Development of glutamatergic innervation during maturation of adult-born neurons
Received date: 03 Apr 2015
Accepted date: 30 Apr 2015
Published date: 14 Aug 2015
Copyright
The dentate gyrus is the entrance of the hippocampal formation and a primary target of excitatory afferents from the entorhinal cortex that carry spatial and sensory information. Mounting evidence suggests that continual adult neurogenesis contributes to appropriate processing of cortical information. The ongoing integration of adult born neurons dynamically modulates connectivity of the network, potentially contributing to dentate cognitive function. Here we review the current understanding of how glutamatergic innervation develops during the progression of adult-born neuron maturation. Summarizing the developmental stages of dentate neurogenesis, we also demonstrate that new neurons at an immature stage of maturation begin to process afferent activity from both medial and lateral entorhinal cortices.
Cristina V. Dieni , Adam J. Wieckert , Linda Overstreet-Wadiche . Development of glutamatergic innervation during maturation of adult-born neurons[J]. Frontiers in Biology, 2015 , 10(4) : 310 -320 . DOI: 10.1007/s11515-015-1362-2
1 |
Abraham W C, McNaughton N (1984). Differences in synaptic transmission between medial and lateral components of the perforant path. Brain Res, 303(2): 251–260
|
2 |
Alvarez-Buylla A, Lim D A (2004). For the long run: maintaining germinal niches in the adult brain. Neuron, 41(5): 683–686
|
3 |
Amaral D G (1978). A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol, 182(4 Pt 2): 851–914
|
4 |
Amaral D G, Kurz J (1985). An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J Comp Neurol, 240(1): 37–59
|
5 |
Amaral D G, Witter M P (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31(3): 571–591
|
6 |
Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa J L (1997). GABAA, NMDA and AMPA receptors: a developmentally regulated ‘ménage à trois’. Trends Neurosci, 20(11): 523–529
|
7 |
Berg D A, Belnoue L, Song H, Simon A (2013). Neurotransmitter-mediated control of neurogenesis in the adult vertebrate brain. Development, 140(12): 2548–2561
|
8 |
Brunner J, Neubrandt M, Van-Weert S, Andrási T, Kleine Borgmann F B, Jessberger S, Szabadics J (2014). Adult-born granule cells mature through two functionally distinct states. eLife, 3: e03104
|
9 |
Brus M, Keller M, Lévy F (2013). Temporal features of adult neurogenesis: differences and similarities across mammalian species. Front Neurosci, 7: 135
|
10 |
Buckmaster P S, Strowbridge B W, Kunkel D D, Schmiege D L, Schwartzkroin P A (1992). Mossy cell axonal projections to the dentate gyrus molecular layer in the rat hippocampal slice. Hippocampus, 2(4): 349–362
|
11 |
Buckmaster P S, Wenzel H J, Kunkel D D, Schwartzkroin P A (1996). Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol, 366(2): 271–292
|
12 |
Campbell N R, Fernandes C C, Halff A W, Berg D K (2010). Endogenous signaling through alpha7-containing nicotinic receptors promotes maturation and integration of adult-born neurons in the hippocampus. J Neurosci, 30(26): 8734–8744
|
13 |
Chancey J H, Adlaf E W, Sapp M C, Pugh P C, Wadiche J I, Overstreet-Wadiche L S (2013). GABA depolarization is required for experience-dependent synapse unsilencing in adult-born neurons. J Neurosci, 33(15): 6614–6622
|
14 |
Chancey J H, Poulsen D J, Wadiche J I, Overstreet-Wadiche L (2014). Hilar mossy cells provide the first glutamatergic synapses to adult-born dentate granule cells. J Neurosci, 34(6): 2349–2354
|
15 |
Chiu C Q, Castillo P E (2008). Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus. Neuropharmacology, 54(1): 68–78
|
16 |
Coulter D A, Carlson G C (2007). Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog Brain Res, 163: 235–243
|
17 |
Deng W, Aimone J B, Gage F H (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci, 11(5): 339–350
|
18 |
Dent J A, Galvin N J, Stanfield B B, Cowan W M (1983). The mode of termination of the hypothalamic projection to the dentate gyrus: an EM autoradiographic study. Brain Res, 258(1): 1–10
|
19 |
Diaz J, Ridray S, Mignon V, Griffon N, Schwartz J C, Sokoloff P (1997). Selective expression of dopamine D3 receptor mRNA in proliferative zones during embryonic development of the rat brain. J Neurosci, 17(11): 4282–4292
|
20 |
Dieni C V, Nietz A K, Panichi R, Wadiche J I, Overstreet-Wadiche L (2013). Distinct determinants of sparse activation during granule cell maturation. J Neurosci, 33(49): 19131–19142
|
21 |
Domínguez-Escribà L, Hernández-Rabaza V, Soriano-Navarro M, Barcia J A, Romero F J, García-Verdugo J M, Canales J J (2006). Chronic cocaine exposure impairs progenitor proliferation but spares survival and maturation of neural precursors in adult rat dentate gyrus. Eur J Neurosci, 24(2): 586–594
|
22 |
Durand G M, Kovalchuk Y, Konnerth A (1996). Long-term potentiation and functional synapse induction in developing hippocampus. Nature, 381(6577): 71–75
|
23 |
Encinas J M, Michurina T V, Peunova N, Park J H, Tordo J, Peterson D A, Fishell G, Koulakov A, Enikolopov G (2011). Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell, 8(5): 566–579
|
24 |
Eriksson P S, Perfilieva E, Björk-Eriksson T, Alborn A M, Nordborg C, Peterson D A, Gage F H (1998). Neurogenesis in the adult human hippocampus. Nat Med, 4(11): 1313–1317
|
25 |
Espósito M S, Piatti V C, Laplagne D A, Morgenstern N A, Ferrari C C, Pitossi F J, Schinder A F (2005). Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci, 25(44): 10074–10086
|
26 |
Ewell L A, Jones M V (2010). Frequency-tuned distribution of inhibition in the dentate gyrus. J Neurosci, 30(38): 12597–12607
|
27 |
Frotscher M (1991). Target cell specificity of synaptic connections in the hippocampus. Hippocampus, 1(2): 123–130
|
28 |
Gage F H (2000). Mammalian neural stem cells. Science, 287(5457): 1433–1438
|
29 |
Ge S, Goh E L, Sailor K A, Kitabatake Y, Ming G L, Song H (2006). GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 439(7076): 589–593
|
30 |
Ge S, Pradhan D A, Ming G L, Song H (2007). GABA sets the tempo for activity-dependent adult neurogenesis. Trends Neurosci, 30(1): 1–8
|
31 |
Gilbert P E, Kesner R P, Lee I (2001). Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus, 11(6): 626–636
|
32 |
Goldowitz D, White W F, Steward O, Lynch G, Cotman C (1975). Anatomical evidence for a projection from the entorhinal cortex to the contralateral dentate gyrus of the rat. Exp Neurol, 47(3): 433–441
|
33 |
Gu Y, Arruda-Carvalho M, Wang J, Janoschka S R, Josselyn S A, Frankland P W, Ge S (2012). Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci, 15(12): 1700–1706
|
34 |
Hafting T, Fyhn M, Molden S, Moser M B, Moser E I (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052): 801–806
|
35 |
Hargreaves E L, Rao G, Lee I, Knierim J J (2005). Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science, 308(5729): 1792–1794
|
36 |
Herman M A, Jahr C E (2007). Extracellular glutamate concentration in hippocampal slice. J Neurosci, 27(36): 9736–9741
|
37 |
Höglinger G U, Rizk P, Muriel M P, Duyckaerts C, Oertel W H, Caille I, Hirsch E C (2004). Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci, 7(7): 726–735
|
38 |
Isaac J T, Crair M C, Nicoll R A, Malenka R C (1997). Silent synapses during development of thalamocortical inputs. Neuron, 18(2): 269–280
|
39 |
Isaac J T, Nicoll R A, Malenka R C (1995). Evidence for silent synapses: implications for the expression of LTP. Neuron, 15(2): 427–434
|
40 |
Itou Y, Nochi R, Kuribayashi H, Saito Y, Hisatsune T (2011). Cholinergic activation of hippocampal neural stem cells in aged dentate gyrus. Hippocampus, 21(4): 446–459
|
41 |
Jinde S, Zsiros V, Nakazawa K (2013). Hilar mossy cell circuitry controlling dentate granule cell excitability. Front Neural Circuits, 7: 14
|
42 |
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(10): 1145–1159
|
43 |
Kilbride J, Rush A M, Rowan M J, Anwyl R (2001). Presynaptic group II mGluR inhibition of short-term depression in the medial perforant path of the dentate gyrus in vitro. J Neurophysiol, 85(6): 2509–2515
|
44 |
Kiss J, Csáki A, Bokor H, Shanabrough M, Leranth C (2000). The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]D-aspartate autoradiographic and immunohistochemical study. Neuroscience, 97(4): 657–669
|
45 |
Kullmann D M (1994). Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron, 12(5): 1111–1120
|
46 |
Kumamoto N, Gu Y, Wang J, Janoschka S, Takemaru K, Levine J, Ge S (2012) A role for primary cilia in glutamatergic synaptic integration of adult-born neurons. Nat Neurosci, 15: 399–405, S391
|
47 |
Kwon H B, Castillo P E (2008). Role of glutamate autoreceptors at hippocampal mossy fiber synapses. Neuron, 60(6): 1082–1094
|
48 |
Laplagne D A, Espósito M S, Piatti V C, Morgenstern N A, Zhao C, van Praag H, Gage F H, Schinder A F (2006). Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol, 4(12): e409
|
49 |
Laurberg S, Sørensen K E (1981). Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentatae and subfield CA3). Brain Res, 212(2): 287–300
|
50 |
Leranth C, Hajszan T (2007). Extrinsic afferent systems to the dentate gyrus. Prog Brain Res, 163: 63–84
|
51 |
Leutgeb J K, Leutgeb S, Moser M B, Moser E I (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science, 315(5814): 961–966
|
52 |
Li Y, Stam F J, Aimone J B, Goulding M, Callaway E M, Gage F H (2013). Molecular layer perforant path-associated cells contribute to feed-forward inhibition in the adult dentate gyrus. Proc Natl Acad Sci USA, 110(22): 9106–9111
|
53 |
Liao D, Hessler N A, Malinow R (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature, 375(6530): 400–404
|
54 |
Lisman J E, Jensen O (2013). The θ-γ neural code. Neuron, 77(6): 1002–1016
|
55 |
Lübke J, Deller T, Frotscher M (1997). Septal innervation of mossy cells in the hilus of the rat dentate gyrus: an anterograde tracing and intracellular labeling study. Exp Brain Res, 114(3): 423–432
|
56 |
Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Götz M, Haas C A, Kempermann G, Taylor V, Giachino C (2010). Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell, 6(5): 445–456
|
57 |
Ma D K, Jang M H, Guo J U, Kitabatake Y, Chang M L, Pow-Anpongkul N, Flavell R A, Lu B, Ming G L, Song H (2009). Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science, 323(5917): 1074–1077
|
58 |
Ma W, Maric D, Li B S, Hu Q, Andreadis J D, Grant G M, Liu Q Y, Shaffer K M, Chang Y H, Zhang L, Pancrazio J J, Pant H C, Stenger D A, Barker J L (2000). Acetylcholine stimulates cortical precursor cell proliferation in vitro via muscarinic receptor activation and MAP kinase phosphorylation. Eur J Neurosci, 12(4): 1227–1240
|
59 |
Macek T A, Winder D G, Gereau R W 4th, Ladd C O, Conn P J (1996). Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol, 76(6): 3798–3806
|
60 |
Maglóczky Z, Acsády L, Freund T F (1994). Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus, 4(3): 322–334
|
61 |
Manzoni O, Bockaert J (1995). Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur J Neurosci, 7(12): 2518–2523
|
62 |
Manzoni O J, Castillo P E, Nicoll R A (1995). Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus. Neuropharmacology, 34(8): 965–971
|
63 |
Marín-Burgin A, Mongiat L A, Pardi M B, Schinder A F (2012). Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science, 335(6073): 1238–1242
|
64 |
Markwardt S, Overstreet-Wadiche L (2008). GABAergic signalling to adult-generated neurons. J Physiol, 586(16): 3745–3749
|
65 |
Markwardt S J, Dieni C V, Wadiche J I, Overstreet-Wadiche L (2011). Ivy/neurogliaform interneurons coordinate activity in the neurogenic niche. Nat Neurosci, 14(11): 1407–1409
|
66 |
McNaughton B L (1980). Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res, 199(1): 1–19
|
67 |
Mignone J L, Kukekov V, Chiang A S, Steindler D, Enikolopov G (2004). Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol, 469(3): 311–324
|
68 |
Milner T A, Bacon C E (1989). Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus. J Comp Neurol, 290(4): 544–560
|
69 |
Ming G L, Song H (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70(4): 687–702
|
70 |
Mohapel P, Leanza G, Kokaia M, Lindvall O (2005). Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging, 26(6): 939–946
|
71 |
Mongiat L A, Espósito M S, Lombardi G, Schinder A F (2009). Reliable activation of immature neurons in the adult hippocampus. PLoS ONE, 4(4): e5320
|
72 |
Moser E I, Roudi Y, Witter M P, Kentros C, Bonhoeffer T, Moser M B (2014). Grid cells and cortical representation. Nat Rev Neurosci, 15(7): 466–481
|
73 |
Mosko S, Lynch G, Cotman C W (1973). The distribution of septal projections to the hippocampus of the rat. J Comp Neurol, 152(2): 163–174
|
74 |
Mu Y, Zhao C, Gage F H (2011). Dopaminergic modulation of cortical inputs during maturation of adult-born dentate granule cells. J Neurosci, 31(11): 4113–4123
|
75 |
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
|
76 |
Neunuebel J P, Knierim J J (2012). Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J Neurosci, 32(11): 3848–3858
|
77 |
Nochi R, Kato T, Kaneko J, Itou Y, Kuribayashi H, Fukuda S, Terazono Y, Matani A, Kanatani S, Nakajima K, Hisatsune T (2012). Involvement of metabotropic glutamate receptor 5 signaling in activity-related proliferation of adult hippocampal neural stem cells. Eur J Neurosci, 36(3): 2273–2283
|
78 |
Overstreet Wadiche L, Bromberg D A, Bensen A L, Westbrook G L (2005). GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol, 94(6): 4528–4532
|
78a |
Overstreet-Wadiche L, Bensen A L, Westbrook G L (2006). Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci, 26(8): 2326–2334
|
79 |
Overstreet-Wadiche L S, Westbrook G L (2006). Functional maturation of adult-generated granule cells. Hippocampus, 16(3): 208–215
|
80 |
Park J H, Enikolopov G (2010). Transient elevation of adult hippocampal neurogenesis after dopamine depletion. Exp Neurol, 222(2): 267–276
|
81 |
Petersen R P, Moradpour F, Eadie B D, Shin J D, Kannangara T S, Delaney K R, Christie B R (2013). Electrophysiological identification of medial and lateral perforant path inputs to the dentate gyrus. Neuroscience, 252: 154–168
|
82 |
Piatti V C, Davies-Sala M G, Espósito M S, Mongiat L A, Trinchero M F, Schinder A F (2011). The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci, 31(21): 7715–7728
|
83 |
Regan J, Smalley M (2007). Prospective isolation and functional analysis of stem and differentiated cells from the mouse mammary gland. Stem Cell Rev, 3(2): 124–136
|
84 |
Regan M R, Huang Y H, Kim Y S, Dykes-Hoberg M I, Jin L, Watkins A M, Bergles D E, Rothstein J D (2007). Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci, 27(25): 6607–6619
|
85 |
Renzel R, Sadek A R, Chang C H, Gray W P, Seifert G, Steinhäuser C (2013). Polarized distribution of AMPA, but not GABAA, receptors in radial glia-like cells of the adult dentate gyrus. Glia, 61(7): 1146–1154
|
86 |
Sahay A, Wilson D A, Hen R (2011). Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron, 70(4): 582–588
|
87 |
Schmidt-Hieber C, Jonas P, Bischofberger J (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature, 429(6988): 184–187
|
88 |
Schmidt-Salzmann C, Li L, Bischofberger J (2014). Functional properties of extrasynaptic AMPA and NMDA receptors during postnatal hippocampal neurogenesis. J Physiol, 592(Pt 1): 125–140
|
89 |
Sloviter R S, Lømo T (2012). Updating the lamellar hypothesis of hippocampal organization. Front Neural Circuits, 6: 102
|
90 |
Snyder J S, Ferrante S C, Cameron H A (2012). Late maturation of adult-born neurons in the temporal dentate gyrus. PLoS ONE, 7(11): e48757
|
91 |
Soltesz I, Bourassa J, Deschênes M (1993). The behavior of mossy cells of the rat dentate gyrus during theta oscillations in vivo. Neuroscience, 57(3): 555–564
|
92 |
Song J, Sun J, Moss J, Wen Z, Sun G J, Hsu D, Zhong C, Davoudi H, Christian K M, Toni N, Ming G L, Song H (2013). Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus. Nat Neurosci, 16(12): 1728–1730
|
93 |
Spalding K L, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner H B, Boström E, Westerlund I, Vial C, Buchholz B A, Possnert G, Mash D C, Druid H, Frisén J (2013). Dynamics of hippocampal neurogenesis in adult humans. Cell, 153(6): 1219–1227
|
94 |
Spalding K L, Bhardwaj R D, Buchholz B A, Druid H, Frisén J (2005). Retrospective birth dating of cells in humans. Cell, 122(1): 133–143
|
95 |
Steward O (1976). Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol, 167(3): 285–314
|
96 |
Steward O, Scoville S A (1976). Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol, 169(3): 347–370
|
97 |
Stone S S, Teixeira C M, Zaslavsky K, Wheeler A L, Martinez-Canabal A, Wang A H, Sakaguchi M, Lozano A M, Frankland P W (2011). Functional convergence of developmentally and adult-generated granule cells in dentate gyrus circuits supporting hippocampus-dependent memory. Hippocampus, 21(12): 1348–1362
|
98 |
Suh H, Consiglio A, Ray J, Sawai T, D’Amour K A, Gage F H (2007). In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell, 1(5): 515–528
|
99 |
Suh H, Deng W, Gage F H (2009). Signaling in adult neurogenesis. Annu Rev Cell Dev Biol, 25(1): 253–275
|
100 |
Tashiro A, Sandler V M, Toni N, Zhao C, Gage F H (2006). NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature, 442(7105): 929–933
|
101 |
Temprana S G, Mongiat L A, Yang S M, Trinchero M F, Alvarez D D, Kropff E, Giacomini D, Beltramone N, Lanuza G M, Schinder A F (2015). Delayed coupling to feedback inhibition during a critical period for the integration of adult-born granule cells. Neuron, 85(1): 116–130
|
102 |
Toni N, Laplagne D A, Zhao C, Lombardi G, Ribak C E, Gage F H, Schinder A F (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci, 11(8): 901–907
|
103 |
Toni N, Teng E M, Bushong E A, Aimone J B, Zhao C, Consiglio A, van Praag H, Martone M E, Ellisman M H, Gage F H (2007). Synapse formation on neurons born in the adult hippocampus. Nat Neurosci, 10(6): 727–734
|
104 |
Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005). GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron, 47(6): 803–815
|
105 |
van Groen T, Miettinen P, Kadish I (2003). The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus, 13(1): 133–149
|
106 |
Vivar C, Potter M C, Choi J, Lee J Y, Stringer T P, Callaway E M, Gage F H, Suh H, van Praag H (2012). Monosynaptic inputs to new neurons in the dentate gyrus. Nat Commun, 3: 1107
|
107 |
Vivar C, Potter M C, van Praag H (2013). All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci, 15: 189–210
|
108 |
Vivar C, van Praag H (2013). Functional circuits of new neurons in the dentate gyrus. Front Neural Circuits, 7: 15
|
109 |
Vogt K E, Regehr W G (2001). Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci, 21(1): 75–83
|
110 |
Wang L P, Kempermann G, Kettenmann H (2005). A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci, 29(2): 181–189
|
111 |
Wang S, Scott B W, Wojtowicz J M (2000). Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol, 42(2): 248–257
|
112 |
Witter M P (2007). The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res, 163: 43–61
|
113 |
Witter M P, Amaral D G (1991). Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J Comp Neurol, 307(3): 437–459
|
114 |
Witter M P, Van Hoesen G W, Amaral D G (1989). Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci, 9(1): 216–228
|
115 |
Wu G, Malinow R, Cline H T (1996). Maturation of a central glutamatergic synapse. Science, 274(5289): 972–976
|
116 |
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660
|
117 |
Zhao C, Teng E M, Summers R G Jr, Ming G L, Gage F H (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci, 26(1): 3–11
|
118 |
Zhao S, Zhou Y, Gross J, Miao P, Qiu L, Wang D, Chen Q, Feng G (2010). Fluorescent labeling of newborn dentate granule cells in GAD67-GFP transgenic mice: a genetic tool for the study of adult neurogenesis. PLoS ONE, 5(9): 5
|
119 |
Zhou C, Wen Z X, Shi D M, Xie Z P (2004). Muscarinic acetylcholine receptors involved in the regulation of neural stem cell proliferation and differentiation in vitro. Cell Biol Int, 28(1): 63–67
|
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〈 | 〉 |