergaard, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1217-15.2015 · Cited by 225 · see citing works
Butts, D. A., Kanold, P. O., & Shatz, C. J. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050061 · Cited by 208 · see citing works
Bidirectional Microglia‐Neuron Communication in the Healthy Brain
Eyo, U. B., & Wu, L. (2013) · Neural Plasticity · doi:10.1155/2013/456857 · Cited by 203 · see citing works
Cacci, E., Claasen, J.-H., & Kokaia, Z. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20531 · Cited by 188 · see citing works
Effects of Microglia on Neurogenesis
Sato, K. (2015) · Glia · doi:10.1002/glia.22858 · Cited by 187 · see citing works
Permissive proteolytic activity for visual cortical plasticity
Mataga, N., Nagai, N., & Hensch, T. K. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.102088899 · Cited by 179 · see citing works
Lindvall, O., & Kokaia, Z. (2011) · Stroke · doi:10.1161/strokeaha.110.599654 · Cited by 176 · see citing works
Integrated technology for evaluation of brain function and neural plasticity
Rossini, P. M., & Forno, G. D. (2004) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/s1047-9651(03)00124-4 · Cited by 159 · see citing works
Grailer, J. J., Haggadone, M. D., Sarma, J. V., Zetoune, F. S., & Ward, P. A. (2014) · Journal of Innate Immunity · doi:10.1159/000358524 · Cited by 157 · see citing works
Massensini, A. R., Ghuman, H., Saldin, L. T., Medberry, C. J., Keane, T. J., Nicholls, F. J., Velankar, S., Badylak, S. F., & Modo, M. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.08.040 · Cited by 152 · see citing works
Neurogenesis in the Caudate Nucleus of the Adult Rabbit
Luzzati, F., Marchis, S. D., Fasolo, A., & Peretto, P. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4371-05.2006 · Cited by 150 · see citing works
Bible, E., Qutachi, O., Chau, D. Y. S., Alexander, M. R., Shakesheff, K. M., & Modo, M. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.06.085 · Cited by 141 · see citing works
Defining the NG2-expressing cell of the adult CNS
Horner, P. J., Thallmair, M., & Gage, F. H. (2002) · Journal of Neurocytology · doi:10.1023/a:1025739630398 · Cited by 131 · see citing works
Local Hemodynamics Dictate Long-Term Dendritic Plasticity in Peri-Infarct Cortex
Mostany, R., Chowdhury, T. G., Johnston, D. G., Portonovo, S. A., Carmichael, S. T., & Portera‐Cailliau, C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3908-10.2010 · Cited by 122 · see citing works
Microglia and macrophages differ in their inflammatory profile after permanent brain ischemia
Zarruk, J. G., Greenhalgh, A. D., & David, S. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2017.08.011 · Cited by 119 · see citing works
Grossmann, R. E., Stence, N., Carr, J., Fuller, L. C., Waite, M., & Dailey, M. E. (2002) · Glia · doi:10.1002/glia.10031 · Cited by 118 · see citing works
Qü, M., Mittmann, T., Luhmann, H. J., Schleicher, A., & Zilles, K. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00656-8 · Cited by 118 · see citing works
D'Haese, J. G., Demir, I. E., Friess, H., & Ceyhan, G. O. (2010) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728220903540265 · Cited by 116 · see citing works
Askim, T., Indredavik, B., Vangberg, T. R., & Haberg, A. K. (2008) · Neurorehabilitation and neural repair · doi:10.1177/1545968308322840 · Cited by 116 · see citing works
Fractalkine in the nervous system: neuroprotective or neurotoxic molecule?
Lauro, C., Catalano, M., Trettel, F., & Limatola, C. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12805 · Cited by 114 · see citing works
Brown, C. E., Boyd, J. D., & Murphy, T. H. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.241 · Cited by 114 · see citing works
Displacement of Sensory Maps and Disorganization of Motor Cortex After Targeted Stroke in Mice
Harrison, T. C., Silasi, G., Boyd, J. D., & Murphy, T. H. (2013) · Stroke · doi:10.1161/strokeaha.113.001272 · Cited by 113 · see citing works
Que, M., Schiene, K., Witte, O. W., et al. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00598-4 · Cited by 109 · see citing works
Differential activation of microglia in neurogenic versus non‐neurogenic regions of the forebrain
Goings, G. E., Kozlowski, D. A., & Szele, F. G. (2006) · Glia · doi:10.1002/glia.20381 · Cited by 107 · see citing works
Electrophysiological transcortical diaschisis after middle cerebral artery occlusion (MCAO) in rats
Reinecke, S., Lutzenburg, M., Hagemann, G., Bruehl, C., Neumann‐Haefelin, T., & Witte, O. W. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00014-2 · Cited by 102 · see citing works
Inflammation in Ischemic Stroke: Mechanisms, Consequences and Possible Drug Targets
Ahmad, M., Dar, N. J., Bhat, Z. S., Hussain, A., Shah, A., Liu, H., & Graham, S. H. (2014) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527313666141023094720 · Cited by 102 · see citing works
Iosif, R. E., Ahlenius, H., Ekdahl, C. T., Darsalia, V., Thored, P., Jovinge, S. V., Kokaia, Z., & Lindvall, O. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.47 · Cited by 99 · see citing works
On cerebral motor control: The recovery from experimentally produced hemiplegia.
Ogden, R., & Franz, S. I. (1917) · Psychobiology · doi:10.1037/h0074814 · Cited by 96 · see citing works
Rehabilitation and plasticity following stroke: Insights from rodent models
Caleo, M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.029 · Cited by 95 · see citing works
Ransom, B. R. (2012) · doi:10.1093/med/9780199794591.001.0001 · Cited by 93 · see citing works
Physical Activity Early after Stroke and Its Association to Functional Outcome 3 Months Later
Askim, T., Bernhardt, J., Salvesen, Ø., & Indredavik, B. (2014) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2013.12.011 · Cited by 91 · see citing works
RGD‐peptide modified alginate by a chemoenzymatic strategy for tissue engineering applications
Sandvig, I., Karstensen, K., Rokstad, A. M., Aachmann, F. L., Formo, K., Sandvig, A., Skjåk‐Bræk, G., & Strand, B. L. (2014) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.35230 · Cited by 87 · see citing works
Self-citationGherardini, L. M., Gennaro, M., & Pizzorusso, T. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht217 · Cited by 86 · see citing works
Neurogenesis and Gliogenesis in Nervous System Plasticity and Repair
Frisén, J. (2016) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-124953 · Cited by 83 · see citing works
Visual discrimination training improves Humphrey perimetry in chronic cortically induced blindness
Cavanaugh, M. R., & Huxlin, K. R. (2017) · Neurology · doi:10.1212/wnl.0000000000003921 · Cited by 82 · see citing works
Lowery, R. L., Tremblay, M., Hopkins, B. E., & Majewska, A. K. (2017) · Glia · doi:10.1002/glia.23192 · Cited by 80 · see citing works
High-level expression of functional chemokine receptor CXCR4 on human neural precursor cells
Ni, H. T., Hu, S., Sheng, W. S., Olson, J. M., Cheeran, M. C. ‐., Chan, A. S. H., Lokensgard, J. R., & Peterson, P. K. (2004) · Developmental Brain Research · doi:10.1016/j.devbrainres.2004.06.015 · Cited by 78 · see citing works
Sinden, J. D., Hicks, C. A., Stroemer, P., Vishnubhatla, I., & Corteling, R. L. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0009 · Cited by 78 · see citing works
Heterogeneous induction of microglia M2a phenotype by central administration of interleukin-4
Pepe, G., Calderazzi, G., Maglie, M. D., Villa, A. M., & Vegeto, E. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0211-6 · Cited by 77 · see citing works
Que, M., Witte, O. W., Neumann‐Haefelin, T., Schiene, K., Schroeter, M., & Zilles, K. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00197-9 · Cited by 72 · see citing works
Home sweet home: the neural stem cell niche throughout development and after injury
Ruddy, R. M., & Morshead, C. M. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2658-0 · Cited by 66 · see citing works
Aging and neurogenesis in the adult forebrain: what we have learned and where we should go from here
Hamilton, L. K., Joppé, S. E., Cochard, L. M., & Fernandes, K. J. L. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12207 · Cited by 64 · see citing works
Extracellular Membrane Vesicles and Immune Regulation in the Brain
Cossetti, C., Smith, J. A., Iraci, N., Leonardi, T., Alfaro‐Cervelló, C., & Pluchino, S. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00117 · Cited by 61 · see citing works
Cuprizone demyelination induces a unique inflammatory response in the subventricular zone
Hillis, J. M., Davies, J., Mundim, M. V., Al‐Dalahmah, O., & Szele, F. G. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0651-2 · Cited by 55 · see citing works
Okabe, N., Shiromoto, T., Himi, N., Feng, L., Nakamura‐Maruyama, E., Narita, K., Iwachidou, N., Yagita, Y., & Miyamoto, O. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.008 · Cited by 55 · see citing works
Xerri, C., Zennou‐Azogui, Y., Sadlaoud, K., & Sauvajon, D. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.066 · Cited by 52 · see citing works
Hospital Differences in Motor Activity Early after Stroke: A Comparison of 11 Norwegian Stroke Units
Hokstad, A., Indredavik, B., Bernhardt, J. A., Ihle‐Hansen, H., Salvesen, Ø. O., Seljeseth, Y. M., Schüler, S., Engstad, T. A., & Askim, T. (2015) · Journal of Stroke and Cerebrovascular Diseases · doi:10.1016/j.jstrokecerebrovasdis.2015.02.009 · Cited by 51 · see citing works
Lesion-Induced Accumulation of Platelets Promotes Survival of Adult Neural Stem / Progenitor Cells
Kazanis, I., Feichtner, M., Lange, S., Rotheneichner, P., Hainzl, S., Oeller, M., Schallmoser, K., Rohde, E., Reitsamer, H. A., Couillard‐Després, S., et al. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.03.018 · Cited by 50 · see citing works
Cavanaugh, M. R., Barbot, A., Carrasco, M., & Huxlin, K. R. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.12.010 · Cited by 50 · see citing works
Ischemic stroke and repair: current trends in research and tissue engineering treatments
Wang, J., Yang, W., Xie, H., Song, Y., Li, Y., & Wang, L. (2014) · Regenerative Medicine Research · doi:10.1186/2050-490x-2-3 · Cited by 40 · see citing works
Molecular/genetic manipulation of extrinsic axon guidance factors for CNS repair and regeneration
Curinga, G., & Smith, G. M. (2007) · Experimental Neurology · doi:10.1016/j.expneurol.2007.06.026 · Cited by 39 · see citing works
Sandvig, I., Gadjanski, I., Vlaski‐Lafarge, M., Bużańska, L., Loncaric, D., Sarnowska, A., Rodríguez, L., Sandvig, A., & Ivanović, Z. (2017) · Stem Cells and Development · doi:10.1089/scd.2016.0268 · Cited by 39 · see citing works
Self-citationExtracellular matrix modulation is driven by experience-dependent plasticity during stroke recovery.
Quattromani, M. J., Pruvost, M., Guerreiro, C., Backlund, F., Englund, E., Aspberg, A., Jaworski, T., Hakon, J., Ruscher, K., Kaczmarek, L., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-017-0461-2 · Cited by 39 · see citing works
Vise, W. M. (1977) · Archives of Neurology · doi:10.1001/archneur.1977.00500230030004 · Cited by 37 · see citing works
Age dependence of excitatory-inhibitory balance following stroke
Schmidt, S., Bruehl, C., Frahm, C., Redecker, C., & Witte, O. W. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.11.019 · Cited by 37 · see citing works
Plasticity and regeneration in the injured spinal cord after cell transplantation therapy
Nori, S., Nakamura, M., & Okano, H. (2017) · Progress in brain research · doi:10.1016/bs.pbr.2016.12.007 · Cited by 37 · see citing works
Nakajima, K., Yamamoto, S., Kohsaka, S., & Kurihara, T. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.03.058 · Cited by 35 · see citing works
Current developments in cell- and biomaterial-based approaches for stroke repair
Jendelová, P., Kubinová, Š., Sandvig, I., Erceg, S., Sandvig, A., & Syková, E. (2015) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2016.1094457 · Cited by 32 · see citing works
Self-citationKazanis, I., Gorenkova, N., Zhao, J., Franklin, R. J. M., Modo, M., & ffrench‐Constant, C. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.06.025 · Cited by 28 · see citing works
Mayor, S. J. (1973) · Physiological Psychology · doi:10.3758/bf03326864 · Cited by 26 · see citing works
Askim, T., Langhammer, B., Ihle‐Hansen, H., Magnussen, J., Engstad, T. A., & Indredavik, B. (2012) · Stroke Research and Treatment · doi:10.1155/2012/392101 · Cited by 26 · see citing works
Stem cell repair of striatal ischemia
Kokaia, Z., & Lindvall, O. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59544-7.00003-2 · Cited by 25 · see citing works
Bioengineering solutions for neural repair and recovery in stroke
Modo, M., Ambrosio, F., Friedlander, R. M., Badylak, S. F., & Wechsler, L. R. (2013) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000031 · Cited by 23 · see citing works
Neurogenesis in the Adult Mammalian Brain: How Much Do We Need, How Much Do We Have?
Kazanis, I. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_227 · Cited by 20 · see citing works
Augestad, I. L., Nyman, A. K. G., Costa, A. I., Barnett, S. C., Sandvig, A., Haberg, A. K., & Sandvig, I. (2017) · Neurochemical Research · doi:10.1007/s11064-016-2098-3 · Cited by 19 · see citing works
Self-citationYu, X., & Koretsky, A. P. (2014) · Brain Connectivity · doi:10.1089/brain.2014.0259 · Cited by 18 · see citing works
Askim, T., Indredavik, B., Engen, A., Roos, K., Aas, T., & Mørkved, S. (2012) · Physiotherapy Theory and Practice · doi:10.3109/09593985.2012.734008 · Cited by 15 · see citing works
Askim, T., Indredavik, B., & Haberg, A. K. (2010) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2010.07.217 · Cited by 12 · see citing works
Strippers Reveal Their Depressing Secrets: Removing AMPA Receptors
Collingridge, G. L., & Peineau, S. (2014) · Neuron · doi:10.1016/j.neuron.2014.03.019 · Cited by 10 · see citing works
Epileptiform discharges and neuronal plasticity in the acute peri-infarct cortex of rats
Fujioka, H., Kaneko, H., Fujii, M., et al. (2009) · Neurological Research · doi:10.1179/174313209x459138 · Cited by 8 · see citing works
Concepts of Central Nervous System Plasticity and Their Implications for Recovery After Brain Damage
Stein, D. G. (2012) · Springer Publishing Company eBooks · doi:10.1891/9781617050572.0013 · Cited by 3 · see citing works
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Crapser, J. D., Ochaba, J., Soni, N., Reidling, J. C., Thompson, L. M., & Green, K. N. (2020) · Brain · doi:10.1093/brain/awz363 · Cited by 157 · see citing works
- Authors
- Sandvig, I., Augestad, I. L., Håberg, A. K., & Sandvig, A.
- Affiliations
- Norwegian University of Science and Technology (NO)
- Faculty of Medicine and Health Sciences Department of Neuromedicine and Movement Science Norwegian University of Science and Technology (NTNU) Trondheim Norway
- Corresponding author
- Sandvig, Ioanna
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2018-06
- Volume
- 47
- Issue
- 12
- Pages
- 1414-1428
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2803968036
- Cited by
- 94
- References
- 159
- Citations by year
- 2026: 2 · 2025: 12 · 2024: 11 · 2023: 13 · 2022: 14 · 2021: 14 · 2020: 10 · 2019: 15 · 2018: 2
- FWCI
- 0.97
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- NORA - Norwegian Open Research Archives (submittedVersion, other-oa)
- Funders
- The Liaison Committee for Education, Research, and Innovation in Central Norway (Helse Midt-Norge RHF)
- Joint Research Committee between St Olav´s Hospital and the Faculty of Medicine and Health Sciences, NTNU (Felles Forskingsutvalg)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- neuroplasticity, stroke recovery, microglia, ischemic brain injury, synaptogenesis, neurogenesis, neural progenitor cells, neurogenic niche, microglial activation, inflammation, synaptic plasticity, tissue remodeling
- MeSH terms
- Animals, Brain Ischemia, Humans, Nerve Net, Neuronal Plasticity, Synapses, Microglia, Stroke, Neurogenesis, Gray Matter
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