GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons

Journal of Neuroscience

Volumn 33, Issue 15, 2013, Pages 6614-6622

  Chancey, Jessica H ^a   Adlaf, Elena W ^a   Sapp, Matthew C ^a,b   Pugh, Phyllis C ^a,c   Wadiche, Jacques I ^a   Overstreet Wadiche, Linda S ^a  

^a Civitan International Research Center Evelyn F McKnight Brain Institute University of Alabama at Birmingham   (United States)

^b Rice University   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; DEPOLARIZATION; ENVIRONMENTAL EXPOSURE; EXPERIENCE; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; STEREOLOGY; SYNAPSE; SYNAPSE UNSILENCING; SYNAPTIC TRANSMISSION;

ANIMALS; CRITICAL PERIOD (PSYCHOLOGY); ENVIRONMENT; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGENESIS; NEURONS; PRO-OPIOMELANOCORTIN; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84875996639     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0781-13.2013     Document Type: Article

References (51)

1. Akerman CJ, Cline HT (2006) Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J Neurosci 26:5117-5130.
2. Alme CB, Buzzetti RA, Marrone DF, Leutgeb JK, Chawla MK, Schaner MJ, Bohanick JD, Khoboko T, Leutgeb S, Moser EI, Moser MB, McNaughton BL, Barnes CA (2010) Hippocampal granule cells opt for early retirement. Hippocampus 20:1109-1123.
3. Ambrogini P, Cuppini R, Lattanzi D, Ciuffoli S, Frontini A, Fanelli M (2010) Synaptogenesis in adult-generated hippocampal granule cells is affected by behavioral experiences. Hippocampus 20:799-810.
4. Anderson ML, Sisti HM, Curlik, DM 2nd, Shors TJ (2011) Associative learning increases adult neurogenesis during a critical period. Eur J Neurosci 33:175-181.
5. Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa JL (1997) GABAA, NMDA and AMPA receptors: a developmentally regulated "menage a trois." Trends Neurosci 20:523-529
6. Biebl M, Cooper CM, Winkler J, Kuhn HG (2000) Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett 291:17-20.
7. Bijak M, Misgeld U (1996) Suppression by GABAB receptors of 4-aminopyridine-induced hyperactivity in guinea-pig dentate neurons. Neurosci Lett 205:49-52.
8. Cancedda L, Fiumelli H, Chen K, Poo MM (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27:5224-5235.
9. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD, Low MJ (2001) Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484.
10. 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 460:563-572.
11. Dieni CV, Chancey JH, Overstreet-Wadiche LS (2012) Dynamic functions of GABA signaling during granule cell maturation. Front Neural Circuits 6:113.
12. Durand GM, Kovalchuk Y, Konnerth A (1996) Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381: 71-75.
13. Duveau V, Laustela S, Barth L, Gianolini F, Vogt KE, Keist R, Chandra D, Homanics GE, Rudolph U, Fritschy JM (2011) Spatiotemporal specificity of GABAA receptor-mediated regulation of adult hippocampal neurogenesis. Eur J Neurosci 34:362-373.
14. 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 25:10074-10086.
15. 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 439:589-593.
16. Ge S, Pradhan DA, Ming GL, Song H (2007a) GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci 30:1-8.
17. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007b) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566.
18. Gonzalez-Sulser A, Wang J, Motamedi GK, Avoli M, Vicini S, Dzakpasu R (2011) The 4-aminopyridine in vitro epilepsy model analyzed with a perforated multi-electrode array. Neuropharmacology 60:1142-1153.
19. Huang FL, Huang KP, Wu J, Boucheron C (2006) Environmental enrichment enhances neurogranin expression and hippocampal learning and memory but fails to rescue the impairments of neurogranin null mutant mice. J Neurosci 26:6230-6237.
20. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
21. Isaac JT, Crair MC, Nicoll RA, Malenka RC (1997) Silent synapses during development of thalamocortical inputs. Neuron 18:269-280.
22. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, Gage FH, Song H, Lie DC (2009) GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci 29:7966-7977.
23. 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 10:355-362.
24. Kitamura T, Saitoh Y, Murayama A, Sugiyama H, Inokuchi K (2010) LTP induction within a narrow critical period of immature stages enhances the survival of newly generated neurons in the adult rat dentate gyrus. Mol Brain 3:13.
25. 2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18:243-255.
26. Leveille F, Papadia S, Fricker M, Bell KF, Soriano FX, Martel MA, Puddifoot C, Habel M, Wyllie DJ, Ikonomidou C, Tolkovsky AM, Hardingham GE (2010) Suppression of the intrinsic apoptosis pathway by synaptic activity. J Neurosci 30:2623-2635.
27. Liao D, Malinow R (1996) Deficiency in induction but not expression of LTP in hippocampal slices from young rats. Learn Mem 3:138-149.
28. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
29. Luikart BW, Bensen AL, Washburn EK, Perederiy JV, Su KG, Li Y, Kernie SG, Parada LF, Westbrook GL (2011) miR-132 mediates the integration of newborn neurons into the adult dentate gyrus. PLoS One 6:e19077.
30. Markwardt SJ, Wadiche JI, Overstreet-Wadiche LS (2009) Input-specific GABAergic signaling to newborn neurons in adult dentate gyrus. J Neurosci 29:15063-15072.
31. Markwardt SJ, Dieni CV, Wadiche JI, Overstreet-Wadiche L (2011) Ivy/ neurogliaform interneurons coordinate activity in the neurogenic niche. Nat Neurosci 14:1407-1409.
32. Merz K, Herold S, Lie DC (2011) CREB in adult neurogenesis: master and partner in the development of adult-born neurons? Eur J Neurosci 33: 1078-1086.
33. Michelson HB, Wong RK (1994) Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J Physiol 477:35-45.
34. Mongiat LA, Esposito MS, Lombardi G, Schinder AF (2009) Reliable activation of immature neurons in the adult hippocampus. PLoS One 4:e5320.
35. Müller W, Misgeld U (1991) Picrotoxin- and 4-aminopyridine-induced activity in hilar neurons in the guinea pig hippocampal slice. J Neurophysiol 65:141-147.
36. Nitz D, McNaughton B (2004) Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J Neurophysiol 91:863-872.
37. Overstreet LS, Hentges ST, Bumaschny VF, deSouza 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 24:3251-3259.
38. Overstreet Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94:4528-4532.
39. Overstreet-Wadiche LS, Bensen AL, Westbrook GL (2006) Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 26: 2326-2334.
40. Piatti VC, Davies-Sala MG, Esposito MS, Mongiat LA, Trinchero MF, Schinder AF (2011) The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 31:7715-7728.
41. Pugh P, Adlaf E, Zhao CS, Markwardt S, Gavin C, Wadiche J, Overstreet-Wadiche L (2011) Enhanced integration of newborn neurons after neonatal insults. Front Neurosci 5:45.
42. Represa A, Ben-Ari Y (2005) Trophic actions of GABA on neuronal development. Trends Neurosci 28:278-283.
43. Sierra A, Encinas JM, Deudero JJ, Chancey JH, Enikolopov G, Overstreet-Wadiche LS, Tsirka SE, Maletic-Savatic M (2010) Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7:483-495.
44. 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 GL, Song H (2012) Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature 489:150-154.
45. 2+ signalling in young and mature hippocampal granule cells. J Physiol 586:3795-3811.
46. 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 442:929-933.
47. Tashiro A, Makino H, Gage FH (2007) Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 27:3252-3259.
48. Thoeringer CK, Erhardt A, Sillaber I, Mueller MB, Ohl F, Holsboer F, Keck ME (2010) Long-term anxiolytic and antidepressant-like behavioural effects of tiagabine, a selective GABA transporter-1 (GAT-1) inhibitor, coincide with a decrease in HPA system activity in C57BL/6 mice. J Psy-chopharmacol 24:733-743.
49. Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
50. Wang DD, Kriegstein AR (2008) GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci 28:5547-5558.
51. Wu G, Malinow R, Cline HT (1996) Maturation of a central glutamatergic synapse. Science 274:972-976.