Adult hippocampal neurogenesis and its role in cognition

Wiley Interdisciplinary Reviews: Cognitive Science

Volumn 5, Issue 5, 2014, Pages 573-587

  Oomen, Charlotte A ^a,b,d   Bekinschtein, Pedro ^c   Kent, Brianne A ^a,b   Saksida, Lisa M ^a,b   Bussey, Timothy J ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Universidad de Buenos Aires   (Argentina)

^d RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84906501534     PISSN: 19395078     EISSN: 19395086     Source Type: Journal    
DOI: 10.1002/wcs.1304     Document Type: Review

References (189)

1. Altman J. Are new neurons formed in the brains of adult mammals? Science 1962, 135:1127-1128.
2. Altman J. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec 1963, 145:573-591.
3. Cameron HA, Woolley CS, McEwen BS, Gould E. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 1993, 56:337-344.
4. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. Neurogenesis in the adult human hippocampus. Nat Med 1998, 4:1313-1317.
5. Altman J. 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 1969, 137:433-457.
6. Kaplan MS, Hinds JW. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 1977, 197:1092-1094.
7. Kempermann G. Adult neurogenesis, Stem Cells and Neuronal Development in the Adult Brain. New York: Oxford University Press; 2005.
8. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. 1957. J Neuropsychiatry Clin Neurosci 2000, 12:103-113.
9. Barnea A, Nottebohm F. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 1994, 91:11217-11221.
10. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 1999, 2:260-265.
11. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH. Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 2007, 10:727-734.
12. Vivar C, Potter MC, Choi J, Lee JY, Stringer TP, Callaway EM, Gage FH, Suh H, van Praag H. Monosynaptic inputs to new neurons in the dentate gyrus. Nat Commun 2012, 3:1107.
13. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 2008, 11:901-907.
14. Sun GJ, Sailor KA, Mahmood QA, Chavali N, Christian KM, Song H, Ming GL. Seamless reconstruction of intact adult-born neurons by serial end-block imaging reveals complex axonal guidance and development in the adult hippocampus. J Neurosci 2013, 33:11400-11411.
15. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature 2002, 415:1030-1034.
16. Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S. Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 2012, 15:1700-1706.
17. Esposito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF. Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 2005, 25:10074-10086.
18. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002, 3:728-739.
19. Laplagne DA, Esposito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF. Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 2006, 4:e409.
20. Laplagne DA, Kamienkowski JE, Esposito MS, Piatti VC, Zhao C, Gage FH, Schinder AF. Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 2007, 25:2973-2981.
21. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006, 439:589-593.
22. Song J, Sun J, Moss J, Wen Z, Sun GJ, Hsu D, Zhong C, Davoudi H, Christian KM, Toni N et al. Parvalbumin interneurons mediate neuronal circuitry-neurogenesis coupling in the adult hippocampus. Nat Neurosci 2013, 16:1728-1730.
23. Kim JY, Liu CY, Zhang F, Duan X, Wen Z, Song J, Feighery E, Lu B, Rujescu D, St Clair D et al. Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 2012, 148:1051-1064.
24. Gould E, Cameron HA, McEwen BS. Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J Comp Neurol 1994, 340:551-565.
25. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 2006, 442:929-933.
26. Marques-Mari AI, Nacher J, Crespo C, Gutierrez-Mecinas M, Martinez-Guijarro FJ, Blasco-Ibanez JM. Loss of input from the mossy cells blocks maturation of newly generated granule cells. Hippocampus 2007, 17:510-524.
27. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999, 2:266-270.
28. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997, 386:493-495.
29. Freund J, Brandmaier AM, Lewejohann L, Kirste I, Kritzler M, Kruger A, Sachser N, Lindenberger U, Kempermann G. Emergence of individuality in genetically identical mice. Science 2013, 340:756-759.
30. Cameron HA, Gould E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 1994, 61:203-209.
31. Tanapat P, Hastings NB, Reeves AJ, Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 1999, 19:5792-5801.
32. Garza JC, Guo M, Zhang W, Lu XY. Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J Biol Chem 2008, 283:18238-18247.
33. Galea LA. Gonadal hormone modulation of neurogenesis in the dentate gyrus of adult male and female rodents. Brain Res Rev 2008, 57:332-341.
34. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 2004, 19:131-144.
35. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 2000, 97:11032-11037.
36. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004, 7:841-846.
37. Duman RS, Nakagawa S, Malberg J. Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 2001, 25:836-844.
38. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
39. Schmidt-Hieber C, Jonas P, Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004, 429:184-187.
40. Ge S, Yang CH, Hsu KS, Ming GL, Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 2007, 54:559-566.
41. Mongiat LA, Esposito MS, Lombardi G, Schinder AF. Reliable activation of immature neurons in the adult hippocampus. PLoS One 2009, 4:e5320.
42. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 2006, 26:3-11.
43. Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN. Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci USA 2010, 107:7963-7968.
44. Lemaire V, Tronel S, Montaron MF, Fabre A, Dugast E, Abrous DN. Long-lasting plasticity of hippocampal adult-born neurons. J Neurosci 2012, 32:3101-3108.
45. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA. Integration of new neurons into functional neural networks. J Neurosci 2006, 26:12237-12241.
46. van Strien NM, Cappaert NL, Witter MP. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 2009, 10:272-282.
47. Steward O, Scoville SA. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 1976, 169:347-370.
48. Treves A, Tashiro A, Witter MP, Moser EI. What is the mammalian dentate gyrus good for? Neuroscience 2008, 154:1155-1172.
49. Scharfman HE. The CA3 "backprojection" to the dentate gyrus. Prog Brain Res 2007, 163:627-637.
50. Jung MW, McNaughton BL. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 1993, 3:165-182.
51. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
52. Neunuebel JP, Knierim JJ. Spatial firing correlates of physiologically distinct cell types of the rat dentate gyrus. J Neurosci 2012, 32:3848-3858.
53. Lambert JD, Jones RS. A reevaluation of excitatory amino acid-mediated synaptic transmission in rat dentate gyrus. J Neurophysiol 1990, 64:119-132.
54. Scharfman HE. Dentate hilar cells with dendrites in the molecular layer have lower thresholds for synaptic activation by perforant path than granule cells. J Neurosci 1991, 11:1660-1673.
55. Ewell LA, Jones MV. Frequency-tuned distribution of inhibition in the dentate gyrus. J Neurosci 2010, 30:12597-12607.
56. Rolls ET. A computational theory of episodic memory formation in the hippocampus. Behav Brain Res 2010, 215:180-196.
57. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 2005, 15:579-586.
58. Henze DA, McMahon DB, Harris KM, Barrionuevo G. Giant miniature EPSCs at the hippocampal mossy fiber to CA3 pyramidal cell synapse are monoquantal. J Neurophysiol 2002, 87:15-29.
59. O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 1971, 34:171-175.
60. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 2005, 309:619-623.
61. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
62. Burwell RD. The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 2000, 911:25-42.
63. Burwell RD, Amaral DG. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 1998, 398:179-205.
64. Carlsen J, De Olmos J, Heimer L. Tracing of two-neuron pathways in the olfactory system by the aid of transneuronal degeneration: projections to the amygdaloid body and hippocampal formation. J Comp Neurol 1982, 208:196-208.
65. Knierim JJ. Neural representations of location outside the hippocampus. Learn Mem 2006, 13:405-415.
66. Hargreaves EL, Rao G, Lee I, Knierim JJ. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 2005, 308:1792-1794.
67. Renno-Costa C, Lisman JE, Verschure PF. The mechanism of rate remapping in the dentate gyrus. Neuron 2010, 68:1051-1058.
68. Piatti VC, Ewell LA, Leutgeb JK. Neurogenesis in the dentate gyrus: carrying the message or dictating the tone. Front Neurosci 2013, 7:50.
69. Xavier GF, Costa VC. Dentate gyrus and spatial behaviour. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:762-773.
70. Kesner RP. An analysis of the dentate gyrus function. Behav Brain Res 2013, 254:1-7.
71. McLamb RL, Mundy WR, Tilson HA. Intradentate colchicine disrupts the acquisition and performance of a working memory task in the radial arm maze. Neurotoxicology 1988, 9:521-528.
72. Walsh TJ, Schulz DW, Tilson HA, Schmechel DE. Colchicine-induced granule cell loss in rat hippocampus: selective behavioral and histological alterations. Brain Res 1986, 398:23-36.
73. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ. Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 1989, 76:485-496.
74. Jeltsch H, Bertrand F, Lazarus C, Cassel JC. Cognitive performances and locomotor activity following dentate granule cell damage in rats: role of lesion extent and type of memory tested. Neurobiol Learn Mem 2001, 76:81-105.
75. Lee I, Kesner RP. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 2004, 14:301-310.
76. Hernandez-Rabaza V, Hontecillas-Prieto L, Velazquez-Sanchez C, Ferragud A, Perez-Villaba A, Arcusa A, Barcia JA, Trejo JL, Canales JJ. The hippocampal dentate gyrus is essential for generating contextual memories of fear and drug-induced reward. Neurobiol Learn Mem 2008, 90:553-559.
77. Costa VC, Bueno JL, Xavier GF. Dentate gyrus-selective colchicine lesion and performance in temporal and spatial tasks. Behav Brain Res 2005, 160:286-303.
78. Emerich DF, Walsh TJ. Selective working memory impairments following intradentate injection of colchicine: attenuation of the behavioral but not the neuropathological effects by gangliosides GM1 and AGF2. Physiol Behav 1989, 45:93-101.
79. Gilbert PE, Kesner RP, Lee I. Dissociating hippocampal subregions: double dissociation between dentate gyrus and CA1. Hippocampus 2001, 11:626-636.
80. Marr D. Simple memory: a theory for archicortex. Philos Trans R Soc Lond B Biol Sci 1971, 262:23-81.
81. McNaughton BL, Morris RGM. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 1987, 10:408-415.
82. Treves A, Rolls ET. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 1992, 2:189-199.
83. Leutgeb JK, Leutgeb S, Moser MB, Moser EI. Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 2007, 315:961-966.
84. Park E, Dvorak D, Fenton AA. Ensemble place codes in hippocampus: CA1, CA3, and dentate gyrus place cells have multiple place fields in large environments. PLoS One 2011, 6:e22349.
85. Neunuebel JP, Knierim JJ. CA3 retrieves coherent representations from degraded input: direct evidence for CA3 pattern completion and dentate gyrus pattern separation. Neuron 2014, 81:416-427.
86. Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning. Behav Neurosci 1998, 112:863-874.
87. Selden NR, Everitt BJ, Jarrard LE, Robbins TW. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 1991, 42:335-350.
88. Gilbert PE, Kesner RP, DeCoteau WE. Memory for spatial location: role of the hippocampus in mediating spatial pattern separation. J Neurosci 1998, 18:804-810.
89. McTighe SM, Mar AC, Romberg C, Bussey TJ, Saksida LM. A new touchscreen test of pattern separation: effect of hippocampal lesions. Neuroreport 2009, 20:881-885.
90. Talpos JC, McTighe SM, Dias R, Saksida LM, Bussey TJ. Trial-unique, delayed nonmatching-to-location (TUNL): a novel, highly hippocampus-dependent automated touchscreen test of location memory and pattern separation. Neurobiol Learn Mem 2010, 94:341-352.
91. Lee I, Solivan F. Dentate gyrus is necessary for disambiguating similar object-place representations. Learn Mem 2010, 17:252-258.
92. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 2007, 317:94-99.
93. Bekinschtein P, Kent BA, Oomen CA, Clemenson GD Jr, Gage FH, Saksida LM, Bussey TJ. BDNF in the dentate gyrus is required for consolidation of "pattern-separated" memories. Cell Rep 2013, 5:1-10.
94. Bakker A, Kirwan CB, Miller M, Stark CE. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319:1640-1642.
95. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410:372-376.
96. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E. Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 2002, 12:578-584.
97. Nokia MS, Anderson ML, Shors TJ. Chemotherapy disrupts learning, neurogenesis and theta activity in the adult brain. Eur J Neurosci 2012, 36:3521-3530.
98. Goodman T, Trouche S, Massou I, Verret L, Zerwas M, Roullet P, Rampon C. Young hippocampal neurons are critical for recent and remote spatial memory in adult mice. Neuroscience 2010, 171:769-778.
99. Ko HG, Jang DJ, Son J, Kwak C, Choi JH, Ji YH, Lee YS, Son H, Kaang BK. Effect of ablated hippocampal neurogenesis on the formation and extinction of contextual fear memory. Mol Brain 2009, 2:1.
100. Garthe A, Behr J, Kempermann G. Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 2009, 4:e5464.
101. Martinez-Canabal A, Akers KG, Josselyn SA, Frankland PW. Age-dependent effects of hippocampal neurogenesis suppression on spatial learning. Hippocampus 2013, 23:66-74.
102. Dupret D, Montaron MF, Drapeau E, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Methylazoxymethanol acetate does not fully block cell genesis in the young and aged dentate gyrus. Eur J Neurosci 2005, 22:778-783.
103. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, Costet P, Abrous DN, Piazza PV. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 2008, 3:e1959.
104. Fan Y, Liu Z, Weinstein PR, Fike JR, Liu J. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. Eur J Neurosci 2007, 25:38-46.
105. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, Mizumatsu S, VandenBerg SR, Fike JR. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 2004, 162:39-47.
106. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008, 11:1153-1161.
107. Farioli-Vecchioli S, Saraulli D, Costanzi M, Pacioni S, Cina I, Aceti M, Micheli L, Bacci A, Cestari V, Tirone F. The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol 2008, 6:e246.
108. Zhang CL, Zou Y, He W, Gage FH, Evans RM. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 2008, 451:1004-1007.
109. Meshi D, Drew MR, Saxe M, Ansorge MS, David D, Santarelli L, Malapani C, Moore H, Hen R. Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 2006, 9:729-731.
110. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005, 130:843-852.
111. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, Monckton JE, Garcia AD, Sofroniew MV, Kandel ER, Santarelli L et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 2006, 103:17501-17506.
112. Iwata Y, Suzuki K, Wakuda T, Seki N, Thanseem I, Matsuzaki H, Mamiya T, Ueki T, Mikawa S, Sasaki T et al. Irradiation in adulthood as a new model of schizophrenia. PLoS One 2008, 3:e2283.
113. Wojtowicz JM, Askew ML, Winocur G. The effects of running and of inhibiting adult neurogenesis on learning and memory in rats. Eur J Neurosci 2008, 27:1494-1502.
114. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, Lie DC, Squire LR, Gage FH. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 2009, 16:147-154.
115. Deng W, Saxe MD, Gallina IS, Gage FH. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 2009, 29:13532-13542.
116. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg SR, Morhardt DR, Fike JR. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 2004, 188:316-330.
117. Winocur G, Wojtowicz JM, Sekeres M, Snyder JS, Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 2006, 16:296-304.
118. Hernandez-Rabaza V, Llorens-Martin M, Velazquez-Sanchez C, Ferragud A, Arcusa A, Gumus HG, Gomez-Pinedo U, Perez-Villalba A, Rosello J, Trejo JL et al. Inhibition of adult hippocampal neurogenesis disrupts contextual learning but spares spatial working memory, long-term conditional rule retention and spatial reversal. Neuroscience 2009, 159:59-68.
119. Warner-Schmidt JL, Madsen TM, Duman RS. Electroconvulsive seizure restores neurogenesis and hippocampus-dependent fear memory after disruption by irradiation. Eur J Neurosci 2008, 27:1485-1493.
120. Jaholkowski P, Kiryk A, Jedynak P, Ben Abdallah NM, Knapska E, Kowalczyk A, Piechal A, Blecharz-Klin K, Figiel I, Lioudyno V et al. New hippocampal neurons are not obligatory for memory formation; cyclin D2 knockout mice with no adult brain neurogenesis show learning. Learn Mem 2009, 16:439-451.
121. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 2010, 11:339-350.
122. Koehl M, Abrous DN. A new chapter in the field of memory: adult hippocampal neurogenesis. Eur J Neurosci 2011, 33:1101-1114.
123. Marin-Burgin A, Schinder AF. Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res 2012, 227:391-399.
124. Kee N, Teixeira CM, Wang AH, Frankland PW. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 2007, 10:355-362.
125. Massa F, Koehl M, Wiesner T, Grosjean N, Revest JM, Piazza PV, Abrous DN, Oliet SH. Conditional reduction of adult neurogenesis impairs bidirectional hippocampal synaptic plasticity. Proc Natl Acad Sci USA 2011, 108:6644-6649.
126. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011, 472:466-470.
127. Kitamura T, Saitoh Y, Takashima N, Murayama A, Niibori Y, Ageta H, Sekiguchi M, Sugiyama H, Inokuchi K. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009, 139:814-827.
128. Lacefield CO, Itskov V, Reardon T, Hen R, Gordon JA. Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 2012, 22:106-116.
129. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 2009, 29:14484-14495.
130. Nottebohm F. Neuronal replacement in adult brain. Brain Res Bull 2002, 57:737-749.
131. Wiskott L, Rasch MJ, Kempermann G. A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 2006, 16:329-343.
132. Frankland PW, Kohler S, Josselyn SA. Hippocampal neurogenesis and forgetting. Trends Neurosci 2013, 36:497-503.
133. Josselyn SA, Frankland PW. Infantile amnesia: a neurogenic hypothesis. Learn Mem 2012, 19:423-433.
134. Chambers RA, Potenza MN, Hoffman RE, Miranker W. Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks. Neuropsychopharmacology 2004, 29:747-758.
135. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 2004, 42:535-552.
136. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M, Sopher B, Miller MW, Ware CB, Martin GM et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 2001, 32:911-926.
137. Van der Borght K, Havekes R, Bos T, Eggen BJ, Van der Zee EA. Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 2007, 121:324-334.
138. Akers KG, Martinez-Canabal A, Restivo L, Yiu AP, De Cristofaro A, Hsiang HL, Wheeler AL, Guskjolen A, Niibori Y, Shoji H et al. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 2014, 344:598-602.
139. Squire LR. Mechanisms of memory. Science 1986, 232:1612-1619.
140. Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, Lamarque S, Lemaire V, Oliet SH, Piazza PV, Abrous DN. Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 2007, 5:e214.
141. Becker S. A computational principle for hippocampal learning and neurogenesis. Hippocampus 2005, 15:722-738.
142. Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009, 325:210-213.
143. Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, Koehl M, Abrous DN. Adult-born neurons are necessary for extended contextual discrimination. Hippocampus 2012, 22:292-298.
144. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ et al. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 2012, 149:188-201.
145. Kheirbek MA, Tannenholz L, Hen R. NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J Neurosci 2012, 32:8696-8702.
146. Niibori Y, Yu TS, Epp JR, Akers KG, Josselyn SA, Frankland PW. Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region. Nat Commun 2012, 3:1253.
147. Creer DJ, Romberg C, Saksida LM, van Praag H, Bussey TJ. Running enhances spatial pattern separation in mice. Proc Natl Acad Sci USA 2010, 107:2367-2372.
148. Bekinschtein P, Oomen CA, Saksida LM, Bussey TJ. Effects of environmental enrichment and voluntary exercise on neurogenesis, learning and memory, and pattern separation: BDNF as a critical variable? Semin Cell Dev Biol 2011, 22:536-542.
149. Alme CB, Buzzetti RA, Marrone DF, Leutgeb JK, Chawla MK, Schaner MJ, Bohanick JD, Khoboko T, Leutgeb S, Moser EI et al. Hippocampal granule cells opt for early retirement. Hippocampus 2010, 20:1109-1123.
150. Marin-Burgin A, Mongiat LA, Pardi MB, Schinder AF. Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 2012, 335:1238-1242.
151. Aimone JB, Wiles J, Gage FH. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 2006, 9:723-727.
152. Aimone JB, Wiles J, Gage FH. Computational influence of adult neurogenesis on memory encoding. Neuron 2009, 61:187-202.
153. Bekinschtein P, Kent BA, Oomen CA, Clemenson GD, Gage FH, Saksida LM, Bussey TJ. Brain-derived neurotrophic factor interacts with adult-born immature cells in the dentate gyrus during consolidation of overlapping memories. Hippocampus 2014, 24:905-911.
154. Sahay A, Wilson DA, Hen R. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 2011, 70:582-588.
155. Burghardt NS, Park EH, Hen R, Fenton AA. Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 2012, 22:1795-1808.
156. Barense MD, Bussey TJ, Lee AC, Rogers TT, Davies RR, Saksida LM, Murray EA, Graham KS. Functional specialization in the human medial temporal lobe. J Neurosci 2005, 25:10239-10246.
157. Bussey TJ, Saksida LM. The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex. Eur J Neurosci 2002, 15:355-364.
158. Bussey TJ, Saksida LM. Memory, perception, and the ventral visual-perirhinal-hippocampal stream: thinking outside of the boxes. Hippocampus 2007, 17:898-908.
159. Cowell RA, Bussey TJ, Saksida LM. Components of recognition memory: dissociable cognitive processes or just differences in representational complexity? Hippocampus 2010, 20:1245-1262.
160. Nadel L, Peterson MA. The hippocampus: part of an interactive posterior representational system spanning perceptual and memorial systems. J Exp Psychol Gen 2013, 142:1242-1254.
161. Cowell RA, Bussey TJ, Saksida LM. Why does brain damage impair memory? A connectionist model of object recognition memory in perirhinal cortex. J Neurosci 2006, 26:12186-12197.
162. McTighe SM, Cowell RA, Winters BD, Bussey TJ, Saksida LM. Paradoxical false memory for objects after brain damage. Science 2010, 330:1408-1410.
163. Winters BD, Bartko SJ, Saksida LM, Bussey TJ. Scopolamine infused into perirhinal cortex improves object recognition memory by blocking the acquisition of interfering object information. Learn Mem 2007, 14:590-596.
164. Winters BD, Saksida LM, Bussey TJ. Paradoxical facilitation of object recognition memory after infusion of scopolamine into perirhinal cortex: implications for cholinergic system function. J Neurosci 2006, 26:9520-9529.
165. Goodale MA. Transforming vision into action. Vision Res 2011, 51:1567-1587.
166. Rauschecker JP, Scott SK. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 2009, 12:718-724.
167. Ungerleider L, Mishkin M. In: Ingle D, Goodale M, Mansfield R, eds. Analysis of Behavior. Cambridge, MA: MIT Press; 1983, 549-586.
168. Yassa MA, Stark CE. Pattern separation in the hippocampus. Trends Neurosci 2011, 34:515-525.
169. Azab M, Stark SM, Stark CE. Contributions of human hippocampal subfields to spatial and temporal pattern separation. Hippocampus 2014, 24:293-302.
170. Wood ER, Dudchenko PA, Eichenbaum H. The global record of memory in hippocampal neuronal activity. Nature 1999, 397:613-616.
171. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000, 27:623-633.
172. Saksida LM, Bussey TJ, Buckmaster CA, Murray EA. No effect of hippocampal lesions on perirhinal cortex-dependent feature-ambiguous visual discriminations. Hippocampus 2006, 16:421-430.
173. Saksida LM, Bussey TJ, Buckmaster CA, Murray EA. Impairment and facilitation of transverse patterning after lesions of the perirhinal cortex and hippocampus, respectively. Cereb Cortex 2007, 17:108-115.
174. Spalding KL, Bhardwaj RD, Buchholz BA, Druid H, Frisen J. Retrospective birth dating of cells in humans. Cell 2005, 122:133-143.
175. Dranovsky A, Hen R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 2006, 59:1136-1143.
176. Duman RS. Depression: a case of neuronal life and death? Biol Psychiatry 2004, 56:140-145.
177. Jacobs BL, Praag H, Gage FH. Adult brain neurogenesis and psychiatry: a novel theory of depression. Mol Psychiatry 2000, 5:262-269.
178. Voss MW, Vivar C, Kramer AF, van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci 2013, 17:525-544.
179. Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP. Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 2006, 11:514-522.
180. Boekhoorn K, Joels M, Lucassen PJ. Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis 2006, 24:1-14.
181. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA. Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA 2004, 101:343-347.
182. Marlatt MW, Lucassen PJ. Neurogenesis and Alzheimer's disease: biology and pathophysiology in mice and men. Curr Alzheimer Res 2010, 7:113-125.
183. Sahay A, Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci 2007, 10:1110-1115.
184. Czeh B, Lucassen PJ. What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? Eur Arch Psychiatry Clin Neurosci 2007, 257:250-260.
185. Eisch AJ, Eisch AJ, Cameron HA, Encinas JM, Meltzer LA, Ming GL, Overstreet-Wadiche LS. Adult neurogenesis, mental health, and mental illness: hope or hype? J Neurosci 2008, 28:11785-11791.
186. Coras R, Siebzehnrubl FA, Pauli E, Huttner HB, Njunting M, Kobow K, Villmann C, Hahnen E, Neuhuber W, Weigel D et al. Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans. Brain 2010, 133:3359-3372.
187. Bartko SJ, Cowell RA, Winters BD, Bussey TJ, Saksida LM. Heightened susceptibility to interference in an animal model of amnesia: impairment in encoding, storage, retrieval-or all three? Neuropsychologia 2010, 48:2987-2997.
188. Bussey TJ, Saksida LM, Murray EA. Impairments in visual discrimination after perirhinal cortex lesions: testing 'declarative' vs. 'perceptual-mnemonic' views of perirhinal cortex function. Eur J Neurosci 2003, 17:649-660.
189. Luu P, Sill OC, Gao L, Becker S, Wojtowicz JM, Smith DM. The role of adult hippocampal neurogenesis in reducing interference. Behav Neurosci 2012, 126:381-391.