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Cell and Tissue Research

, Volume 371, Issue 1, pp 33–46 | Cite as

Neural mechanisms underlying GABAergic regulation of adult hippocampal neurogenesis

  • Christina Catavero
  • Hechen Bao
  • Juan SongEmail author
Review

Abstract

Within the dentate gyrus of the adult hippocampus is the subgranular zone, which contains a neurogenic niche for radial-glia like cells, the most primitive neural stem cells in the adult brain. The quiescence of neural stem cells is maintained by tonic gamma-aminobutyric acid (GABA) released from local interneurons. Once these cells differentiate into neural progenitor cells, GABA continues to regulate their development into mature granule cells, the principal cell type of the dentate gyrus. Here, we review the role of GABA circuits, signaling, and receptors in regulating development of adult-born cells, as well as the molecular players that modulate GABA signaling. Furthermore, we review recent findings linking dysregulation of adult hippocampal neurogenesis to the altered GABAergic circuitry and signaling under various pathological conditions.

Keywords

Adult hippocampal neurogenesis GABA signaling GABA circuits GABA receptors Adult neural stem cells 

Notes

Acknowledgements

We thank Brent Asrican for helpful comments on the review. This work was supported by grants from the American Heart Association, Whitehall Foundation and NIH (R01MH111773, R21MH106939) to J.S. and NIH (T32NS007431) to C.C.

References

  1. Adlaf EW, Vaden RJ, Niver AJ, Manuel AF, Onyilo VC, Araujo MT, Dieni CV, Vo HT, King GD, Wadiche JI, Overstreet-Wadiche L (2017) Adult-born neurons modify excitatory synaptic transmission to existing neurons. elife 6:e19886PubMedPubMedCentralCrossRefGoogle Scholar
  2. Airan RD, Meltzer LA, Roy M, Gong Y, Chen H, Deisseroth K (2007) High-speed imaging reveals Neurophysiological links to behavior in an animal model of depression. Science 317:819–823PubMedCrossRefGoogle Scholar
  3. Alvarez DD, Giacomini D, Yang SM, Trinchero MF, Temprana SG, Buttner KA, Beltramone N, Schinder AF (2016) A disynaptic feedback network activated by experience promotes the integration of new granule cells. Science 354:459–465PubMedCrossRefGoogle Scholar
  4. Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22PubMedPubMedCentralCrossRefGoogle Scholar
  5. Becker S, Wojtowicz JM (2007) A model of hippocampal neurogenesis in memory and mood disorders. Trends Cogn Sci 11:70–76PubMedCrossRefGoogle Scholar
  6. Bhattacharyya BJ, Banisadr G, Jung H, Ren D, Cronshaw DG, Zou Y, Miller RJ (2008) The Chemokine Stromal cell-derived factor-1 regulates GABAergic inputs to neural progenitors in the postnatal dentate Gyrus. J Neurosci 28:6720–6730PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming G, Song H (2011) In vivo Clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145:1142–1155PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bruel-Jungerman E, Rampon C, Laroche S (2007) Adult hippocampal neurogenesis, synaptic plasticity and memory: facts and hypotheses. Rev Neurosci 18:93–114PubMedCrossRefGoogle Scholar
  9. Brunner J, Neubrandt M, Van-Weert S, Andrási T, Kleine Borgmann FB, Jessberger S, Szabadics J, Suh H, van Praag H, Buchholz B, Possnert G, Mash D, Druid H, Frisen J (2014) Adult-born granule cells mature through two functionally distinct states. elife 3:e03104PubMedPubMedCentralCrossRefGoogle Scholar
  10. Cardoso A, Freitas-da-Costa P, Carvalho LS, Lukoyanov NV (2010) Seizure-induced changes in neuropeptide Y-containing cortical neurons: potential role for seizure threshold and epileptogenesis. Epilepsy Behav 19:559–567PubMedCrossRefGoogle Scholar
  11. Chancey JH, Adlaf EW, Sapp MC, Pugh PC, Wadiche JI, Overstreet-Wadiche LS (2013) GABA depolarization is required for experience-dependent synapse Unsilencing in adult-born neurons. J Neurosci 33:6614–6622PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chen Z, Li X, Zhou J, Yuan B, Yu B, Tong D, Cheng C, Shao Y, Xia S, Zhang R, Lyu J, Yu X, Dong C, Zhou W-H, Qiu Z (2017) Accumulated quiescent neural stem cells in adult hippocampus of the mouse model for the MECP2 duplication syndrome. Sci Rep 7:41701PubMedPubMedCentralCrossRefGoogle Scholar
  13. Crowther AJ, Song J (2014) Activity-dependent signaling mechanisms regulating adult hippocampal neural stem cells and their progeny. Neurosci Bull 30:542–556PubMedPubMedCentralCrossRefGoogle Scholar
  14. Czéh B, Varga ZKK, Henningsen K, Kovács GL, Miseta A, Wiborg O (2015) Chronic stress reduces the number of GABAergic interneurons in the adult rat hippocampus, dorsal-ventral and region-specific differences. Hippocampus 25:393–405PubMedCrossRefGoogle Scholar
  15. David DJ, Samuels BA, Rainer Q, Wang J-W, Marsteller D, Mendez I, Drew M, Craig DA, Guiard BP, Guilloux J-P, Artymyshyn RP, Gardier AM, Gerald C, Antonijevic IA, Leonardo ED, Hen R (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62:479–493PubMedPubMedCentralCrossRefGoogle Scholar
  16. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563–572PubMedCrossRefGoogle Scholar
  17. Deng W, Aimone JB, Gage FH (2010) New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11:339–350PubMedPubMedCentralCrossRefGoogle Scholar
  18. Deprez F, Vogt F, Floriou-Servou A, Lafourcade C, Rudolph U, Tyagarajan SK, Fritschy J-M (2016) Partial inactivation of GABA A receptors containing the α5 subunit affects the development of adult-born dentate gyrus granule cells. Eur J Neurosci 44:2258–2271PubMedPubMedCentralCrossRefGoogle Scholar
  19. Deshpande A, Bergami M, Ghanem A, Conzelmann K-K, Lepier A, Götz M, Berninger B (2013) Retrograde monosynaptic tracing reveals the temporal evolution of inputs onto new neurons in the adult dentate gyrus and olfactory bulb. Proc Natl Acad Sci U S A 110:E1152–E1161Google Scholar
  20. Diaz SL, Narboux-Nême N, Trowbridge S, Scotto-Lomassese S, Kleine Borgmann FB, Jessberger S, Giros B, Maroteaux L, Deneris E, Gaspar P (2013) Paradoxical increase in survival of newborn neurons in the dentate gyrus of mice with constitutive depletion of serotonin. Eur J Neurosci 38:2650–2658PubMedCrossRefGoogle Scholar
  21. Dieni CV, Panichi R, Aimone JB, Kuo CT, Wadiche JI, Overstreet-Wadiche L (2016) Low excitatory innervation balances high intrinsic excitability of immature dentate neurons. Nat Commun 7:11313PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dumitru I, Neitz A, Alfonso J, Monyer H (2017) Diazepam binding inhibitor promotes stem cell expansion controlling environment-dependent Neurogenesis. Neuron 94:125–137.e5PubMedCrossRefGoogle Scholar
  23. Duveau V, Laustela S, Barth L, Gianolini F, Vogt KE, Keist R, Chandra D, Homanics GE, Rudolph U, Fritschy J-M (2011) Spatiotemporal specificity of GABAA receptor-mediated regulation of adult hippocampal neurogenesis. Eur J Neurosci 34:362–373PubMedPubMedCentralCrossRefGoogle Scholar
  24. Earnheart JC, Schweizer C, Crestani F, Iwasato T, Itohara S, Mohler H, Lüscher B (2007) GABAergic control of adult hippocampal neurogenesis in relation to behavior indicative of trait anxiety and depression states. J Neurosci 27:3845–3854PubMedPubMedCentralCrossRefGoogle Scholar
  25. Egeland M, Warner-Schmidt J, Greengard P, Svenningsson P (2010) Neurogenic effects of fluoxetine are attenuated in p11 (S100A10) knockout mice. Biol Psychiatry 67:1048–1056PubMedCrossRefGoogle Scholar
  26. Enna SJ, McCarson KE (2006) The role of GABA in the mediation and perception of pain. Adv Pharmacol 54:1–27PubMedCrossRefGoogle Scholar
  27. Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn A-M, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317PubMedCrossRefGoogle Scholar
  28. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074–10086PubMedCrossRefGoogle Scholar
  29. Evans J, Sun Y, McGregor A, Connor B (2012) Allopregnanolone regulates neurogenesis and depressive/anxiety-like behaviour in a social isolation rodent model of chronic stress. Neuropharmacology 63:1315–1326PubMedCrossRefGoogle Scholar
  30. Felice D, O’Leary OF, Pizzo RC, Cryan JF (2012) Blockade of the GABAB receptor increases neurogenesis in the ventral but not dorsal adult hippocampus: relevance to antidepressant action. Neuropharmacology 63:1380–1388PubMedCrossRefGoogle Scholar
  31. Fiorentino H, Kuczewski N, Diabira D, Ferrand N, Pangalos MN, Porcher C, Gaiarsa J-L (2009) GABAB receptor activation triggers BDNF release and promotes the maturation of GABAergic synapses. J Neurosci 29:11650–11661PubMedCrossRefGoogle Scholar
  32. Freund TF (2003) Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489–495PubMedCrossRefGoogle Scholar
  33. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170–173PubMedCrossRefGoogle Scholar
  34. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347–470PubMedCrossRefGoogle Scholar
  35. Ge S, Goh ELK, Sailor KA, Kitabatake Y, Ming G, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589–593PubMedCrossRefGoogle Scholar
  36. Ge S, Pradhan DA, Ming G-L, Song H (2007) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30:1–8PubMedCrossRefGoogle Scholar
  37. Ghose S, Winter MK, McCarson KE, Tamminga CA, Enna SJ (2011) The GABAβ receptor as a target for antidepressant drug action. Br J Pharmacol 162:1–17PubMedPubMedCentralCrossRefGoogle Scholar
  38. Giachino C, Barz M, Tchorz JS, Tome M, Gassmann M, Bischofberger J, Bettler B, Taylor V (2013) GABA suppresses neurogenesis in the adult hippocampus through GABAB receptors. Development 141:83–90PubMedCrossRefGoogle Scholar
  39. Griguoli M, Cherubini E (2012) Regulation of hippocampal inhibitory circuits by nicotinic acetylcholine receptors. J Physiol 590:655–666PubMedCrossRefGoogle Scholar
  40. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15:1700–1706PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gunn BG, Cunningham L, Mitchell SG, Swinny JD, Lambert JJ, Belelli D (2015) GABAA receptor-acting neurosteroids: a role in the development and regulation of the stress response. Front Neuroendocrinol 36:28–48PubMedPubMedCentralCrossRefGoogle Scholar
  42. Guo N, Yoshizaki K, Kimura R, Suto F, Yanagawa Y, Osumi N (2013) A sensitive period for GABAergic Interneurons in the dentate Gyrus in modulating Sensorimotor gating. J Neurosci 33:6691–6704PubMedCrossRefGoogle Scholar
  43. Halasy K, Miettinen R, Szabat E, Freund TF (1992) GABAergic Interneurons are the major postsynaptic targets of median Raphe afferents in the rat dentate Gyrus. Eur J Neurosci 4:144–153PubMedCrossRefGoogle Scholar
  44. Han ZS, Buhl EH, Lorinczi Z, Somogyi P (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of the rat hippocampus. Eur J Neurosci 5:395–410PubMedCrossRefGoogle Scholar
  45. Harrison P (2004) The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology 174:151–162PubMedCrossRefGoogle Scholar
  46. Heese K, Otten U, Mathivet P, Raiteri M, Marescaux C, Bernasconi R (2000) GABA(B) receptor antagonists elevate both mRNA and protein levels of the neurotrophins nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) but not neurotrophin-3 (NT-3) in brain and spinal cord of rats. Neuropharmacology 39:449–462PubMedCrossRefGoogle Scholar
  47. Heigele S, Sultan S, Toni N, Bischofberger J (2016) Bidirectional GABAergic control of action potential firing in newborn hippocampal granule cells. Nat Neurosci 19:263–270PubMedCrossRefGoogle Scholar
  48. Hester MS, Danzer SC (2013) Accumulation of abnormal adult-generated Hippocampal granule cells predicts seizure frequency and severity. J Neurosci 33:8926–8936PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hosford BE, Liska JP, Danzer SC (2016) Ablation of newly generated Hippocampal granule cells has disease-modifying effects in epilepsy. J Neurosci 36:11013–11023PubMedPubMedCentralCrossRefGoogle Scholar
  50. Houser CR (2007) Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity. Prog Brain Res 163:217–232PubMedCrossRefGoogle Scholar
  51. Howell OW, Scharfman HE, Herzog H, Sundstrom LE, Beck-Sickinger A, Gray WP (2003) Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J Neurochem 86:646–659PubMedCrossRefGoogle Scholar
  52. Howell OW, Silva S, Scharfman HE, Sosunov AA, Zaben M, Shatya A, Mckhann G, Herzog H, Laskowski A, Gray WP, Gray WP (2007) Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus. Neurobiol Dis 26:174–188PubMedCrossRefGoogle Scholar
  53. Ikrar T, Guo N, He K, Besnard A, Levinson S, Hill A, Lee H-K, Hen R, Xu X, Sahay A (2013) Adult neurogenesis modifies excitability of the dentate gyrus. Front Neural Circuits 7:204PubMedPubMedCentralCrossRefGoogle Scholar
  54. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisén J (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25–34PubMedCrossRefGoogle Scholar
  55. Johnston ST, Shtrahman M, Parylak S, Gonçalves JT, Gage FH (2016) Paradox of pattern separation and adult neurogenesis: a dual role for new neurons balancing memory resolution and robustness. Neurobiol Learn Mem 129:60–68PubMedCrossRefGoogle Scholar
  56. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, Sato K (2001) The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 104:933–946PubMedCrossRefGoogle Scholar
  57. Kang E, Wen Z, Song H, Christian KM, Ming G (2016) Adult Neurogenesis and psychiatric disorders. Cold Spring Harb Perspect Biol 8:a019026PubMedCrossRefGoogle Scholar
  58. Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355–362PubMedCrossRefGoogle Scholar
  59. Kempermann G (2015) Activity dependency and aging in the regulation of adult Neurogenesis. Cold Spring Harb Perspect Biol 7:a018929PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kempermann G, Krebs J, Fabel K (2008) The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr Opin Psychiatry 21:290–295PubMedCrossRefGoogle Scholar
  61. Kim JY, Duan X, Liu CY, Jang M-H, Guo JU, Pow-anpongkul N, Kang E, Song H, Ming G (2009) DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 63:761–773PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kim JY, Liu CY, Zhang F, Duan X, Wen Z, Song J, Feighery E, Lu B, Rujescu D, St Clair D, Christian K, Callicott JH, Weinberger DR, Song H, Ming G (2012) Interplay between DISC1 and GABA signaling regulates Neurogenesis in mice and risk for schizophrenia. Cell 148:1051–1064PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kolodziej A, Schulz S, Guyon A, Wu D-F, Pfeiffer M, Odemis V, Hollt V, Stumm R (2008) Tonic activation of CXC Chemokine receptor 4 in immature granule cells supports Neurogenesis in the adult dentate Gyrus. J Neurosci 28:4488–4500PubMedCrossRefGoogle Scholar
  64. Krzisch M, Fülling C, Jabinet L, Armida J, Gebara E, Cassé F, Habbas S, Volterra A, Hornung J-P, Toni N (2016) Synaptic adhesion molecules regulate the integration of new granule neurons in the postnatal mouse hippocampus and their impact on spatial memory. Cereb Cortex. doi: 10.1093/cercor/bhw217
  65. Kuhn HG, Cooper-Kuhn CM, Boekhoorn K, Lucassen PJ (2007) Changes in neurogenesis in dementia and Alzheimer mouse models: are they functionally relevant? Eur Arch Psychiatry Clin Neurosci 257:281–289PubMedCrossRefGoogle Scholar
  66. Kumamoto N, Gu Y, Wang J, Janoschka S, Takemaru K-I, Levine J, Ge S (2012) A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat Neurosci 15:399–405PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lacefield CO, Itskov V, Reardon T, Hen R, Gordon JA (2010) Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 22:106–116PubMedPubMedCentralCrossRefGoogle Scholar
  68. Lagace DC, Whitman MC, Noonan MA, Ables JL, DeCarolis NA, Arguello AA, Donovan MH, Fischer SJ, Farnbauch LA, Beech RD, DiLeone RJ, Greer CA, Mandyam CD, Eisch AJ (2007) Dynamic contribution of nestin-expressing stem cells to adult Neurogenesis. J Neurosci 27:12623–12629PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lazarov O, Marr RA (2010) Neurogenesis and Alzheimer’s disease: at the crossroads. Exp Neurol 223:267–281PubMedCrossRefGoogle Scholar
  70. Le Strat Y, Ramoz N, Gorwood P (2009) The role of genes involved in neuroplasticity and neurogenesis in the observation of a gene-environment interaction (GxE) in schizophrenia. Curr Mol Med 9:506–518PubMedCrossRefGoogle Scholar
  71. Lee K-H, Lee H, Yang CH, Ko J-S, Park C-H, Woo R-S, Kim JY, Sun W, Kim J-H, Ho W-K, Lee S-H (2015) Bidirectional signaling of Neuregulin-2 mediates formation of GABAergic synapses and maturation of Glutamatergic synapses in newborn granule cells of postnatal hippocampus. J Neurosci 35:16479–16493PubMedCrossRefGoogle Scholar
  72. Lee AS, De Jesús-Cortés H, Kabir ZD, Knobbe W, Orr M, Burgdorf C, Huntington P, McDaniel L, Britt JK, Hoffmann F, Brat DJ, Rajadhyaksha AM, Pieper AA (2016) The neuropsychiatric disease-associated gene cacna1c mediates survival of young Hippocampal neurons. eNeuro 3:0006CrossRefGoogle Scholar
  73. Li G, Bien-Ly N, Andrews-Zwilling Y, Xu Q, Bernardo A, Ring K, Halabisky B, Deng C, Mahley RW, Huang Y (2009) GABAergic interneuron dysfunction impairs Hippocampal Neurogenesis in adult Apolipoprotein E4 Knockin mice. Cell Stem Cell 5:634–645PubMedPubMedCentralCrossRefGoogle Scholar
  74. Li Y, Aimone JB, Xu X, Callaway EM, Gage FH (2012) Development of GABAergic inputs controls the contribution of maturing neurons to the adult hippocampal network. Proc Natl Acad Sc U S Ai 109:4290–4295Google Scholar
  75. Lin Y-S, Wang H-Y, Huang D-F, Hsieh P-F, Lin M-Y, Chou C-H, Wu I-J, Huang G-J, Gau SS-F, Huang H-S (2016) Neuronal splicing regulator RBFOX3 (NeuN) regulates adult Hippocampal Neurogenesis and Synaptogenesis. PLoS ONE 11:e0164164PubMedPubMedCentralCrossRefGoogle Scholar
  76. Loreth D, Ozmen L, Revel FG, Knoflach F, Wetzel P, Frotscher M, Metzger F, Kretz O (2012) Selective degeneration of septal and hippocampal GABAergic neurons in a mouse model of amyloidosis and tauopathy. Neurobiol Dis 47:1–12PubMedCrossRefGoogle Scholar
  77. Luscher B, Fuchs T (2015) GABAergic control of depression-related brain states. Adv Pharmacol 73:97–144PubMedPubMedCentralCrossRefGoogle Scholar
  78. Mabunga DFN, Gonzales ELT, Kim J-W, Kim KC, Shin CY (2015) Exploring the validity of Valproic acid animal model of autism. Exp Neurobiol 24:285–300PubMedPubMedCentralCrossRefGoogle Scholar
  79. Maccaferri G, Lacaille J-C (2003) Interneuron diversity series: Hippocampal interneuron classifications – making things as simple as possible, not simpler. Trends Neurosci 26:564–571PubMedCrossRefGoogle Scholar
  80. Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:1562–1571PubMedCrossRefGoogle Scholar
  81. Marín O (2012) Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 13:107–120PubMedGoogle Scholar
  82. Marín-Burgin A, Schinder AF (2012) Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res 227:391–399PubMedCrossRefGoogle Scholar
  83. Markwardt SJ, Wadiche JI, Overstreet-Wadiche LS (2009) Input-specific GABAergic signaling to newborn neurons in adult dentate gyrus. J Neurosci 29:15063–15072PubMedPubMedCentralCrossRefGoogle Scholar
  84. Markwardt SJ, Dieni CV, Wadiche JI, Overstreet-Wadiche LS (2011) Ivy/neurogliaform interneurons coordinate activity in the neurogenic niche. Nat Neurosci 14:1407–1409PubMedPubMedCentralCrossRefGoogle Scholar
  85. Marlatt MW, Lucassen PJ (2010) Neurogenesis and Alzheimer’s disease: biology and pathophysiology in mice and men. Curr Alzheimer Res 7:113–125PubMedCrossRefGoogle Scholar
  86. Matsuyama S, Nei K, Tanaka C (1997) Regulation of GABA release via NMDA and 5-HT1A receptors in guinea pig dentate gyrus. Brain Res 761:105–112PubMedCrossRefGoogle Scholar
  87. McAvoy KM, Scobie KN, Berger S, Russo C, Guo N, Decharatanachart P, Vega-Ramirez H, Miake-Lye S, Whalen M, Nelson M, Bergami M, Bartsch D, Hen R, Berninger B, Sahay A (2016) Modulating neuronal competition dynamics in the dentate Gyrus to rejuvenate aging memory circuits. Neuron 91:1356–1373PubMedPubMedCentralCrossRefGoogle Scholar
  88. Ming G, Song H (2011) Adult Neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702PubMedPubMedCentralCrossRefGoogle Scholar
  89. Muñoz MD, Antolín-Vallespín M, Tapia-González S, Sánchez-Capelo A (2016) Smad3 deficiency inhibits dentate gyrus LTP by enhancing GABA A neurotransmission. J Neurochem 137:190–199PubMedCrossRefGoogle Scholar
  90. Myers CE, Scharfman HE (2009) A role for hilar cells in pattern separation in the dentate gyrus: a computational approach. Hippocampus 19:321–337PubMedPubMedCentralCrossRefGoogle Scholar
  91. Neunuebel JP, Knierim JJ (2012) Spatial firing correlates of physiologically distinct cell types of the rat dentate Gyrus. J Neurosci 32:3848–3858PubMedPubMedCentralCrossRefGoogle Scholar
  92. O’Leary OF, Felice D, Galimberti S, Savignac HM, Bravo JA, Crowley T, El Yacoubi M, Vaugeois J-M, Gassmann M, Bettler B, Dinan TG, Cryan JF (2014) GABA B(1) receptor subunit isoforms differentially regulate stress resilience. Proc Natl Acad Sci U S A 111:15232–15237PubMedPubMedCentralCrossRefGoogle Scholar
  93. Ohira K, Takeuchi R, Iwanaga T, Miyakawa T (2013) Chronic fluoxetine treatment reduces parvalbumin expression and perineuronal nets in gamma-aminobutyric acidergic interneurons of the frontal cortex in adult mice. Mol Brain 6:43PubMedPubMedCentralCrossRefGoogle Scholar
  94. Overstreet Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94:4528–4532PubMedCrossRefGoogle Scholar
  95. Overstreet LS, Hentges ST, Bumaschny VF, de Souza FS, Smart JL, Santangelo AM, Low MJ, Westbrook GL, Rubinstein M (2004) A transgenic marker for newly born granule cells in dentate gyrus. J Neurosci 24:3251–3259PubMedCrossRefGoogle Scholar
  96. Pabst M, Braganza O, Dannenberg H, Hu W, Pothmann L, Rosen J, Mody I, van Loo K, Deisseroth K, Becker AJ, Schoch S, Beck H (2016) Astrocyte intermediaries of Septal cholinergic modulation in the hippocampus. Neuron 90:853–865PubMedCrossRefGoogle Scholar
  97. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727–3738PubMedGoogle Scholar
  98. Parihar VK, Hattiangady B, Kuruba R, Shuai B, Shetty AK (2011) Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory. Mol Psychiatry 16:171–183PubMedCrossRefGoogle Scholar
  99. Park EH, Burghardt NS, Dvorak D, Hen R, Fenton AA (2015) Experience-dependent regulation of dentate Gyrus excitability by adult-born granule cells. J Neurosci 35:11656–11666PubMedPubMedCentralCrossRefGoogle Scholar
  100. Piatti VC, Ewell LA, Leutgeb JK (2013) Neurogenesis in the dentate gyrus: carrying the message or dictating the tone. Front Neurosci 7:50PubMedPubMedCentralCrossRefGoogle Scholar
  101. Quadrato G, Benevento M, Alber S, Jacob C, Floriddia EM, Nguyen T, Elnaggar MY, Pedroarena CM, Molkentin JD, Di Giovanni S (2012) Nuclear factor of activated T cells (NFATc4) is required for BDNF-dependent survival of adult-born neurons and spatial memory formation in the hippocampus. Proc Natl Acad Sci U S A 109:E1499–E1508PubMedPubMedCentralCrossRefGoogle Scholar
  102. Quadrato G, Elnaggar MY, Duman C, Sabino A, Forsberg K, Di Giovanni S (2014) Modulation of GABAA receptor signaling increases Neurogenesis and suppresses anxiety through NFATc4. J Neurosci 34:8630–8645PubMedCrossRefGoogle Scholar
  103. Ramirez-Amaya V (2005) Spatial exploration-induced arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 25:1761–1768PubMedCrossRefGoogle Scholar
  104. Sahay A, Hen R (2008) Hippocampal neurogenesis and depression. Novartis Found Symp 289:152–160 discussion 160–4, 193–5PubMedCrossRefGoogle Scholar
  105. Santarelli L (2003) Requirement of Hippocampal Neurogenesis for the behavioral effects of antidepressants. Science 301:805–809Google Scholar
  106. Scharfman HE, Brooks-Kayal AR (2014) Is plasticity of GABAergic mechanisms relevant to Epileptogenesis? Adv Exp Med Biol 813:133–150PubMedPubMedCentralCrossRefGoogle Scholar
  107. Shen Q, Fuchs T, Sahir N, Luscher B, Habre W (2012) GABAergic control of critical developmental periods for anxiety- and depression-related behavior in mice. PLoS ONE 7:e47441PubMedPubMedCentralCrossRefGoogle Scholar
  108. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:843–852PubMedCrossRefGoogle Scholar
  109. Song J, Zhong C, Bonaguidi MA, Sun GJ, Hsu D, Gu Y, Meletis K, Huang ZJ, Ge S, Enikolopov G, Deisseroth K, Luscher B, Christian KM, Ming G, Song H (2012a) Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489:150–154PubMedPubMedCentralCrossRefGoogle Scholar
  110. Song J, Christian KM, Ming G, Song H (2012b) Modification of hippocampal circuitry by adult neurogenesis. Dev Neurobiol 72:1032–1043PubMedPubMedCentralCrossRefGoogle Scholar
  111. Song J, Sun J, Moss J, Wen Z, Sun GJ, Hsu D, Zhong C, Davoudi H, Christian KM, Toni N, Ming G, Song H (2013) Parvalbumin interneurons mediate neuronal circuitry–neurogenesis coupling in the adult hippocampus. Nat Neurosci 16:1728–1730PubMedPubMedCentralCrossRefGoogle Scholar
  112. Song J, Olsen RHJ, Sun J, Ming G, Song H (2016) Neuronal circuitry mechanisms regulating adult mammalian Neurogenesis. Cold Spring Harb Perspect Biol 8:a018937PubMedPubMedCentralCrossRefGoogle Scholar
  113. Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisén J (2013) Dynamics of Hippocampal Neurogenesis in adult humans. Cell 153:1219–1227PubMedPubMedCentralCrossRefGoogle Scholar
  114. Stocca G, Schmidt-Hieber C, Bischofberger J (2008) Differential dendritic ca 2+ signalling in young and mature hippocampal granule cells. J Physiol 586:3795–3811PubMedPubMedCentralCrossRefGoogle Scholar
  115. Sun B, Halabisky B, Zhou Y, Palop JJ, Yu G, Mucke L, Gan L (2009) Imbalance between GABAergic and Glutamatergic transmission impairs adult Neurogenesis in an animal model of Alzheimer’s disease. Cell Stem Cell 5:624–633PubMedPubMedCentralCrossRefGoogle Scholar
  116. 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 442:929–933PubMedCrossRefGoogle Scholar
  117. Teles-Grilo Ruivo LM, Mellor JR (2013) Cholinergic modulation of hippocampal network function. Front Synaptic Neurosci. doi: 10.3389/fnsyn.2013.00002
  118. Temprana SG, Mongiat LA, Yang SM, Trinchero MF, Alvarez DD, Kropff E, Giacomini D, Beltramone N, Lanuza GM, Schinder AF (2015) Delayed coupling to feedback inhibition during a critical period for the integration of adult-born granule cells. Neuron 85:116–130PubMedCrossRefGoogle Scholar
  119. Thind KK, Yamawaki R, Phanwar I, Zhang G, Wen X, Buckmaster PS (2010) Initial loss but later excess of GABAergic synapses with dentate granule cells in a rat model of temporal lobe epilepsy. J Comp Neurol 518:647–667PubMedPubMedCentralCrossRefGoogle Scholar
  120. Toni N, Schinder AF (2015) Maturation and functional integration of new granule cells into the adult hippocampus. Cold Spring Harb Perspect Biol 8:a018903Google Scholar
  121. Toni N, Sultan S (2011) Synapse formation on adult-born hippocampal neurons. Eur J Neurosci 33:1062–1068PubMedCrossRefGoogle Scholar
  122. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10:727–734PubMedCrossRefGoogle Scholar
  123. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901–907PubMedPubMedCentralCrossRefGoogle Scholar
  124. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005) GABAergic excitation promotes neuronal differentiation in adult Hippocampal progenitor cells. Neuron 47:803–815PubMedCrossRefGoogle Scholar
  125. Vivar C, Potter MC, Choi J, Lee J, Stringer TP, Callaway EM, Gage FH, Suh H, van Praag H (2012) Monosynaptic inputs to new neurons in the dentate gyrus. Nat Commun 3:1107PubMedPubMedCentralCrossRefGoogle Scholar
  126. Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzaki H, Ogawa T, Mori N, Fukuda A, Sato K (2002) Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Dev Brain Res 139:59–66CrossRefGoogle Scholar
  127. Wang LP, Kempermann G, Kettenmann H (2005) A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29:181–189PubMedCrossRefGoogle Scholar
  128. Wang JM, Liu L, Irwin RW, Chen S, Brinton RD (2008) Regenerative potential of allopregnanolone. Brain Res Rev 57:398–409PubMedCrossRefGoogle Scholar
  129. Wang JM, Singh C, Liu L, Irwin RW, Chen S, Chung EJ, Thompson RF, Brinton RD (2010) Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer’s disease. Proc Natl Acad Sci U S A 107:6498–6503PubMedPubMedCentralCrossRefGoogle Scholar
  130. Wang B, Wang Z, Sun L, Yang L, Li H, Cole AL, Rodriguez-Rivera J, Lu H-C, Zheng H (2014) The Amyloid precursor protein controls adult Hippocampal Neurogenesis through GABAergic Interneurons. J Neurosci 34:13314–13325PubMedPubMedCentralCrossRefGoogle Scholar
  131. Watanabe Y, Murakami T, Kawashima M, Hasegawa-Baba Y, Mizukami S, Imatanaka N, Akahori Y, Yoshida T, Shibutani M (2017) Maternal exposure to valproic acid primarily targets interneurons followed by late effects on neurogenesis in the hippocampal dentate gyrus in rat offspring. Neurotox Res 31(1):46–62Google Scholar
  132. Waterhouse EG, An JJ, Orefice LL, Baydyuk M, Liao G-Y, Zheng K, Lu B, Xu B (2012) BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. J Neurosci 32:14318–14330PubMedPubMedCentralCrossRefGoogle Scholar
  133. Whissell PD, Rosenzweig S, Lecker I, Wang D-S, Wojtowicz JM, Orser BA (2013) γ-aminobutyric acid type a receptors that contain the δ subunit promote memory and neurogenesis in the dentate gyrus. Ann Neurol 74:611–621PubMedCrossRefGoogle Scholar
  134. Winner B, Winkler J (2015) Adult Neurogenesis in Neurodegenerative Diseases: Figure 1. Cold Spring Harb Perspect Biol 7:a021287PubMedPubMedCentralCrossRefGoogle Scholar
  135. Xu J-C, Xiao M-F, Jakovcevski I, Sivukhina E, Hargus G, Cui Y-F, Irintchev A, Schachner M, Bernreuther C (2014) The extracellular matrix glycoprotein tenascin-R regulates neurogenesis during development and in the adult dentate gyrus of mice. J Cell Sci 127:641–652PubMedCrossRefGoogle Scholar
  136. Young SZ, Taylor MM, Wu S, Ikeda-Matsuo Y, Kubera C, Bordey A (2012) NKCC1 knockdown decreases neuron production through GABA(a)-regulated neural progenitor proliferation and delays dendrite development. J Neurosci 32:13630–13638PubMedPubMedCentralCrossRefGoogle Scholar
  137. Yutsudo N, Kamada T, Kajitani K, Nomaru H, Katogi A, Ohnishi YH, Ohnishi YN, Takase K, Sakumi K, Shigeto H, Nakabeppu Y (2013) fosB-null mice display impaired adult hippocampal neurogenesis and spontaneous epilepsy with depressive behavior. Neuropsychopharmacology 38:895–906PubMedPubMedCentralCrossRefGoogle Scholar
  138. Zaben M, Sheward WJ, Shtaya A, Abbosh C, Harmar AJ, Pringle AK, Gray WP (2009) The neurotransmitter VIP expands the pool of symmetrically dividing postnatal dentate gyrus precursors via VPAC2 receptors or directs them toward a neuronal fate via VPAC1 receptors. Stem Cells 27:2539–2551PubMedCrossRefGoogle Scholar
  139. Zhao C, Teng EM, Summers RG, Ming G-L, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3–11PubMedCrossRefGoogle Scholar
  140. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult Neurogenesis. Cell 132:645–660PubMedCrossRefGoogle Scholar
  141. Zhou M, Li W, Huang S, Song J, Kim Y, Tian X, Kang E, Sano Y, Liu C, Balaji J, Wu S, Zhou Y, Parivash SN, Ehninger D, He L, Song H, Ming GL, Silva AJ (2013) mTOR inhibition ameliorates cognitive and affective deficits caused by Disc1 knockdown in adult-born dentate granule neurons. Neuron 77(4):647–654PubMedPubMedCentralCrossRefGoogle Scholar
  142. Zhuo J-M, Tseng H, Desai M, Bucklin ME, Mohammed AI, Robinson NT, Boyden ES, Rangel LM, Jasanoff AP, Gritton HJ, Han X (2016) Young adult born neurons enhance hippocampal dependent performance via influences on bilateral networks. elife 5:e22429PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of PharmacologyUniversity of North CarolinaChapel HillUSA
  2. 2.Neurobiology CurriculumUniversity of North CarolinaChapel HillUSA
  3. 3.Bio-X InstitutesShanghai Jiao Tong UniversityShanghaiChina
  4. 4.Neuroscience CenterUniversity of North CarolinaChapel HillUSA

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