Is there a link between adult neurogenesis and learning?

Hippocampus

Volumn 16, Issue 3, 2006, Pages 216-224

  Leuner, Benedetta ^a   Gould, Elizabeth ^a   Shors, Tracey J ^b  

^a PRINCETON UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

BrdU; Dentate gyrus; Eyeblink conditioning; Hippocampus; Memory; Water maze

Indexed keywords

ANIMAL BEHAVIOR; CELL COUNT; CELL FUNCTION; CELL MATURATION; CELL POPULATION; CELL SURVIVAL; DENTATE GYRUS; GABAERGIC TRANSMISSION; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MAZE TEST; MEMORY; MENTAL PERFORMANCE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; TASK PERFORMANCE;

ANIMALS; CELL PROLIFERATION; CONDITIONING, EYELID; DENTATE GYRUS; HUMANS; LEARNING; MAZE LEARNING; MODELS, ANIMAL; NEURONAL PLASTICITY; NEURONS; STEM CELLS;

EID: 33645098296     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20153     Document Type: Review

References (96)

1. Abrous DN, Adriani W, Montaron MF, Aurousseau C, Rougon G, Le Moal M, Piazza PV. 2002. Nicotine self-administration impairs hippocampal plasticity. J Neurosci 22:3656-3662.
2. Akirav I, Kozenicky M, Tal D, Sandi C, Venero C, Richter-Levin G. 2004. A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress. Learn Mem 11:188-195.
3. Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in adult rats. J Comp Neurol 124:319-335.
4. Alvarez-Buyalla A, Kirn JR, Nottebohm F. 1990. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249:1444-1446.
5. Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, Feri P, Sartini S, DelGrade P. 2000. Spatial learning affects immature granule cell survival in the adult dentate gyrus. Neurosci Lett 286:21-24.
6. Ambrogini P, Orsini L, Mancini C, Ferrri P, Ciaroni S, Cuppini R. 2004a. Learning may reduce neurogenesis in the adult rat dentate gyrus. Neurosci Lett 359:13-16.
7. Ambrogini P, Lattanzi D, Ciuffoli S, Agostini D, Bertini L, Stocchi V, Santi S, Cuppini R. 2004b. Morpho-functional characterization of neuronal cells at different stages of maturation in granule cell layer of adult rat dentate gyrus. Brain Res 1017:21-31.
8. Barnea A, Nottebohm F. 1994. Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci USA 91:11217-11221.
9. Barnea A, Nottebohm F. 1996. Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc Natl Acad Sci USA 93: 714-718.
10. Bartolomucci A, de Biurrun G, Czeh B, van Kampen M, Fuchs E. 2002. Selective enhancement of spatial learning under chronic psychosocial stress. Eur J Neurosci 15:1863-1866.
11. Bayer SA, Brunner RL, Hine R, Altman J. 1973. Behavioral effects of interference with postnatal acquisition of hippocampal granule cells. Nat New Biol 242:222-224.
12. Becker S. 2005. A computational principle for hippocampal learning and neurogenesis. Hippocampus 15:722-738.
13. Ben-Ari Y. 2001. Developing networks play a similar melody. Trends Neurosci 24:353-360.
14. Beylin AV, Talk AC, Ghandi CC, Wood GE, Matzel LD, Shors TJ. 2001. The role of the hippocampus in trace conditioning: temporal discontiguity or task difficulty. Neurobiol Learn Mem 76:447-461.
15. Bizon JL, Gallagher M. 2003. Production of new cells in the rat dentate gyrus over the lifespan: relation to cognitive decline. Eur J Neurosci 18:215-219.
16. Bruel-Jungerman E, Laroche S, Rampon C. 2005. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21:513-521.
17. Carlen M, Cassidy RM, Brismar H, Smith GA, Enquist LW, Frisen J. 2002. Functional integration of adult-born neurons. Curr Biol 12:606-608.
18. Cameron HA, Woolley CS, McEwen BS, Gould E. 1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56:337-344.
19. Cameron HA, McKay R. 2001. Adult neurogenesis produces a large pool of new granule neurons in the dentate gyrus. J Comp Neurol 435:406-417.
20. Chambers RA, Potenza MN, Hoffman RE, Miranker W. 2004. Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks. Neuropsychopharmacology 29:747-758.
21. Daniel JM, Fader AJ, Spencer AL, Dohanich GP. 1994. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm Behav 32:217-225.
22. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA. 2003. Short-term and long-term survival of new granule cells in the dentate gyrus. J Comp Neurol 460:563-572.
23. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC. 2004. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552.
24. de Quervain DJ, Roozendaal B, McGaugh JL. 1998. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394:787-790.
25. Diamond DM, Park CR, Heman KL, Rose GM. 1999. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9:542-552.
26. Dobrossy MD, Drapeau E, Aurousseau C, LeMoal M, Piazza PV, Abrous DN. 2003. Differential effects of learning in neurogenesis: learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8:974-982.
27. Drapeau E, Mayo W, Aurousseau C, LeMoal M, Piazza P, Abrous DN. 2003. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100:14385-14390.
28. Dupret D, Montaron MF, Drapeau E, Aurosseau C, LeMoal M, Piazza PV, Abrous DN. 2005. Methylazoxymethanol acetate does not fully block cell genesis in the young and aged dentate gyrus. Eur J Neurosci 22:778-783.
29. Eisch AJ, Barrot M, Schad CA, Self DW, Nestler EJ. 2000. Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci USA 97:7579-7584.
30. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 11:1313-1317.
31. Gazzara RA, Altman J. 1981. Early postnatal X-irradiation of the hippocampus and discrimination learning in adult rats. J Comp Physiol Psychol 95:484-495.
32. Goldman SA, Nottebohm F. 1983. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80:2390-2394.
33. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E. 1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168-3171.
34. Gould E, Reeves AJ, Fallah M, Tanapat P, Fuchs E. 1999a. Hippocampal neurogenesis in adult Old World primates. Proc Natl Acad Sci USA 96:5263-5267.
35. Gould E, Tanapat P, Hastings NB, Shors TJ. 1999b. Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 3:186-192.
36. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999c. Learning enhances neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
37. Gross CG. 2000. Neurogenesis in the adult brain: death of a dogma. Nature Rev Neurosci 1:67-73.
38. Hairston IS, Little MT, Scanlon MD, Barakat MT, Palmer TD, Sapolsky RM, Heller HC. 2005. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J Neurophysiol 94: 4224-4233.
39. Hastings N, Gould E. 1999. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413:146-154.
40. Holmes MM, Wide JK, Galea LA. 2002. Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behav Neurosci 116:928-934.
41. Huot RL, Plotsky PM, Lenox RH, McNamara RK. 2002. Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950:52-63.
42. Kaplan MS, Hinds JW. 1977. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-1094.
43. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
44. Kempermann G. 2002. Why new neurons? Possible functions for adult hippocampal neurogenesis. J Neurosci 22:635-638.
45. Kempermann G, Gage FH. 2002. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16:129-136.
46. Kempermann G, Kuhn HG, Gage FH. 1997. More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
47. Kim JJ, Clark RE, Thompson RF. 1995. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109:195-203.
48. Kirn J, O'Loughlin B, Kasparian S, Nottebohm F. 1994. Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc Natl Acad Sci USA 91:7844-7848.
49. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
50. Lamprecht R, LeDoux J. 2004. Structural plasticity and memory. Nat Rev Neurosci 5:45-54.
51. Lemaire V, Aurousseau C, LeMoal M, Abrous DN. 1999. Behavioral trait of reactivity to novelty is related to hippocampal neurogenesis. Eur J Neurosci 11:4006-4014.
52. Lemaire V, Koehl M, LeMoal M, Abrous DN. 2000. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97:11032-11037.
53. Leuner B, Mendolia-Loffredo S, Shors TJ. 2004a. High levels of estrogen enhance associative memory formation in ovariectomized females. Psychoneuroendocrinology 29:883-890.
54. Leuner B, Mendolia-Loffredo S, Shors TJ. 2004b. Males and females respond differently to controllability and antidepressant treatment. Biol Psychiatry 56:964-970.
55. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ. 2004c. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci 24:7477-7481.
56. Lombardino AJ, Li XC, Hertel M, Nottebohm F. 2005. Replaceable neurons and neurodegenerative disease share depressed UCHL1 levels. Proc Natl Acad Sci USA 102:8036-8041.
57. Luine V, Villegas M, Martinez C, McEwen BS. 1994. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167-170.
58. Luine VN, Richards ST, Wu VY, Beck KD. 1998. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav 34:149-162.
59. Madsen TM, Kristjansen PEG, Bolwig TG, Wortwein G. 2003. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119:635-642.
60. Markakis E, Gage F. 1999. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol 406:449-460.
61. Martin SJ, Grimwood PD, Morris RG. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
62. Matthews DB, Silvers JR. 2004. The use of acute ethanol administration as a tool to investigate multiple memory systems. Neurobiol Learn Mem 82:299-308.
63. McEchron MD, Bouwmeester H, Tseng W, Weiss C, Disterhoft JF. 1998. Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat. Hippocampus 8:638-646.
64. Mirescu C, Peters JD, Gould E. 2004. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841-846.
65. Monje ML, Mizumatsu S, Fike JR, Palmer TD. 2002. Irradiation induced neural precursor-cell dysfunction. Nat Med 8:955-962.
66. Moscovitch M, Rosenbaum RS, Gilboa A, Addis DR, Westmacott R, Grady C, McAndrews MP, Levine B, Black S, Winocur G, Nadel L. 2005. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 207:35-66.
67. Nixon K, Crews FT. 2002. Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. J Neurochem 83:1087-1093.
68. Nottebohm F. 1985. Neuronal replacement in adulthood. Ann NY Acad Sci 457:143-161.
69. Nyberg L. 2005. Any novelty in hippocampal formation and memory? Curr Opin Neurol 18:424-428.
70. Olariu A, Cleaver KM, Shore LE, Brewer MD, Cameron HA. 2005. A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrus. Hippocampus 15:750-762.
71. Pham K, McEwen BS, Ledoux JE, Nader K. 2005. Fear learning transiently impairs hippocampal cell proliferation. Neuroscience 130: 17-24.
72. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, Mizumatsu S, Vandenberg SR, Fike JR. 2004. Radiation induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162:39-47.
73. Ramirez OA, Carrer HF. 1989. Correlation between threshold to induce long-term potentiation in the hippocampus and performance in a shuttle box avoidance response in rats. Neurosci Lett 104:152-156.
74. Rola R, Raber J, Rizk A, Otsuka S, Vandenberg SR, Morhardt DR, Fike JR. 2004. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 188:316-330.
75. Scerri C, Stewart CA, Breen KC, Balfour DJ. 2005. The effects of chronic nicotine on spatial learning and bromodeoxyuridine incorporation into the dentate gyrus of the rat. Psychopharmacology 16:1-7.
76. Schmidt-Hieber C, Jonas P, Bischofberger J. 2004. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
77. Scoville WB, Milner B. 1957. Loss of recent memory after bilateral hippocampal lesions. Neurol Neurosurg Psychiatry 20:11-21.
78. Shapiro ML, Tanila H, Eichenbaum H. 1997. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7:624-642.
79. Shors TJ. 2004. Memory traces of trace memories: neurogenesis, synpatogenesis and awareness. Trends Neurosci 27:250-256.
80. Shors TJ, Miesagaes G, Beylin A, Zhao M, Rydel T, Gould E. 2001. Neurogenesis in the adult rat is involved in the formation of trace memories. Nature 410:372-376.
81. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E. 2002. Neurogenesis may relate to some but not all types of hippocampal dependent learning. Hippocampus 12:578-584.
82. Snyder JS, Kee N, Wojtowicz JM. 2001. Effects of adult neurogenesis in synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85:2423-2431.
83. Snyder JS, Hong NS, McDonald R, Wojtowicz JM. 2005. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:843-852.
84. Spain JW, Newsom GC. 1991. Chronic opioids impair acquisition of both radial maze and Y-maze choice escape, Psychopharmacology 105:101-106.
85. Squire LR. 1982. The neuropsychology of human memory. Annu Rev Neurosci 5:241-273.
86. Takehara K, Kawahara S, Kirino Y. 2003. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci 23:9897-9905.
87. Tanapat P, Hastings NB, Reeves AJ, Gould E. 1999. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792-5801.
88. Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E. 2001. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol 437:496-504.
89. Van der Borght K, Wallinga AE, Lutien PG, Eggen BJL, Van der Zee EA. 2005a. Morris water maze learning in two rat strains increases the expression of the polysialyated form of the neural cell adhesion molecule in the dentate gyrus but has no effect on hippocampal neurogenesis. Behav Neurosci 119:926-932.
90. Van der Borght K, Meerlo P, Lutien PGM, Eggen BJL, Van der Zee EA. 2005b. Effects of active shock avoidance learning on hippocampal neurogenesis and plasma levels of corticosterone. Behav Brain Res 157:23-30.
91. van Praag H, Christie BR, Sejnowski TJ, Gage FH. 1999. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431.
92. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage F. 2002. Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
93. Vega CJ, Peterson DA. 2005. Stem cell proliferative history in tissue revealed by temporal halogenated thymidine analog discrimination. Nat Methods 2:167-169.
94. Wang S, Scott BW, Wojtowicz JM. 2000. Heterogeneous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257.
95. Weisz DJ, Clark GA, Thompson RF. 1984. Increased responsivity of dentate granule cells during nictitating membrane response conditioning in rabbit. Behav Brain Res 12:145-154.
96. Wood GE, Beylin AV, Shors TJ. 2001. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav Neurosci 115:175-187.