|
|
|
Novel functions of GABA signaling in adult neurogenesis |
Adalto PONTES1,2, Yonggang ZHANG1, Wenhui HU1( ) |
| 1. Department of Neuroscience, Temple University School of Medicine, Philadelphia, PA 19140, USA; 2. Universidade do Estado do Pará, Santarém, PA, Brasil |
|
|
|
|
Abstract Neurotransmitter gamma-aminobutiric acid (GABA) through ionotropic GABAA and metabotropic GABAB receptors plays key roles in modulating the development, plasticity and function of neuronal networks. GABA is inhibitory in mature neurons but excitatory in immature neurons, neuroblasts and neural stem/progenitor cells (NSCs/NPCs). The switch from excitatory to inhibitory occurs following the development of glutamatergic synaptic input and results from the dynamic changes in the expression of Na+/K+/2Cl- co-transporter NKCC1 driving Cl- influx and neuron-specific K+/ Cl- co-transporter KCC2 driving Cl- efflux. The developmental transition of KCC2 expression is regulated by Disrupted-in-Schizophrenia 1 (DISC1) and brain-derived neurotrophic factor (BDNF) signaling. The excitatory GABA signaling during early neurogenesis is important to the activity/experience-induced regulation of NSC quiescence, NPC proliferation, neuroblast migration and new-born neuronal maturation/functional integration. The inhibitory GABA signaling allows for the sparse and static functional networking essential for learning/memory development and maintenance.
|
| Keywords
neurogenesis
neural stem cells
GABA
signal pathways
co-transporter
neurons
|
|
Corresponding Author(s):
HU Wenhui,Email:whu@temple.edu
|
|
Issue Date: 01 October 2013
|
|
| 1 |
Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J, Fukuda A, Luhmann H J, Kilb W (2007). Kinetic properties of Cl uptake mediated by Na+-dependent K+-2Cl cotransport in immature rat neocortical neurons. J Neurosci , 27(32): 8616-8627 doi: 10.1523/JNEUROSCI.5041-06.2007 pmid:17687039
|
| 2 |
Aguado F, Carmona M A, Pozas E, Aguiló A, Martínez-Guijarro F J, Alcantara S, Borrell V, Yuste R, Iba?ez C F, Soriano E (2003). BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2. Development , 130(7): 1267-1280 doi: 10.1242/dev.00351 pmid: PMID:12588844
|
| 3 |
Altman J (1969). Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol , 137(4): 433-457 doi: 10.1002/cne.901370404 pmid:5361244
|
| 4 |
Altman J, Das G D (1966). Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J Comp Neurol , 126(3): 337-389 doi: 10.1002/cne.901260302 pmid:5937257
|
| 5 |
And?ng M, Hjerling-Leffler J, Moliner A, Lundgren T K, Castelo-Branco G, Nanou E, Pozas E, Bryja V, Halliez S, Nishimaru H, Wilbertz J, Arenas E, Koltzenburg M, Charnay P, El Manira A, Iba?ez C F, Ernfors P (2008). Histone H2AX-dependent GABA(A) receptor regulation of stem cell proliferation. Nature , 451(7177): 460-464 doi: 10.1038/nature06488 pmid:18185516
|
| 6 |
Becker L, Peterson J, Kulkarni S, Pasricha P J (2013). Ex vivo neurogenesis within enteric ganglia occurs in a PTEN dependent manner. PLoS ONE , 8(3): e59452 doi: 10.1371/journal.pone.0059452 pmid:23527198
|
| 7 |
Benarroch E E (2013). Cation-chloride cotransporters in the nervous system: general features and clinical correlations. Neurology , 80(8): 756-763 doi: 10.1212/WNL.0b013e318283bb1c pmid:23420893
|
| 8 |
Binder S, Baier P C, M?lle M, Inostroza M, Born J, Marshall L (2012). Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats. Neurobiol Learn Mem , 97(2): 213-219 doi: 10.1016/j.nlm.2011.12.004 pmid:22207008
|
| 9 |
Bowery N G, Hill D R, Hudson A L, Doble A, Middlemiss D N, Shaw J, Turnbull M (1980). (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature , 283(5742): 92-94 doi: 10.1038/283092a0 pmid:6243177
|
| 10 |
Chamma I, Chevy Q, Poncer J C, Lévi S (2012). Role of the neuronal K-Cl co-transporter KCC2 in inhibitory and excitatory neurotransmission. Front Cell Neurosci , 6: 5 doi: 10.3389/fncel.2012.00005 pmid:22363264
|
| 11 |
Chater T E, Goda Y (2013). CA3 mossy fiber connections: giant synapses that gain control. Neuron , 77(1): 4-6 doi: 10.1016/j.neuron.2012.12.024 pmid:23312510
|
| 12 |
Cherubini E, Griguoli M, Safiulina V, Lagostena L (2011). The depolarizing action of GABA controls early network activity in the developing hippocampus. Mol Neurobiol , 43(2): 97-106 doi: 10.1007/s12035-010-8147-z pmid:21042953
|
| 13 |
Clelland C D, Choi M, Romberg C, Clemenson G D Jr, Fragniere A, Tyers P, Jessberger S, Saksida L M, Barker R A, Gage F H, Bussey T J (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science , 325(5937): 210-213 doi: 10.1126/science.1173215 pmid:19590004
|
| 14 |
Cohen E, Ivenshitz M, Amor-Baroukh V, Greenberger V, Segal M (2008). Determinants of spontaneous activity in networks of cultured hippocampus. Brain Res , 1235: 21-30 doi: 10.1016/j.brainres.2008.06.022 pmid:18602907
|
| 15 |
Cortes C, Galindo F, Galicia S, Cebada J, Flores A (2013). Excitatory actions of GABA in developing chick vestibular afferents: Effects on resting electrical activity. Synapse , 67(7): 374-381 doi: 10.1002/syn.21646 pmid:23401185
|
| 16 |
Couillard-Després S (2013). Hippocampal neurogenesis and ageing. Curr Top Behav Neurosci , 15: 343-355 doi: 10.1007/7854_2012_232 pmid:23065635
|
| 17 |
Couillard-Despres S, Iglseder B, Aigner L (2011). Neurogenesis, cellular plasticity and cognition: the impact of stem cells in the adult and aging brain—a mini-review. Gerontology , 57(6): 559-564 doi: 10.1159/000323481 pmid:21311170
|
| 18 |
Cryan J F, Slattery D A (2010). GABAB receptors and depression. Current status. Adv Pharmacol , 58: 427-451 doi: 10.1016/S1054-3589(10)58016-5 pmid:20655491
|
| 19 |
Cserép C, Szabadits E, Sz?nyi A, Watanabe M, Freund T F, Nyiri G (2012). NMDA receptors in GABAergic synapses during postnatal development. PLoS ONE , 7(5): e37753 doi: 10.1371/journal.pone.0037753 pmid:22662211
|
| 20 |
Curtis M A, Low V F, Faull R L (2012). Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation. Dev Neurobiol , 72(7): 990-1005 doi: 10.1002/dneu.22028 pmid:22539366
|
| 21 |
Daynac M, Chicheportiche A, Pineda J R, Gauthier L R, Boussin F D, Mouthon M A (2013). Quiescent neural stem cells exit dormancy upon alteration of GABAAR signaling following radiation damage. Stem Cell Res (Amst) , 11(1): 516-528 doi: 10.1016/j.scr.2013.02.008 pmid:23562833
|
| 22 |
Delpire E (2000). Cation-chloride cotransporters in neuronal communication. News Physiol Sci , 15: 309-312 pmid:11390932
|
| 23 |
Dieni C V, Chancey J H, Overstreet-Wadiche L S (2012). Dynamic functions of GABA signaling during granule cell maturation. Front Neural Circuits , 6: 113 pmid:23316139
|
| 24 |
Duan X, Chang J H, Ge S, Faulkner R L, Kim J Y, Kitabatake Y, Liu X B, Yang C H, Jordan J D, Ma D K, Liu C Y, Ganesan S, Cheng H J, Ming G L, Lu B, Song H (2007). Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell , 130(6): 1146-1158 doi: 10.1016/j.cell.2007.07.010 pmid:17825401
|
| 25 |
Dzhala V I, Talos D M, Sdrulla D A, Brumback A C, Mathews G C, Benke T A, Delpire E, Jensen F E, Staley K J (2005). NKCC1 transporter facilitates seizures in the developing brain. Nat Med , 11(11): 1205-1213 doi: 10.1038/nm1301 pmid:16227993
|
| 26 |
Eisch A J, Petrik D (2012). Depression and hippocampal neurogenesis: a road to remission? Science , 338(6103): 72-75 doi: 10.1126/science.1222941 pmid:23042885
|
| 27 |
Erlander M G, Tillakaratne N J, Feldblum S, Patel N, Tobin A J (1991). Two genes encode distinct glutamate decarboxylases. Neuron , 7(1): 91-100 doi: 10.1016/0896-6273(91)90077-D pmid:2069816
|
| 28 |
Espinosa J, Rocha A, Nunes F, Costa M S, Schein V, Kazlauckas V, Kalinine E, Souza D O, Cunha R A, Porciúncula L O (2013). Caffeine consumption prevents memory impairment, neuronal damage, and adenosine A2A receptors upregulation in the hippocampus of a rat model of sporadic dementia. J Alzheimers Dis , 34(2): 509-518 pmid:23241554
|
| 29 |
Faigle R, Song H (2013). Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta , 1830(2): 2435-2448 doi: 10.1016/j.bbagen.2012.09.002 pmid:22982587
|
| 30 |
Feierstein C E (2012). Linking adult olfactory neurogenesis to social behavior. Front Neurosci , 6: 173 doi: 10.3389/fnins.2012.00173 pmid:23226115
|
| 31 |
Feierstein C E, Lazarini F, Wagner S, Gabellec M M, de Chaumont F, Olivo-Marin J C, Boussin F D, Lledo P M, Gheusi G (2010). Disruption of adult neurogenesis in the olfactory bulb affects social interaction but not maternal behavior. Front Behav Neurosci , 4: 176 doi: 10.3389/fnbeh.2010.00176 pmid:21160552
|
| 32 |
Fernandes F S, de Souza A S, do Carmo M, Boaventura G T (2011). Maternal intake of flaxseed-based diet (Linum usitatissimum) on hippocampus fatty acid profile: implications for growth, locomotor activity and spatial memory. Nutrition , 27(10): 1040-1047 doi: 10.1016/j.nut.2010.11.001 pmid:21439792
|
| 33 |
Fernando R N, Eleuteri B, Abdelhady S, Nussenzweig A, And?ng M, Ernfors P (2011). Cell cycle restriction by histone H2AX limits proliferation of adult neural stem cells. Proc Natl Acad Sci USA , 108(14): 5837-5842 doi: 10.1073/pnas.1014993108 pmid:21436033
|
| 34 |
Fiumelli H, Woodin M A (2007). Role of activity-dependent regulation of neuronal chloride homeostasis in development. Curr Opin Neurobiol , 17(1): 81-86 doi: 10.1016/j.conb.2007.01.002 pmid:17234400
|
| 35 |
Foster P P, Rosenblatt K P, Kulji? R O (2011). Exercise-induced cognitive plasticity, implications for mild cognitive impairment and Alzheimer’s disease. Front Neurol , 2: 28 doi: 10.3389/fneur.2011.00028 pmid:21602910
|
| 36 |
Fotuhi M, Do D, Jack C (2012). Modifiable factors that alter the size of the hippocampus with ageing. Nat Rev Neurol , 8(4): 189-202 pmid:22410582
|
| 37 |
García-Verdugo J M, Ferrón S, Flames N, Collado L, Desfilis E, Font E (2002). The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res Bull , 57(6): 765-775 doi: 10.1016/S0361-9230(01)00769-9 pmid:12031273
|
| 38 |
Garrett L, Lie D C, Hrabé de Angelis M, Wurst W, H?lter S M (2012). Voluntary wheel running in mice increases the rate of neurogenesis without affecting anxiety-related behaviour in single tests. BMC Neurosci , 13(1): 61 doi: 10.1186/1471-2202-13-61 pmid:22682077
|
| 39 |
Gershon M D (2011). Behind an enteric neuron there may lie a glial cell. J Clin Invest , 121(9): 3386-3389 doi: 10.1172/JCI59573 pmid:21865648
|
| 40 |
Glasper E R, Gould E (2013). Sexual experience restores age-related decline in adult neurogenesis and hippocampal function. Hippocampus : n/a doi: 10.1002/hipo.22090 pmid:23460298
|
| 41 |
Gonzalez-Perez O (2012). Neural stem cells in the adult human brain. Biol Biomed Rep , 2(1): 59-69 pmid:23181200
|
| 42 |
Goto K, Kato G, Kawahara I, Luo Y, Obata K, Misawa H, Ishikawa T, Kuniyasu H, Nabekura J, Takaki M (2013). In vivo imaging of enteric neurogenesis in the deep tissue of mouse small intestine. PLoS ONE , 8(1): e54814 doi: 10.1371/journal.pone.0054814 pmid:23382976
|
| 43 |
Haan N, Goodman T, Najdi-Samiei A, Stratford C M, Rice R, El Agha E, Bellusci S, Hajihosseini M K (2013). Fgf10-expressing tanycytes add new neurons to the appetite/energy-balance regulating centers of the postnatal and adult hypothalamus. J Neurosci , 33(14): 6170-6180 doi: 10.1523/JNEUROSCI.2437-12.2013 pmid:23554498
|
| 44 |
Huang Y, Wang J J, Yung W H (2013). Coupling Between GABA-A Receptor and Chloride Transporter Underlies Ionic Plasticity in Cerebellar Purkinje Neurons. Cerebellum , 12(3): 328-330 doi: 10.1007/s12311-013-0453-3 pmid:23341142
|
| 45 |
Huehnchen P, Prozorovski T, Klaissle P, Lesemann A, Ingwersen J, Wolf S A, Kupsch A, Aktas O, Steiner B (2011). Modulation of adult hippocampal neurogenesis during myelin-directed autoimmune neuroinflammation. Glia , 59(1): 132-142 doi: 10.1002/glia.21082 pmid:20967885
|
| 46 |
Imayoshi I, Sakamoto M, Ohtsuka T, Kageyama R (2009). Continuous neurogenesis in the adult brain. Dev Growth Differ , 51(3): 379-386 doi: 10.1111/j.1440-169X.2009.01094.x pmid:19298551
|
| 47 |
Ivakine E A, Acton B A, Mahadevan V, Ormond J, Tang M, Pressey J C, Huang M Y, Ng D, Delpire E, Salter M W, Woodin M A, McInnes R R (2013). Neto2 is a KCC2 interacting protein required for neuronal Cl- regulation in hippocampal neurons. Proc Natl Acad Sci USA , 110(9): 3561-3566 doi: 10.1073/pnas.1212907110 pmid:23401525
|
| 48 |
Joseph N M, He S, Quintana E, Kim Y G, Nú?ez G, Morrison S J (2011). Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest , 121(9): 3398-3411 doi: 10.1172/JCI58186 pmid:21865643
|
| 49 |
Jun H, Mohammed Qasim Hussaini S, Rigby M J, Jang M H (2012). Functional role of adult hippocampal neurogenesis as a therapeutic strategy for mental disorders. Neural Plast , 2012: 854285 doi: 10.1155/2012/854285 pmid:23346419
|
| 50 |
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(4): 933-946 doi: 10.1016/S0306-4522(01)00149-X pmid:11457581
|
| 51 |
Keller M, Douhard Q, Baum M J, Bakker J (2006). Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem Senses , 31(4): 315-323 doi: 10.1093/chemse/bjj035 pmid:16484502
|
| 52 |
Kempermann G (2011). Neurogenesis in the hippocampus. In: Adult neurogenesis 2:Stem cells and neuronal development in the adult brain. , Oxford University Press, New York.
|
| 53 |
Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Tyzio R, Hirsch J, Dzhala V, Berger B, Ben-Ari Y (2001). Early development of neuronal activity in the primate hippocampus in utero. J Neurosci , 21(24): 9770-9781 pmid:11739585
|
| 54 |
Kim J Y, Liu C Y, Zhang F, Duan X, Wen Z, Song J, Feighery E, Lu B, Rujescu D, St Clair D, Christian K, Callicott J H, Weinberger D R, Song H, Ming G L (2012). Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell , 148(5): 1051-1064 doi: 10.1016/j.cell.2011.12.037 pmid:22385968
|
| 55 |
Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P, Pachnis V (2011). Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest , 121(9): 3412-3424 doi: 10.1172/JCI58200 pmid:21865647
|
| 56 |
Lee C, Hu J, Ralls S, Kitamura T, Loh Y P, Yang Y, Mukouyama Y S, Ahn S (2012). The molecular profiles of neural stem cell niche in the adult subventricular zone. PLoS ONE , 7(11): e50501 doi: 10.1371/journal.pone.0050501 pmid:23209762
|
| 57 |
Lee D A, Blackshaw S (2012). Functional implications of hypothalamic neurogenesis in the adult mammalian brain. Int J Dev Neurosci , 30(8): 615-621 doi: 10.1016/j.ijdevneu.2012.07.003 pmid:22867732
|
| 58 |
Lee M C, Inoue K, Okamoto M, Liu Y F, Matsui T, Yook J S, Soya H (2013). Voluntary resistance running induces increased hippocampal neurogenesis in rats comparable to load-free running. Neurosci Lett , 537: 6-10 doi: 10.1016/j.neulet.2013.01.005 pmid:23352660
|
| 59 |
Li J, Tang Y, Cai D (2012). IKKβ/NF-κB disrupts adult hypothalamic neural stem cells to mediate a neurodegenerative mechanism of dietary obesity and pre-diabetes. Nat Cell Biol , 14(10): 999-1012 doi: 10.1038/ncb2562 pmid:22940906
|
| 60 |
Lin D Y, Zhang S Z, Block E, Katz L C (2005). Encoding social signals in the mouse main olfactory bulb. Nature , 434(7032): 470-477 doi: 10.1038/nature03414 pmid:15724148
|
| 61 |
Liu X, Wang Q, Haydar T F, Bordey A (2005). Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat Neurosci , 8(9): 1179-1187 doi: 10.1038/nn1522 pmid:16116450
|
| 62 |
Lovatel G A, Elsner V R, Bertoldi K, Vanzella C, Moysés F S, Vizuete A, Spindler C, Cechinel L R, Netto C A, Muotri A R, Siqueira I R (2013). Treadmill exercise induces age-related changes in aversive memory, neuroinflammatory and epigenetic processes in the rat hippocampus. Neurobiol Learn Mem , 101: 94-102 doi: 10.1016/j.nlm.2013.01.007 pmid:23357282
|
| 63 |
Ludwig A, Uvarov P, Pellegrino C, Thomas-Crusells J, Schuchmann S, Saarma M, Airaksinen M S, Rivera C (2011a). Neurturin evokes MAPK-dependent upregulation of Egr4 and KCC2 in developing neurons. Neural Plast , 2011: 1-8 doi: 10.1155/2011/641248 pmid:21837281
|
| 64 |
Ludwig A, Uvarov P, Soni S, Thomas-Crusells J, Airaksinen M S, Rivera C (2011b). Early growth response 4 mediates BDNF induction of potassium chloride cotransporter 2 transcription. J Neurosci , 31(2): 644-649 doi: 10.1523/JNEUROSCI.2006-10.2011 pmid:21228173
|
| 65 |
Mak G K, Weiss S (2010). Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci , 13(6): 753-758 doi: 10.1038/nn.2550 pmid:20453850
|
| 66 |
Mao Y, Ge X, Frank C L, Madison J M, Koehler A N, Doud M K, Tassa C, Berry E M, Soda T, Singh K K, Biechele T, Petryshen T L, Moon R T, Haggarty S J, Tsai L H (2009). Disrupted in schizophrenia 1 regulates neuronal progenitor proliferation via modulation of GSK3β/β-catenin signaling. Cell , 136(6): 1017-1031 doi: 10.1016/j.cell.2008.12.044 pmid: PMID:19303846
|
| 67 |
Markwardt S J, Wadiche J I, Overstreet-Wadiche L S (2009). Input-specific GABAergic signaling to newborn neurons in adult dentate gyrus. J Neurosci , 29(48): 15063-15072 doi: 10.1523/JNEUROSCI.2727-09.2009 pmid:19955357
|
| 68 |
McDermott K W, Lantos P L (1990). Cell proliferation in the subependymal layer of the postnatal marmoset, Callithrix jacchus. Brain Res Dev Brain Res , 57(2): 269-277 doi: 10.1016/0165-3806(90)90053-2 pmid:2073725
|
| 69 |
McEown K, Treit D (2010). Inactivation of the dorsal or ventral hippocampus with muscimol differentially affects fear and memory. Brain Res , 1353: 145-151 doi: 10.1016/j.brainres.2010.07.030 pmid:20647005
|
| 70 |
McNay D E, Brian?on N, Kokoeva M V, Maratos-Flier E, Flier J S (2012). Remodeling of the arcuate nucleus energy-balance circuit is inhibited in obese mice. J Clin Invest , 122(1): 142-152 doi: 10.1172/JCI43134 pmid:22201680
|
| 71 |
Metzger M (2010). Neurogenesis in the enteric nervous system. Arch Ital Biol , 148(2): 73-83 pmid:20830970
|
| 72 |
Ming G L, Song H (2009). DISC1 partners with GSK3beta in neurogenesis. Cell , 136(6): 990-992 doi: 10.1016/j.cell.2009.03.005 pmid:19303839
|
| 73 |
Misane I, Kruis A, Pieneman A W, ?gren S O, Stiedl O (2013). GABA(A) receptor activation in the CA1 area of the dorsal hippocampus impairs consolidation of conditioned contextual fear in C57BL/6J mice. Behav Brain Res , 238: 160-169 doi: 10.1016/j.bbr.2012.10.027 pmid:23098796
|
| 74 |
Moss J, Toni N (2013). A circuit-based gatekeeper for adult neural stem cell proliferation: Parvalbumin-expressing interneurons of the dentate gyrus control the activation and proliferation of quiescent adult neural stem cells. Bioessays , 35(1): 28-33 doi: 10.1002/bies.201200136 pmid:23165996
|
| 75 |
Mu Y, Gage F H (2011). Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol Neurodegener , 6(1): 85 doi: 10.1186/1750-1326-6-85 pmid:22192775
|
| 76 |
Nakashiba T, Cushman J D, Pelkey K A, Renaudineau S, Buhl D L, McHugh T J, Rodriguez Barrera V, Chittajallu R, Iwamoto K S, McBain C J, Fanselow M S, Tonegawa S (2012). Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell , 149(1): 188-201 doi: 10.1016/j.cell.2012.01.046 pmid:22365813
|
| 77 |
Niibori Y, Yu T S, Epp J R, Akers K G, Josselyn S A, Frankland P W (2012). Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region. Nat Commun , 3: 1253 doi: 10.1038/ncomms2261 pmid:23212382
|
| 78 |
Owens D F, Kriegstein A R (2002). Is there more to GABA than synaptic inhibition? Nat Rev Neurosci , 3(9): 715-727 doi: 10.1038/nrn919 pmid:12209120
|
| 79 |
Pavlov I, Riekki R, Taira T (2004). Synergistic action of GABA-A and NMDA receptors in the induction of long-term depression in glutamatergic synapses in the newborn rat hippocampus. Eur J Neurosci , 20(11): 3019-3026 doi: 10.1111/j.1460-9568.2004.03806.x pmid:15579156
|
| 80 |
Pearce J M (2001). Ammon’s horn and the hippocampus. J Neurol Neurosurg Psychiatry , 71(3): 351 doi: 10.1136/jnnp.71.3.351 pmid:11511709
|
| 81 |
Penfield W, Milner B (1958). Memory deficit produced by bilateral lesions in the hippocampal zone. AMA Arch Neurol Psychiatry , 79(5): 475-497 doi: 10.1001/archneurpsyc.1958.02340050003001 pmid:13519951
|
| 82 |
Pierce A A, Xu A W (2010). De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J Neurosci , 30(2): 723-730 doi: 10.1523/JNEUROSCI.2479-09.2010 pmid:20071537
|
| 83 |
Platel J C, Dave K A, Bordey A (2008). Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol , 586(16): 3739-3743 doi: 10.1113/jphysiol.2008.155325 pmid:18467361
|
| 84 |
Platel J C, Stamboulian S, Nguyen I, Bordey A (2010). Neurotransmitter signaling in postnatal neurogenesis: The first leg. Brain Res Brain Res Rev , 63(1-2): 60-71 doi: 10.1016/j.brainresrev.2010.02.004 pmid:20188124
|
| 85 |
Raimondo J V, Markram H, Akerman C J (2012). Short-term ionic plasticity at GABAergic synapses. Front Synaptic Neurosci , 4: 5 doi: 10.3389/fnsyn.2012.00005 pmid:23087642
|
| 86 |
Recinto P, Samant A R, Chavez G, Kim A, Yuan C J, Soleiman M, Grant Y, Edwards S, Wee S, Koob G F, George O, Mandyam C D (2012). Levels of neural progenitors in the hippocampus predict memory impairment and relapse to drug seeking as a function of excessive methamphetamine self-administration. Neuropsychopharmacology , 37(5): 1275-1287 doi: 10.1038/npp.2011.315 pmid:22205547
|
| 87 |
Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch K P (2006). Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry , 11(5): 514-522 doi: 10.1038/sj.mp.4001791 pmid:16415915
|
| 88 |
Rinehart J, Vázquez N, Kahle K T, Hodson C A, Ring A M, Gulcicek E E, Louvi A, Bobadilla N A, Gamba G, Lifton R P (2011). WNK2 kinase is a novel regulator of essential neuronal cation-chloride cotransporters. J Biol Chem , 286(34): 30171-30180 doi: 10.1074/jbc.M111.222893 pmid:21733846
|
| 89 |
Rivera C, Li H, Thomas-Crusells J, Lahtinen H, Viitanen T, Nanobashvili A, Kokaia Z, Airaksinen M S, Voipio J, Kaila K, Saarma M (2002). BDNF-induced TrkB activation down-regulates the K+- Cl- cotransporter KCC2 and impairs neuronal Cl- extrusion. J Cell Biol , 159(5): 747-752 doi: 10.1083/jcb.200209011 pmid:12473684
|
| 90 |
Ruiz A J, Kullmann D M (2012). Ionotropic receptors at hippocampal mossy fibers: roles in axonal excitability, synaptic transmission, and plasticity. Front Neural Circuits , 6: 112 pmid:23316138
|
| 91 |
Saffrey M J (2013). Cellular changes in the enteric nervous system during ageing. Dev Biol , doi: 10.1016/j.ydbio.2013.03.015 pmid:23537898
|
| 92 |
Sahay A, Scobie K N, Hill A S, O’Carroll C M, Kheirbek M A, Burghardt N S, Fenton A A, Dranovsky A, Hen R (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature , 472(7344): 466-470 doi: 10.1038/nature09817 pmid:21460835
|
| 93 |
Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science , 301(5634): 805-809 doi: 10.1126/science.1083328 pmid:12907793
|
| 94 |
Saxe M D, Battaglia F, Wang J W, Malleret G, David D J, Monckton J E, Garcia A D, Sofroniew M V, Kandel E R, Santarelli L, Hen R, Drew M R (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA , 103(46): 17501-17506 doi: 10.1073/pnas.0607207103 pmid:17088541
|
| 95 |
Scoville W B, Milner B (1957). Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry , 20(1): 11-21 doi: 10.1136/jnnp.20.1.11 pmid:13406589
|
| 96 |
Scullin C S, Partridge L D (2012). Modulation by pregnenolone sulfate of filtering properties in the hippocampal trisynaptic circuit. Hippocampus , 22(11): 2184-2198 doi: 10.1002/hipo.22038 pmid:22648992
|
| 97 |
Sheridan G K, Pickering M, Twomey C, Moynagh P N, O’Connor J J, Murphy K J (2007). NF-κB activity in distinct neural subtypes of the rat hippocampus: Influence of time and GABA antagonism in acute slice preparations. Learn Mem , 14(8): 525-532 doi: 10.1101/lm.590007 pmid:17686946
|
| 98 |
Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, Geary C, Cross J C, Weiss S (2003). Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science , 299(5603): 117-120 doi: 10.1126/science.1076647 pmid:12511652
|
| 99 |
Song J, Zhong C, Bonaguidi M A, Sun G J, Hsu D, Gu Y, Meletis K, Huang Z J, Ge S, Enikolopov G, Deisseroth K, Luscher B, Christian K M, Ming G L, Song H (2012). Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature , 489(7414): 150-154 doi: 10.1038/nature11306 pmid:22842902
|
| 100 |
Speisman R B, Kumar A, Rani A, Foster T C, Ormerod B K (2013). Daily exercise improves memory, stimulates hippocampal neurogenesis and modulates immune and neuroimmune cytokines in aging rats. Brain Behav Immun , 28: 25-43 doi: 10.1016/j.bbi.2012.09.013 pmid:23078985
|
| 101 |
Squire L R (2009). The legacy of patient H.M. for neuroscience. Neuron , 61(1): 6-9 doi: 10.1016/j.neuron.2008.12.023 pmid:19146808
|
| 102 |
Suijo K, Inoue S, Ohya Y, Odagiri Y, Takamiya T, Ishibashi H, Itoh M, Fujieda Y, Shimomitsu T (2012). Resistance exercise enhances cognitive function in mouse. Int J Sports Med pmid:23041964
|
| 103 |
Suwabe T, Mistretta C M, Bradley R M (2013). Excitatory and inhibitory synaptic function in the rostral nucleus of the solitary tract in embryonic rat. Brain Res , 1490: 117-127 doi: 10.1016/j.brainres.2012.10.037 pmid:23107886
|
| 104 |
Szabadits E, Cserép C, Szonyi A, Fukazawa Y, Shigemoto R, Watanabe M, Itohara S, Freund T F, Nyiri G (2011). NMDA receptors in hippocampal GABAergic synapses and their role in nitric oxide signaling. J Neurosci , 31(16): 5893-5904 doi: 10.1523/JNEUROSCI.5938-10.2011 pmid:21508214
|
| 105 |
Tepav?evi? V, Lazarini F, Alfaro-Cervello C, Kerninon C, Yoshikawa K, García-Verdugo J M, Lledo P M, Nait-Oumesmar B, Baron-Van Evercooren A (2011). Inflammation-induced subventricular zone dysfunction leads to olfactory deficits in a targeted mouse model of multiple sclerosis. J Clin Invest , 121(12): 4722-4734 doi: 10.1172/JCI59145 pmid:22056384
|
| 106 |
Ueda S, Yoshimoto K, Kadowaki T, Hirata K, Sakakibara S (2010). Improved learning in microencephalic rats. Congenit Anom (Kyoto) , 50(1): 58-63 doi: 10.1111/j.1741-4520.2009.00265.x pmid:20201969
|
| 107 |
Valeeva G, Valiullina F, Khazipov R (2013). Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro. Front Cell Neurosci , 7: 20 doi: 10.3389/fncel.2013.00020 pmid:23467988
|
| 108 |
van den Berge S A, van Strien M E, Korecka J A, Dijkstra A A, Sluijs J A, Kooijman L, Eggers R, De Filippis L, Vescovi A L, Verhaagen J, van de Berg W D, Hol E M (2011). The proliferative capacity of the subventricular zone is maintained in the parkinsonian brain. Brain , 134(Pt 11): 3249-3263 doi: 10.1093/brain/awr256 pmid:22075520
|
| 109 |
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. Brain Res Dev Brain Res , 139(1): 59-66 doi: 10.1016/S0165-3806(02)00536-9 pmid:12414094
|
| 110 |
Wang D D, Kriegstein A R (2008). GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci , 28(21): 5547-5558 doi: 10.1523/JNEUROSCI.5599-07.2008 pmid:18495889
|
| 111 |
Winner B, Kohl Z, Gage F H (2011). Neurodegenerative disease and adult neurogenesis. Eur J Neurosci , 33(6): 1139-1151 doi: 10.1111/j.1460-9568.2011.07613.x pmid:21395858
|
| 112 |
Wojtowicz J M (2012). Adult neurogenesis. From circuits to models. Behav Brain Res , 227(2): 490-496 doi: 10.1016/j.bbr.2011.08.013 pmid:21893104
|
| 113 |
Zhang Y, Liu J, Yao S, Li F, Xin L, Lai M, Bracchi-Ricard V, Xu H, Yen W, Meng W, Liu S, Yang L, Karmally S, Liu J, Zhu H, Gordon J, Khalili K, Srinivasan S, Bethea J R, Mo X, Hu W (2012). Nuclear factor kappa B signaling initiates early differentiation of neural stem cells. Stem Cells , 30(3): 510-524 doi: 10.1002/stem.1006 pmid:22134901
|
| 114 |
Zhu L, Polley N, Mathews G C, Delpire E (2008). NKCC1 and KCC2 prevent hyperexcitability in the mouse hippocampus. Epilepsy Res , 79(2-3): 201-212 doi: 10.1016/j.eplepsyres.2008.02.005 pmid:18394864
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|