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Abstract

The addition of new neurons and oligodendroglia in the postnatal and adult mammalian brain presents distinct forms of gray and white matter plasticity. Substantial effort has been devoted to understanding the cellular and molecular mechanisms controlling postnatal neurogenesis and gliogenesis, revealing important parallels to principles governing the embryonic stages. While during central nervous system development, scripted temporal and spatial patterns of neural and glial progenitor proliferation and differentiation are necessary to create the nervous system architecture, it remains unclear what driving forces maintain and sustain postnatal neural stem cell (NSC) and oligodendrocyte progenitor cell (OPC) production of new neurons and glia. In recent years, neuronal activity has been identified as an important modulator of these processes. Using the distinct properties of neurotransmitter ionotropic and metabotropic channels to signal downstream cellular events, NSCs and OPCs share common features in their readout of neuronal activity patterns. Here we review the current evidence for neuronal activity-dependent control of NSC/OPC proliferation and differentiation in the postnatal brain, highlight some potential mechanisms used by the two progenitor populations, and discuss future studies that might advance these research areas further.

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2018-07-08
2024-04-24
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Literature Cited

  1. Abiraman K, Pol SU, O'Bara MA, Chen G-D, Khaku ZM et al. 2015. Anti-muscarinic adjunct therapy accelerates functional human oligodendrocyte repair. J. Neurosci. 35:3676–88
    [Google Scholar]
  2. Abrous DN, Adriani W, Montaron MF, Aurousseau C, Rougon G et al. 2002. Nicotine self-administration impairs hippocampal plasticity. J. Neurosci. 22:3656–62
    [Google Scholar]
  3. Agresti C, Meomartini ME, Amadio S, Ambrosini E, Serafini B et al. 2005. Metabotropic P2 receptor activation regulates oligodendrocyte progenitor migration and development. Glia 50:132–44
    [Google Scholar]
  4. Alcantara Llaguno S, Chen J, Kwon CH, Jackson EL, Li Y et al. 2009. Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15:45–56
    [Google Scholar]
  5. Arancibia-Cárcamo IL, Ford MC, Cossell L, Ishida K, Tohyama K, Attwell D 2017. Node of Ranvier length as a potential regulator of myelinated axon conduction speed. eLife 6:e23329
    [Google Scholar]
  6. Attwell D, Gibb A 2005. Neuroenergetics and the kinetic design of excitatory synapses. Nat. Rev. Neurosci. 6:841–49
    [Google Scholar]
  7. Balia M, Benamer N, Angulo MC 2017. A specific GABAergic synapse onto oligodendrocyte precursors does not regulate cortical oligodendrogenesis. Glia 65:1821–32
    [Google Scholar]
  8. Balia M, Vélez-Fort M, Passlick S, Schäfer C, Audinat E et al. 2013. Postnatal down-regulation of the GABAA receptor γ2 subunit in neocortical NG2 cells accompanies synaptic-to-extrasynaptic switch in the GABAergic transmission mode. Cereb. Cortex 25:1114–23
    [Google Scholar]
  9. Barres BA, Raff MC 1993. Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258–60
    [Google Scholar]
  10. Benner EJ, Luciano D, Jo R, Abdi K, Paez-Gonzalez P et al. 2013. Protective astrogenesis from the SVZ niche after injury is controlled by Notch modulator Thbs4. Nature 497:369–73
    [Google Scholar]
  11. Berg DA, Belnoue L, Song H, Simon A 2013. Neurotransmitter-mediated control of neurogenesis in the adult vertebrate brain. Development 140:2548–61
    [Google Scholar]
  12. Bergles D, Roberts J, Somogyi P, Jahr C 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187–91
    [Google Scholar]
  13. Bergmann O, Spalding KL, Frisen J 2015. Adult neurogenesis in humans. Cold Spring Harb. Perspect. Biol. 7:a018994
    [Google Scholar]
  14. Bjornsson CS, Apostolopoulou M, Tian Y, Temple S 2015. It takes a village: constructing the neurogenic niche. Dev. Cell 32:435–46
    [Google Scholar]
  15. Blanke ML, VanDongen AMJ 2009. Activation mechanisms of the NMDA receptor. Biology of the NMDA Receptor AM VanDongen 283–312 Boca Raton, FL: CRC Press
    [Google Scholar]
  16. Bolteus AJ, Bordey A 2004. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci. 24:7623–31
    [Google Scholar]
  17. Borden LA 1996. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem. Int. 29:335–56
    [Google Scholar]
  18. Calzà L, Giuliani A, Fernandez M, Pirondi S, D'Intino G et al. 2003. Neural stem cells and cholinergic neurons: regulation by immunolesion and treatment with mitogens, retinoic acid, and nerve growth factor. PNAS 100:7325–30
    [Google Scholar]
  19. Caulfield MP 1993. Muscarinic receptors—characterization, coupling and function. Pharmacol. Ther. 58:319–79
    [Google Scholar]
  20. Christian KM, Song H, Ming GL 2014. Functions and dysfunctions of adult hippocampal neurogenesis. Annu. Rev. Neurosci. 37:243–62
    [Google Scholar]
  21. Cohen RI, Almazan G 1994. Rat oligodendrocytes express muscarinic receptors coupled to phosphoinositide hydrolysis and adenylyl cyclase. Eur. J. Neurosci. 6:1213–24
    [Google Scholar]
  22. Conn PJ, Pin JP 1997. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37:205–37
    [Google Scholar]
  23. Cooper-Kuhn CM, Winkler J, Kuhn HG 2004. Decreased neurogenesis after cholinergic forebrain lesion in the adult rat. J. Neurosci. Res. 77:155–65
    [Google Scholar]
  24. Dani JA 2001. Overview of nicotinic receptors and their roles in the central nervous system. Biol. Psychiatry. 49:166–74
    [Google Scholar]
  25. Dawson MRL, Polito A, Levine JM, Reynolds R 2003. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell Neurosci. 24:476–88
    [Google Scholar]
  26. De Angelis F, Bernardo A, Magnaghi V, Minghetti L, Tata AM 2012. Muscarinic receptor subtypes as potential targets to modulate oligodendrocyte progenitor survival, proliferation, and differentiation. Dev. Neurobiol. 72:713–28
    [Google Scholar]
  27. De Biase LM, Kang SH, Baxi EG, Fukaya M, Pucak ML et al. 2011. NMDA receptor signaling in oligodendrocyte progenitors is not required for oligodendrogenesis and myelination. J. Neurosci. 31:12650–62
    [Google Scholar]
  28. De Marchis S, Temoney S, Erdelyi F, Bovetti S, Bovolin P et al. 2004. GABAergic phenotypic differentiation of a subpopulation of subventricular derived migrating progenitors. Eur. J. Neurosci. 20:1307–17
    [Google Scholar]
  29. Delpire E 2000. Cation-chloride cotransporters in neuronal communication. News Physiol. Sci. 15:309–12
    [Google Scholar]
  30. Deshmukh VA, Tardif V, Lyssiotis CA, Green CC, Kerman B et al. 2013. A regenerative approach to the treatment of multiple sclerosis. Nature 502:327–32
    [Google Scholar]
  31. Dingledine R, Borges K, Bowie D, Traynelis SF 1999. The glutamate receptor ion channels. Pharmacol. Rev. 51:7–61
    [Google Scholar]
  32. Dutar P, Nicoll RA 1988. Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J. Neurosci. 8:4214–24
    [Google Scholar]
  33. Engel J Jr, Bragin A, Staba R, Mody I 2009. High-frequency oscillations: What is normal and what is not?. Epilepsia 50:598–604
    [Google Scholar]
  34. Etxeberria A, Hokanson KC, Dao DQ, Mayoral SR, Mei F et al. 2016. Dynamic modulation of myelination in response to visual stimuli alters optic nerve conduction velocity. J. Neurosci. 36:6937–48
    [Google Scholar]
  35. Faiz M, Sachewsky N, Gascon S, Bang KW, Morshead CM, Nagy A 2015. Adult neural stem cells from the subventricular zone give rise to reactive astrocytes in the cortex after stroke. Cell Stem Cell 17:624–34
    [Google Scholar]
  36. Fannon J, Tarmier W, Fulton D 2015. Neuronal activity and AMPA-type glutamate receptor activation regulates the morphological development of oligodendrocyte precursor cells. Glia 63:1021–35
    [Google Scholar]
  37. Fontana X, Nacher J, Soriano E, del Rio JA 2006. Cell proliferation in the adult hippocampal formation of rodents and its modulation by entorhinal and fimbria-fornix afferents. Cereb. Cortex 16:301–12
    [Google Scholar]
  38. Ford MC, Alexandrova O, Cossell L, Stange-Marten A, Sinclair J et al. 2015. Tuning of Ranvier node and internode properties in myelinated axons to adjust action potential timing. Nat. Commun. 6:8073
    [Google Scholar]
  39. Freund TF, Buzsaki G 1996. Interneurons of the hippocampus. Hippocampus 6:347–470
    [Google Scholar]
  40. Frisen J 2016. Neurogenesis and gliogenesis in nervous system plasticity and repair. Annu. Rev. Cell Dev. Biol. 32:127–41
    [Google Scholar]
  41. Fritschy JM, Panzanelli P 2014. GABAA receptors and plasticity of inhibitory neurotransmission in the central nervous system. Eur. J. Neurosci. 39:1845–65
    [Google Scholar]
  42. Gallo V, Deneen B 2014. Glial development: the crossroads of regeneration and repair in the CNS. Neuron 83:283–308
    [Google Scholar]
  43. Gallo V, Zhou JM, McBain CJ, Wright P, Knutson PL, Armstrong RC 1996. Oligodendrocyte progenitor cell proliferation and lineage progression are regulated by glutamate receptor-mediated K+ channel block. J. Neurosci. 16:2659–70
    [Google Scholar]
  44. Gascon E, Dayer AG, Sauvain MO, Potter G, Jenny B et al. 2006. GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J. Neurosci. 26:12956–66
    [Google Scholar]
  45. Gautier HOB, Evans KA, Volbracht K, James R, Sitnikov S et al. 2015. Neuronal activity regulates remyelination via glutamate signalling to oligodendrocyte progenitors. Nat. Commun. 6:8518
    [Google Scholar]
  46. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589–93
    [Google Scholar]
  47. Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL et al. 2014. Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344:1252304
    [Google Scholar]
  48. Gilbert P, Kettenmann H, Schachner M 1984. γ-Aminobutyric acid directly depolarizes cultured oligodendrocytes. J. Neurosci. 4:561–69
    [Google Scholar]
  49. Giniatullin R, Nistri A, Yakel JL 2005. Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28:371–78
    [Google Scholar]
  50. Goncalves JT, Schafer ST, Gage FH 2016. Adult neurogenesis in the hippocampus: from stem cells to behavior. Cell 167:897–914
    [Google Scholar]
  51. Greger IH, Watson JF, Cull-Candy SG 2017. Structural and functional architecture of AMPA-type glutamate receptors and their auxiliary proteins. Neuron 94:713–30
    [Google Scholar]
  52. Guo F, Maeda Y, Ko EM, Delgado M, Horiuchi M et al. 2012. Disruption of NMDA receptors in oligodendroglial lineage cells does not alter their susceptibility to experimental autoimmune encephalomyelitis or their normal development. J. Neurosci. 32:639–45
    [Google Scholar]
  53. Harrist A, Beech RD, King SL, Zanardi A, Cleary MA et al. 2004. Alteration of hippocampal cell proliferation in mice lacking the β2 subunit of the neuronal nicotinic acetylcholine receptor. Synapse 54:200–6
    [Google Scholar]
  54. Hill RA, Patel KD, Goncalves CM, Grutzendler J, Nishiyama A 2014. Modulation of oligodendrocyte generation during a critical temporal window after NG2 cell division. Nat. Neurosci. 17:1518–27
    [Google Scholar]
  55. Hines JH, Ravanelli AM, Schwindt R, Scott EK, Appel B 2015. Neuronal activity biases axon selection for myelination in vivo. Nat. Neurosci. 18:683–89
    [Google Scholar]
  56. Hoppe D, Kettenmann H 1989. GABA triggers a Cl efflux from cultured mouse oligodendrocytes. Neurosci. Lett. 97:334–39
    [Google Scholar]
  57. Hughes EG, Kang SH, Fukaya M, Bergles DE 2013. Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16:668–76
    [Google Scholar]
  58. Huh KH, Fuhrer C 2002. Clustering of nicotinic acetylcholine receptors: from the neuromuscular junction to interneuronal synapses. Mol. Neurobiol. 25:79–112
    [Google Scholar]
  59. Iacobucci GJ, Popescu GK 2017. NMDA receptors: linking physiological output to biophysical operation. Nat. Rev. Neurosci. 18:236–49
    [Google Scholar]
  60. Ihrie RA, Alvarez-Buylla A 2011. Lake-front property: a unique germinal niche by the lateral ventricles of the adult brain. Neuron 70:674–86
    [Google Scholar]
  61. Imamura O, Arai M, Dateki M, Ogata T, Uchida R et al. 2015. Nicotinic acetylcholine receptors mediate donepezil-induced oligodendrocyte differentiation. J. Neurochem. 135:1086–98
    [Google Scholar]
  62. Itou Y, Nochi R, Kuribayashi H, Saito Y, Hisatsune T 2011. Cholinergic activation of hippocampal neural stem cells in aged dentate gyrus. Hippocampus 21:446–59
    [Google Scholar]
  63. Jabs R, Pivneva T, Huttmann K, Wyczynski A, Nolte C et al. 2005. Synaptic transmission onto hippocampal glial cells with hGFAP promoter activity. J. Cell Sci. 118:3791–803
    [Google Scholar]
  64. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T et al. 2009. GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J. Neurosci. 29:7966–77
    [Google Scholar]
  65. Jenkins SM, Bennett V 2001. Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J. Cell Biol. 155:739–46
    [Google Scholar]
  66. John D, Shelukhina I, Yanagawa Y, Deuchars J, Henderson Z 2015. Functional alpha7 nicotinic receptors are expressed on immature granule cells of the postnatal dentate gyrus. Brain Res 1601:15–30
    [Google Scholar]
  67. Kaneko N, Okano H, Sawamoto K 2006. Role of the cholinergic system in regulating survival of newborn neurons in the adult mouse dentate gyrus and olfactory bulb. Genes Cells 11:1145–59
    [Google Scholar]
  68. Káradóttir R, Cavelier P, Bergersen LH, Attwell D 2005. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438:1162–66
    [Google Scholar]
  69. Káradóttir R, Hamilton NB, Bakiri Y, Attwell D 2008. Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nat. Neurosci. 11:450–56
    [Google Scholar]
  70. Kastritsis CH, McCarthy KD 1993. Oligodendroglial lineage cells express neuroligand receptors. Glia 8:106–13
    [Google Scholar]
  71. Kempermann G, Kuhn HG, Gage FH 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493–95
    [Google Scholar]
  72. Kempermann G, Song H, Gage FH 2015. Neurogenesis in the adult hippocampus. Cold Spring Harb. Perspect. Biol. 7:a018812
    [Google Scholar]
  73. Kirchhoff F, Kettenmann H 1992. GABA triggers a [Ca2+]i increase in murine precursor cells of the oligodendrocyte lineage. Eur. J. Neurosci. 4:1049–58
    [Google Scholar]
  74. Kotani S, Yamauchi T, Teramoto T, Ogura H 2006. Pharmacological evidence of cholinergic involvement in adult hippocampal neurogenesis in rats. Neuroscience 142:505–14
    [Google Scholar]
  75. Kougioumtzidou E, Shimizu T, Hamilton NB, Tohyama K, Sprengel R et al. 2017. Signalling through AMPA receptors on oligodendrocyte precursors promotes myelination by enhancing oligodendrocyte survival. eLife 6:e28080
    [Google Scholar]
  76. Kriegstein A, Alvarez-Buylla A 2009. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32:149–84
    [Google Scholar]
  77. Kropff E, Yang SM, Schinder AF 2015. Dynamic role of adult-born dentate granule cells in memory processing. Curr. Opin. Neurobiol. 35:21–26
    [Google Scholar]
  78. Kruse AC, Kobilka BK, Gautam D, Sexton PM, Christopoulos A, Wess J 2014. Muscarinic acetylcholine receptors: novel opportunities for drug development. Nat. Rev. Drug Discov. 13:549–60
    [Google Scholar]
  79. Kukley M, Capetillo-Zarate E, Dietrich D 2007. Vesicular glutamate release from axons in white matter. Nat. Neurosci. 10:311–20
    [Google Scholar]
  80. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D et al. 2006. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127:1253–64
    [Google Scholar]
  81. Li C, Xiao L, Liu X, Yang W, Shen W et al. 2013. A functional role of NMDA receptor in regulating the differentiation of oligodendrocyte precursor cells and remyelination. Glia 61:732–49
    [Google Scholar]
  82. Li Q, Brus-Ramer M, Martin JH, McDonald JW 2010. Electrical stimulation of the medullary pyramid promotes proliferation and differentiation of oligodendrocyte progenitor cells in the corticospinal tract of the adult rat. Neurosci. Lett. 479:128–33
    [Google Scholar]
  83. Lin CW, Sim S, Ainsworth A, Okada M, Kelsch W, Lois C 2010. Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 65:32–39
    [Google Scholar]
  84. Lin S-C, Bergles DE 2004. Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat. Neurosci. 7:24–32
    [Google Scholar]
  85. Lin S-C, Huck JH, Roberts JD, Macklin WB, Somogyi P, Bergles DE 2005. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46:773–85
    [Google Scholar]
  86. Liu X, Wang Q, Haydar TF, Bordey A 2005. Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci. 8:1179–87
    [Google Scholar]
  87. Lledo PM, Merkle FT, Alvarez-Buylla A 2008. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31:392–400
    [Google Scholar]
  88. Lopez Juarez A, He D, Lu QR 2016. Oligodendrocyte progenitor programming and reprogramming: toward myelin regeneration. Brain Res 1638:209–20
    [Google Scholar]
  89. Loreti S, Vilaro MT, Visentin S, Rees H, Levey AI, Tata AM 2006. Rat Schwann cells express M1-M4 muscarinic receptor subtypes. J. Neurosci. Res. 84:97–105
    [Google Scholar]
  90. Lundgaard I, Luzhynskaya A, Stockley JH, Wang Z, Evans KA et al. 2013. Neuregulin and BDNF induce a switch to NMDA receptor-dependent myelination by oligodendrocytes. PLOS Biol 11:e1001743
    [Google Scholar]
  91. Luyt K, Slade TP, Dorward JJ, Durant CF, Wu Y et al. 2007. Developing oligodendrocytes express functional GABAB receptors that stimulate cell proliferation and migration. J. Neurochem. 100:822–40
    [Google Scholar]
  92. Ma W, Li BS, Zhang L, Pant HC 2004. Signaling cascades implicated in muscarinic regulation of proliferation of neural stem and progenitor cells. Drug News Perspect 17:258–66
    [Google Scholar]
  93. Ma W, Maric D, Li BS, Hu Q, Andreadis JD et al. 2000. Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur. J. Neurosci. 12:1227–40
    [Google Scholar]
  94. Maccaferri G, Lacaille JC 2003. Interneuron Diversity series: Hippocampal interneuron classifications – making things as simple as possible, not simpler. Trends Neurosci 26:564–71
    [Google Scholar]
  95. Mak GK, Enwere EK, Gregg C, Pakarainen T, Poutanen M et al. 2007. Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat. Neurosci. 10:1003–11
    [Google Scholar]
  96. Mak GK, Weiss S 2010. Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat. Neurosci. 13:753–58
    [Google Scholar]
  97. Mangin J-M, Kunze A, Chittajallu R, Gallo V 2008. Satellite NG2 progenitor cells share common glutamatergic inputs with associated interneurons in the mouse dentate gyrus. J. Neurosci. 28:7610–23
    [Google Scholar]
  98. Mangin J-M, Li P, Scafidi J, Gallo V 2012. Experience-dependent regulation of NG2 progenitors in the developing barrel cortex. Nat. Neurosci. 15:1192–94
    [Google Scholar]
  99. Manns ID, Alonso A, Jones BE 2000. Discharge properties of juxtacellularly labeled and immunohistochemically identified cholinergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J. Neurosci. 20:1505–18
    [Google Scholar]
  100. Markwardt SJ, Dieni CV, Wadiche JI, Overstreet-Wadiche L 2011. Ivy/neurogliaform interneurons coordinate activity in the neurogenic niche. Nat. Neurosci. 14:1407–9
    [Google Scholar]
  101. Mathew TC 1999. Association between supraependymal nerve fibres and the ependymal cilia of the mammalian brain. Anat. Histol. Embryol. 28:193–97
    [Google Scholar]
  102. Matute C 2008. P2X7 receptors in oligodendrocytes: a novel target for neuroprotection. Mol. Neurobiol. 38:123–28
    [Google Scholar]
  103. McKenzie IA, Ohayon D, Li H, Paes de Faria J, Emery B et al. 2014. Motor skill learning requires active central myelination. Science 346:318–22
    [Google Scholar]
  104. Mei F, Fancy SPJ, Shen Y-AA, Niu J, Zhao C et al. 2014. Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis. Nat. Med. 20:954–60
    [Google Scholar]
  105. Mei F, Lehmann-Horn K, Shen Y-AA, Rankin KA, Stebbins KJ et al. 2016. Accelerated remyelination during inflammatory demyelination prevents axonal loss and improves functional recovery. eLife 5:e18246
    [Google Scholar]
  106. Mensch S, Baraban M, Almeida R, Czopka T, Ausborn J et al. 2015. Synaptic vesicle release regulates myelin sheath number of individual oligodendrocytes in vivo. Nat. Neurosci. 18:628–30
    [Google Scholar]
  107. Miller FD, Gauthier-Fisher A 2009. Home at last: neural stem cell niches defined. Cell Stem Cell 4:507–10
    [Google Scholar]
  108. Mitew S, Hay CM, Peckham H, Xiao J, Koenning M, Emery B 2014. Mechanisms regulating the development of oligodendrocytes and central nervous system myelin. Neuroscience 276:29–47
    [Google Scholar]
  109. Mohapel P, Leanza G, Kokaia M, Lindvall O 2005. Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol. Aging 26:939–46
    [Google Scholar]
  110. Mount CW, Monje M 2017. Wrapped to adapt: experience-dependent myelination. Neuron 95:743–56
    [Google Scholar]
  111. Mrzljak L, Levey AI, Goldman-Rakic PS 1993. Association of m1 and m2 muscarinic receptor proteins with asymmetric synapses in the primate cerebral cortex: morphological evidence for cholinergic modulation of excitatory neurotransmission. PNAS 90:5194–98
    [Google Scholar]
  112. Mudo G, Belluardo N, Mauro A, Fuxe K 2007. Acute intermittent nicotine treatment induces fibroblast growth factor-2 in the subventricular zone of the adult rat brain and enhances neuronal precursor cell proliferation. Neuroscience 145:470–83
    [Google Scholar]
  113. Muller J, Reyes-Haro D, Pivneva T, Nolte C, Schaette R et al. 2009. The principal neurons of the medial nucleus of the trapezoid body and NG2+ glial cells receive coordinated excitatory synaptic input. J. Gen. Physiol. 134:115–27
    [Google Scholar]
  114. Narla S, Klejbor I, Birkaya B, Lee YW, Morys J et al. 2013. α7 Nicotinic receptor agonist reactivates neurogenesis in adult brain. Biochem. Pharmacol. 86:1099–104
    [Google Scholar]
  115. Nguyen L, Malgrange B, Breuskin I, Bettendorff L, Moonen G et al. 2003. Autocrine/paracrine activation of the GABAA receptor inhibits the proliferation of neurogenic polysialylated neural cell adhesion molecule-positive (PSA-NCAM+) precursor cells from postnatal striatum. J. Neurosci. 23:3278–94
    [Google Scholar]
  116. Niswender CM, Conn PJ 2010. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 50:295–322
    [Google Scholar]
  117. Noji T, Karasawa A, Kusaka H 2004. Adenosine uptake inhibitors. Eur. J. Pharmacol. 495:1–16
    [Google Scholar]
  118. Okuda H, Tatsumi K, Makinodan M, Yamauchi T, Kishimoto T, Wanaka A 2009. Environmental enrichment stimulates progenitor cell proliferation in the amygdala. J. Neurosci. Res. 87:3546–53
    [Google Scholar]
  119. Paez-Gonzalez P, Abdi K, Luciano D, Liu Y, Soriano-Navarro M et al. 2011. Ank3-dependent SVZ niche assembly is required for the continued production of new neurons. Neuron 71:61–75
    [Google Scholar]
  120. Paez-Gonzalez P, Asrican B, Rodriguez E, Kuo CT 2014. Identification of distinct ChAT+ neurons and activity-dependent control of postnatal SVZ neurogenesis. Nat. Neurosci. 17:934–42
    [Google Scholar]
  121. Pajevic S, Basser PJ, Fields RD 2014. Role of myelin plasticity in oscillations and synchrony of neuronal activity. Neuroscience 276:135–47
    [Google Scholar]
  122. Parikh V, Sarter M 2008. Cholinergic mediation of attention: contributions of phasic and tonic increases in prefrontal cholinergic activity. Ann. N. Y. Acad. Sci. 1129:225–35
    [Google Scholar]
  123. Patneau DK, Mayer ML 1990. Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-d-aspartate and quisqualate receptors. J. Neurosci. 10:2385–99
    [Google Scholar]
  124. Paul A, Chaker Z, Doetsch F 2017. Hypothalamic regulation of regionally distinct adult neural stem cells and neurogenesis. Science 356:1383–86
    [Google Scholar]
  125. Pin JP, Bettler B 2016. Organization and functions of mGlu and GABAB receptor complexes. Nature 540:60–68
    [Google Scholar]
  126. Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A 2010. NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 65:859–72
    [Google Scholar]
  127. Plested AJ 2016. Structural mechanisms of activation and desensitization in neurotransmitter-gated ion channels. Nat. Struct. Mol. Biol. 23:494–502
    [Google Scholar]
  128. Pringle NP, Mudhar HS, Collarini EJ, Richardson WD 1992. PDGF receptors in the rat CNS: During late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage. Development 115:535–51
    [Google Scholar]
  129. Quick MW, Lester RA 2002. Desensitization of neuronal nicotinic receptors. J. Neurobiol. 53:457–78
    [Google Scholar]
  130. Ragheb F, Molina-Holgado E, Cui QL, Khorchid A, Liu HN et al. 2001. Pharmacological and functional characterization of muscarinic receptor subtypes in developing oligodendrocytes. J. Neurochem. 77:1396–406
    [Google Scholar]
  131. Rogers SW, Gregori NZ, Carlson N, Gahring LC, Noble M 2001. Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells. Glia 33:306–13
    [Google Scholar]
  132. Rosenberg MB, Friedmann T, Robertson RC, Tuszynski M, Wolff JA et al. 1988. Grafting genetically modified cells to the damaged brain: restorative effects of NGF expression. Science 242:1575–78
    [Google Scholar]
  133. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA et al. 2011. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–70
    [Google Scholar]
  134. Sakamoto M, Kageyama R, Imayoshi I 2014. The functional significance of newly born neurons integrated into olfactory bulb circuits. Front. Neurosci. 8:121
    [Google Scholar]
  135. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai HH et al. 2011. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–86
    [Google Scholar]
  136. Schmidt HD, Pierce RC 2010. Cocaine-induced neuroadaptations in glutamate transmission. Ann. N. Y. Acad. Sci. 1187:35–75
    [Google Scholar]
  137. Sharma G 2013. The dominant functional nicotinic receptor in progenitor cells in the rostral migratory stream is the α3β4 subtype. J. Neurophysiol. 109:867–72
    [Google Scholar]
  138. Simon C, Gotz M, Dimou L 2011. Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59:869–81
    [Google Scholar]
  139. Song J, Sun J, Moss J, Wen Z, Sun GJ et al. 2013. Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus. Nat. Neurosci. 16:1728–30
    [Google Scholar]
  140. Song J, Zhong C, Bonaguidi MA, Sun GJ, Hsu D et al. 2012. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489:150–54
    [Google Scholar]
  141. Spitzer S, Volbracht K, Lundgaard I, Káradóttir RT 2016. Glutamate signalling: a multifaceted modulator of oligodendrocyte lineage cells in health and disease. Neuropharmacology 110:574–85
    [Google Scholar]
  142. Stevens B, Porta S, Haak LL, Gallo V, Fields RD 2002. Adenosine: a neuron-glial transmitter promoting myelination in the CNS in response to action potentials. Neuron 36:855–68
    [Google Scholar]
  143. Takarada T, Nakamichi N, Kitajima S, Fukumori R, Nakazato R et al. 2012. Promoted neuronal differentiation after activation of alpha4/beta2 nicotinic acetylcholine receptors in undifferentiated neural progenitors. PLOS ONE 7:e46177
    [Google Scholar]
  144. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH 2006. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442:929–33
    [Google Scholar]
  145. Tattersfield AS, Croon RJ, Liu YW, Kells AP, Faull RL, Connor B 2004. Neurogenesis in the striatum of the quinolinic acid lesion model of Huntington's disease. Neuroscience 127:319–32
    [Google Scholar]
  146. Tomasetti C, Vogelstein B 2015. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science 347:78–81
    [Google Scholar]
  147. Tomassy GS, Berger DR, Chen H-H, Kasthuri N, Hayworth KJ et al. 2014. Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:319–24
    [Google Scholar]
  148. Tong CK, Chen J, Cebrian-Silla A, Mirzadeh Z, Obernier K et al. 2014. Axonal control of the adult neural stem cell niche. Cell Stem Cell 14:500–11
    [Google Scholar]
  149. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T 2005. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47:803–15
    [Google Scholar]
  150. Unal CT, Golowasch JP, Zaborszky L 2012. Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Front. Behav. Neurosci. 6:21
    [Google Scholar]
  151. Van der Borght K, Mulder J, Keijser JN, Eggen BJ, Luiten PG, Van der Zee EA 2005. Input from the medial septum regulates adult hippocampal neurogenesis. Brain Res. Bull. 67:117–25
    [Google Scholar]
  152. Van Kampen JM, Eckman CB 2010. Agonist-induced restoration of hippocampal neurogenesis and cognitive improvement in a model of cholinergic denervation. Neuropharm 58:921–29
    [Google Scholar]
  153. Veena J, Srikumar BN, Mahati K, Raju TR, Shankaranarayana Rao BS 2011. Oxotremorine treatment restores hippocampal neurogenesis and ameliorates depression-like behaviour in chronically stressed rats. Psychopharm 217:239–53
    [Google Scholar]
  154. Vélez-Fort M, Audinat E, Angulo MC 2009. Functional α7‐containing nicotinic receptors of NG2‐expressing cells in the hippocampus. Glia 57:1104–14
    [Google Scholar]
  155. Vélez-Fort M, Maldonado PP, Butt AM, Audinat E, Angulo MC 2010. Postnatal switch from synaptic to extrasynaptic transmission between interneurons and NG2 cells. J. Neurosci. 30:6921–29
    [Google Scholar]
  156. Venkatesh HS, Johung TB, Caretti V, Noll A, Tang Y et al. 2015. Neuronal activity promotes glioma growth through neuroligin-3 secretion. Cell 161:803–16
    [Google Scholar]
  157. Vizi ES, Lendvai B 1999. Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system. Brain Res. Rev. 30:219–35
    [Google Scholar]
  158. Wake H, Lee PR, Fields RD 2011. Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647–51
    [Google Scholar]
  159. Wang DD, Krueger DD, Bordey A 2003. GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J. Physiol. 550:785–800
    [Google Scholar]
  160. Wang H, Yan Y, Kintner DB, Lytle C, Sun D 2003. GABA-mediated trophic effect on oligodendrocytes requires Na-K-2Cl cotransport activity. J. Neurophysiol. 90:1257–65
    [Google Scholar]
  161. Wigley R, Hamilton N, Nishiyama A, Kirchhoff F, Butt AM 2007. Morphological and physiological interactions of NG2-glia with astrocytes and neurons. J. Anat. 210:661–70
    [Google Scholar]
  162. Xiao L, Ohayon D, McKenzie IA, Sinclair-Wilson A, Wright JL et al. 2016. Rapid production of new oligodendrocytes is required in the earliest stages of motor-skill learning. Nat. Neurosci. 19:1210–17
    [Google Scholar]
  163. Yakel JL 2014. Nicotinic ACh receptors in the hippocampal circuit; functional expression and role in synaptic plasticity. J. Physiol. 592:4147–53
    [Google Scholar]
  164. Yeung MS, Zdunek S, Bergmann O, Bernard S, Salehpour M et al. 2014. Dynamics of oligodendrocyte generation and myelination in the human brain. Cell 159:766–74
    [Google Scholar]
  165. Young KM, Psachoulia K, Tripathi RB, Dunn S-J, Cossell L et al. 2013. Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77:873–85
    [Google Scholar]
  166. Young SZ, Lafourcade CA, Platel JC, Lin TV, Bordey A 2014. GABAergic striatal neurons project dendrites and axons into the postnatal subventricular zone leading to calcium activity. Front. Cell Neurosci. 8:10
    [Google Scholar]
  167. Young SZ, Taylor MM, Bordey A 2011. Neurotransmitters couple brain activity to subventricular zone neurogenesis. Eur. J. Neurosci. 33:1123–32
    [Google Scholar]
  168. Yu DX, Marchetto MC, Gage FH 2014. How to make a hippocampal dentate gyrus granule neuron. Development 141:2366–75
    [Google Scholar]
  169. Yu YC, Bultje RS, Wang X, Shi SH 2009. Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458:501–4
    [Google Scholar]
  170. Yuan X, Eisen AM, McBain CJ, Gallo V 1998. A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125:2901–14
    [Google Scholar]
  171. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR et al. 2014. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34:11929–47
    [Google Scholar]
  172. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE 2007. Vesicular release of glutamate from unmyelinated axons in white matter. Nat. Neurosci. 10:321–30
    [Google Scholar]
  173. Zonouzi M, Scafidi J, Li P, McEllin B, Edwards J et al. 2015. GABAergic regulation of cerebellar NG2 cell development is altered in perinatal white matter injury. Nat. Neurosci. 18:674–82
    [Google Scholar]
  174. Zuchero JB, Barres BA 2013. Intrinsic and extrinsic control of oligodendrocyte development. Curr. Opin. Neurobiol. 23:914–20
    [Google Scholar]
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