Development of glutamatergic innervation during maturation of adult-born neurons

Cristina V. Dieni, Adam J. Wieckert, Linda Overstreet-Wadiche

PDF(1070 KB)
PDF(1070 KB)
Front. Biol. ›› 2015, Vol. 10 ›› Issue (4) : 310-320. DOI: 10.1007/s11515-015-1362-2
REVIEW
REVIEW

Development of glutamatergic innervation during maturation of adult-born neurons

Author information +
History +

Abstract

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.

Keywords

dentate gyrus / adult neurogenesis / glutamatergic innervation / granule cell / neuroprogenitor

Cite this article

Download citation ▾
Cristina V. Dieni, Adam J. Wieckert, Linda Overstreet-Wadiche. Development of glutamatergic innervation during maturation of adult-born neurons. Front. Biol., 2015, 10(4): 310‒320 https://doi.org/10.1007/s11515-015-1362-2

References

[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
CrossRef Pubmed Google scholar
[2]
Alvarez-Buylla A, Lim D A (2004). For the long run: maintaining germinal niches in the adult brain. Neuron, 41(5): 683–686
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[9]
Brus M, Keller M, Lévy F (2013). Temporal features of adult neurogenesis: differences and similarities across mammalian species. Front Neurosci, 7: 135
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[16]
Coulter D A, Carlson G C (2007). Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog Brain Res, 163: 235–243
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[22]
Durand G M, Kovalchuk Y, Konnerth A (1996). Long-term potentiation and functional synapse induction in developing hippocampus. Nature, 381(6577): 71–75
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[26]
Ewell L A, Jones M V (2010). Frequency-tuned distribution of inhibition in the dentate gyrus. J Neurosci, 30(38): 12597–12607
CrossRef Pubmed Google scholar
[27]
Frotscher M (1991). Target cell specificity of synaptic connections in the hippocampus. Hippocampus, 1(2): 123–130
CrossRef Pubmed Google scholar
[28]
Gage F H (2000). Mammalian neural stem cells. Science, 287(5457): 1433–1438
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[36]
Herman M A, Jahr C E (2007). Extracellular glutamate concentration in hippocampal slice. J Neurosci, 27(36): 9736–9741
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[41]
Jinde S, Zsiros V, Nakazawa K (2013). Hilar mossy cell circuitry controlling dentate granule cell excitability. Front Neural Circuits, 7: 14
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[50]
Leranth C, Hajszan T (2007). Extrinsic afferent systems to the dentate gyrus. Prog Brain Res, 163: 63–84
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[54]
Lisman J E, Jensen O (2013). The θ-γ neural code. Neuron, 77(6): 1002–1016
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[64]
Markwardt S, Overstreet-Wadiche L (2008). GABAergic signalling to adult-generated neurons. J Physiol, 586(16): 3745–3749
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[66]
McNaughton B L (1980). Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res, 199(1): 1–19
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[69]
Ming G L, Song H (2011). Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron, 70(4): 687–702
CrossRef Pubmed Google scholar
[70]
Mohapel P, Leanza G, Kokaia M, Lindvall O (2005). Forebrain acetylcholine regulates adult hippocampal neurogenesis and learning. Neurobiol Aging, 26(6): 939–946
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[80]
Park J H, Enikolopov G (2010). Transient elevation of adult hippocampal neurogenesis after dopamine depletion. Exp Neurol, 222(2): 267–276
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[89]
Sloviter R S, Lømo T (2012). Updating the lamellar hypothesis of hippocampal organization. Front Neural Circuits, 6: 102
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[99]
Suh H, Deng W, Gage F H (2009). Signaling in adult neurogenesis. Annu Rev Cell Dev Biol, 25(1): 253–275
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[108]
Vivar C, van Praag H (2013). Functional circuits of new neurons in the dentate gyrus. Front Neural Circuits, 7: 15
CrossRef Pubmed Google scholar
[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
Pubmed
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[112]
Witter M P (2007). The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res, 163: 43–61
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
Pubmed
[115]
Wu G, Malinow R, Cline H T (1996). Maturation of a central glutamatergic synapse. Science, 274(5289): 972–976
CrossRef Pubmed Google scholar
[116]
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell, 132(4): 645–660
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar
[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
CrossRef Pubmed Google scholar

Acknowledgements

We thank Ryan Vaden and Jose Carlos Gonzalez for critical reading of this manuscript. LOW is funded by NIH (R01NS064025).
Cristina V. Dieni, Adam J. Wieckert and Linda Overstreet-Wadiche declare that they have no conflict of interest. All animal procedures followed the Guide for the Care and Use of Laboratory Animals, US Public Health Service, and were approved by the University of Alabama at Birmingham Institutional Animal Care and Use Committee.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(1070 KB)

Accesses

Citations

Detail

Sections
Recommended

/