Home LiteratureArticle Details
PMID: 19186162 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Computational influence of adult neurogenesis on memory encoding.

Neuron ·Vol. 61 ·No. 2 ·2009-01-29 ·Pages 187-202

Aimone JB, Wiles J, Gage FH

Abstract

Adult neurogenesis in the hippocampus leads to the incorporation of thousands of new granule cells into the dentate gyrus every month, but its function remains unclear. Here, we present computational evidence that indicates that adult neurogenesis may make three separate but related contributions to memory formation. First, immature neurons introduce a degree of similarity to memories learned at the same time, a process we refer to as pattern integration. Second, the extended maturation and change in excitability of these neurons make this added similarity a time-dependent effect, supporting the possibility that temporal information is included in new hippocampal memories. Finally, our model suggests that the experience-dependent addition of neurons results in a dentate gyrus network well suited for encoding new memories in familiar contexts while treating novel contexts differently. Taken together, these results indicate that new granule cells may affect hippocampal function in several unique and previously unpredicted ways.

MeSH Terms
Age Factors Algorithms Animals Cell Proliferation Computer Simulation Dentate Gyrus/cytology,physiology Humans Memory/physiology Nerve Net/cytology,physiology Neural Pathways/cytology,physiology Neurogenesis/physiology Neuronal Plasticity/physiology Neurons/cytology,physiology Stem Cells/cytology,physiology Synapses/physiology Time Perception/physiology
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Aimone James B
Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
Wiles Janet
Gage Fred H
References (55)
55 references, click to expand
  1. Excitation-neurogenesis coupling in adult neural stem/progenitor cells.
    Neuron. 2004 May 27;42(4):535-52 PMID: 15157417
  2. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network.
    Science. 2007 Jul 6;317(5834):94-9 PMID: 17556551
  3. Neurogenesis may relate to some but not all types of hippocampal-dependent learning.
    Hippocampus. 2002;12(5):578-84 PMID: 12440573
  4. A computational theory of hippocampal function, and empirical tests of the theory.
    Prog Neurobiol. 2006 May;79(1):1-48 PMID: 16781044
  5. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus.
    Nat Neurosci. 2007 Mar;10(3):355-62 PMID: 17277773
  6. Spatial relational memory requires hippocampal adult neurogenesis.
    PLoS One. 2008 Apr 09;3(4):e1959 PMID: 18509506
  7. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus.
    J Neurosci. 2006 Jan 4;26(1):3-11 PMID: 16399667
  8. Neurons born in the adult dentate gyrus form functional synapses with target cells.
    Nat Neurosci. 2008 Aug;11(8):901-7 PMID: 18622400
  9. The cognitive neuroscience of constructive memory: remembering the past and imagining the future.
    Philos Trans R Soc Lond B Biol Sci. 2007 May 29;362(1481):773-86 PMID: 17395575
  10. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus.
    Nature. 2004 May 13;429(6988):184-7 PMID: 15107864
  11. Simulated apoptosis/neurogenesis regulates learning and memory capabilities of adaptive neural networks.
    Neuropsychopharmacology. 2004 Apr;29(4):747-58 PMID: 14702022
  12. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network.
    Hippocampus. 1992 Apr;2(2):189-99 PMID: 1308182
  13. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo.
    Nat Neurosci. 2002 Aug;5(8):790-5 PMID: 12118256
  14. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus.
    Nat Neurosci. 1999 Mar;2(3):266-70 PMID: 10195220
  15. From grid cells to place cells: a mathematical model.
    Hippocampus. 2006;16(12):1026-31 PMID: 17094145
  16. Adrenal steroids regulate postnatal development of the rat dentate gyrus: I. Effects of glucocorticoids on cell death.
    J Comp Neurol. 1991 Nov 15;313(3):479-85 PMID: 1770171
  17. Neuronal differentiation in the adult hippocampus recapitulates embryonic development.
    J Neurosci. 2005 Nov 2;25(44):10074-86 PMID: 16267214
  18. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats.
    J Comp Neurol. 1965 Jun;124(3):319-35 PMID: 5861717
  19. A role for adult TLX-positive neural stem cells in learning and behaviour.
    Nature. 2008 Feb 21;451(7181):1004-7 PMID: 18235445
  20. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies).
    Prog Brain Res. 2007;163:3-22 PMID: 17765709
  21. Microstructure of a spatial map in the entorhinal cortex.
    Nature. 2005 Aug 11;436(7052):801-6 PMID: 15965463
  22. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus.
    Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5638-43 PMID: 17374720
  23. NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus.
    Nature. 2006 Aug 24;442(7105):929-33 PMID: 16906136
  24. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice.
    Development. 2003 Jan;130(2):391-9 PMID: 12466205
  25. Spatial selectivity of unit activity in the hippocampal granular layer.
    Hippocampus. 1993 Apr;3(2):165-82 PMID: 8353604
  26. GABA regulates synaptic integration of newly generated neurons in the adult brain.
    Nature. 2006 Feb 2;439(7076):589-93 PMID: 16341203
  27. A computational principle for hippocampal learning and neurogenesis.
    Hippocampus. 2005;15(6):722-38 PMID: 15986407
  28. Synapse formation on neurons born in the adult hippocampus.
    Nat Neurosci. 2007 Jun;10(6):727-34 PMID: 17486101
  29. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus.
    Science. 2005 Jun 17;308(5729):1792-4 PMID: 15961670
  30. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage.
    J Neurosci. 2007 Mar 21;27(12):3252-9 PMID: 17376985
  31. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation.
    J Neurosci. 1996 Mar 15;16(6):2027-33 PMID: 8604047
  32. Adult hippocampal neurogenesis in depression.
    Nat Neurosci. 2007 Sep;10(9):1110-5 PMID: 17726477
  33. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning.
    Science. 2008 Feb 29;319(5867):1260-4 PMID: 18218862
  34. Learning enhances adult neurogenesis in the hippocampal formation.
    Nat Neurosci. 1999 Mar;2(3):260-5 PMID: 10195219
  35. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain.
    Neuron. 2007 May 24;54(4):559-66 PMID: 17521569
  36. Paradoxical influence of hippocampal neurogenesis on working memory.
    Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4642-6 PMID: 17360577
  37. More hippocampal neurons in adult mice living in an enriched environment.
    Nature. 1997 Apr 3;386(6624):493-5 PMID: 9087407
  38. Integrating memories in the human brain: hippocampal-midbrain encoding of overlapping events.
    Neuron. 2008 Oct 23;60(2):378-89 PMID: 18957228
  39. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off.
    Hippocampus. 1994 Dec;4(6):661-82 PMID: 7704110
  40. A behavioral assessment of hippocampal function based on a subregional analysis.
    Rev Neurosci. 2004;15(5):333-51 PMID: 15575490
  41. Neurogenesis in the adult human hippocampus.
    Nat Med. 1998 Nov;4(11):1313-7 PMID: 9809557
  42. Functional neurogenesis in the adult hippocampus.
    Nature. 2002 Feb 28;415(6875):1030-4 PMID: 11875571
  43. The cognitive neuroscience of memory distortion.
    Neuron. 2004 Sep 30;44(1):149-60 PMID: 15450167
  44. Is there a link between adult neurogenesis and learning?
    Hippocampus. 2006;16(3):216-24 PMID: 16421862
  45. Potential role for adult neurogenesis in the encoding of time in new memories.
    Nat Neurosci. 2006 Jun;9(6):723-7 PMID: 16732202
  46. Interneuron diversity series: containing the detonation--feedforward inhibition in the CA3 hippocampus.
    Trends Neurosci. 2003 Nov;26(11):631-40 PMID: 14585604
  47. Stress and adult neurogenesis.
    Hippocampus. 2006;16(3):233-8 PMID: 16411244
  48. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus.
    Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17501-6 PMID: 17088541
  49. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus.
    J Comp Neurol. 2001 Jul 9;435(4):406-17 PMID: 11406822
  50. A role for adult neurogenesis in spatial long-term memory.
    Neuroscience. 2005;130(4):843-52 PMID: 15652983
  51. Temporal encoding of place sequences by hippocampal cell assemblies.
    Neuron. 2006 Apr 6;50(1):145-57 PMID: 16600862
  52. Spike timing-dependent plasticity of neural circuits.
    Neuron. 2004 Sep 30;44(1):23-30 PMID: 15450157
  53. Pattern separation in the dentate gyrus and CA3 of the hippocampus.
    Science. 2007 Feb 16;315(5814):961-6 PMID: 17303747
  54. A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus.
    Hippocampus. 2006;16(3):329-43 PMID: 16435309
  55. Pattern separation in the human hippocampal CA3 and dentate gyrus.
    Science. 2008 Mar 21;319(5870):1640-2 PMID: 18356518
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
1097-4199
DOI
10.1016/j.neuron.2008.11.026
Published
2009-01-29
Pages
187-202
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC2670434
Subset
IM
Grants
NINDS NIH HHS · R01 NS050217 · United States
NINDS NIH HHS · R01 NS050217-04 · United States
NINDS NIH HHS · NS-050217 · United States
External Links
PubMed source DOI: 10.1016/j.neuron.2008.11.026 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2