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2015, Number 1

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Rev Med UV 2015; 15 (1)

Hippocampus: neurogenesis and learning

Olivares HJD, Juárez AE, García GF

Language: Spanish
References: 103
Page: 20-28
PDF size: 920.07 Kb.


ABSTRACT

Learning and memory are two important cognitive processes for the adaptation and survival of organisms. Both behaviors are processed in the central nervous system and their regulation requires the participation of several brain structures. One of these structures is the hippocampus, which is associated in part with declarative memory. Interestingly, the hippocampus is one of two regions of the adult brain where new neurons are being produced. These new neurons have the ability to integrate into the hippocampal neural networks. Recent data suggest that new neurons participate in the regulation of cognitive functions associated with the hippocampus. Therefore, the aim of this review is to briefly describe evidences that show the functional role of new neurons in the context of learning and memory.


REFERENCES

  1. Roediger HL, McDermott KB. Two types of event memory. Proc Natl Acad Sci 2013; 110: 20856-857.

  2. Kandel, ER, Dudai Y, Mayford MR. The molecular and systems biology of memory. Cell 2014; 157:163–186.

  3. Griffin AL. Role of the thalamic nucleus reuniens in mediating interactions between the hippocampus and medial prefrontal cortex during spatial working memory. Front Syst Neurosci 2015 10; 9:29.

  4. Zanto TP, Rubens MT, Thangavel A, Gazzaley A. Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat Neurosci 2011; 14: 656-61.

  5. Squire LR, Dede AJ. Conscious and Unconscious Memory Systems. Cold Spring Harb Perspect Biol 2015 Mar 2;7(3)

  6. Ashby FG1, Turner BO, Horvitz JC. Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn Sci. 2010; 14:208-15.

  7. Timmann D, y col. The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex. 2010; 46: 845-57

  8. Duvarci S. Pare D. Amygdala microcircuits controlling learned fear. Neuron 2014; 482: 966–80.

  9. Sharon T, Moscovitch M, Gilboa A. Rapid neocortical acquisition of long-term arbitrary associations independent of the hippocampus. Proc Natl Acad Sci 2011; 108: 1146-51.

  10. Squire LR, Wixted JT. The cognitive neuroscience of human memory since HM. Annu Rev Neurosci 2011; 34: 259–88.

  11. Eichenbaum H. The cognitive neuroscience of memory: an introduction. Oxford University Press. 2011

  12. Ullman MT. Contributions of memory circuits to language: The declarative/procedural model. Cognition 2004; 92: 231-70.

  13. Keefe JO, Nadel L. The hippocampus as a cognitive map. Oxford: Clarendon Press. 1978.

  14. Burgess N, Maguire EA, O’Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002; 35:625–41.

  15. Buzsáki G, Moser EI. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 2013; 16:130–38.

  16. Morris RGM, y col. Memory reconsolidation: sensitivity of spatialmemory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 2006; 50, 479– 89

  17. Quiroga RQ. Concept cells: the building blocks of declarative memory functions. Nat Rev Neurosci 2012; 13: 587-97.

  18. Amaral DG, Witter MP. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neurosci 1989; 31:571-91.

  19. Lavenex P, Banta LP, Amaral DG: Postnatal development of the primate hippocampal formation. Dev Neurosci 2007; 29:179–19.

  20. Kivisaari SL, Probst A, Taylor KI. The Perirhinal, Entorhinal, and Parahippocampal Cortices and Hippocampus: An Overview of Functional Anatomy and Protocol for Their Segmentation in MR Images In fMRI. Springer Berlin Heidelberg 2013. p. 239-67.

  21. Witter MP, Wouterlood FG, Naber PA, Van Haeften T: Anatomical organization of the parahippocampal-hippocampal network. Ann NY Acad Sci 2000 Jun; 911:1-24.

  22. Lavenex P, Suzuki WA, Amaral DG. Perirhinal and parahippocampal cortices of the macaque monkey: Intrinsic projections and interconnections. J Comp Neurol. 2004; 472:371-94.

  23. Witter MP, Amaral DG. Entorhinal cortex of the monkey: V projections to the dentate gyrus, hippocampus, and subicular complex. J Comp Neurol 1991; 307:437-59.

  24. Khalaf-Nazzal R, Francis F. Hippocampal development - old and new findings. Neurosci 2013; 248:225-42.

  25. Laurberg S, Sorensen KE. Associational and commissural collaterals of neurons in the hippocampal formation (hilus fasciae dentate and subfield CA3. Brain Res 1981; 212:287–00.

  26. Ishizuka N, Weber J, Amaral DG. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 1990; 295:580–23.

  27. Frotscher M, Seress L, Schwerdtfeger WK, Buhl E. The mossy cells of the fascia dentate: a comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 1991; 312:145–63.

  28. Chicurel ME, Harris KM Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J Comp Neurol 1999; 325: 169-82.

  29. Suzuki W, Amaral DG: Perirhinal and parahippocampal cortices of the macaque monkey: cytoarchitectonic and chemoarchitectonic organization. J Comp Neurol 2003; 463:67–91

  30. Kim SM, Ganguli S, Frank LM. Spatial information outflow from the hippocampal circuit: distributed spatial coding and phase precession in the subiculum. J Neurosci 2012; 32: 11539-58.

  31. Zhang SJ, y col. Functional connectivity of the entorhinal– hippocampal space circuit. Philos Trans R Soc Lond B Biol Sci 2013 Dec 23; 369(1635):20120516.

  32. Eichenbaum H, Cohen NJ. Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron 2014; 83: 764-70.

  33. Giovanello KS, Verfaille M, Keane MM. Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn Affect Behav Neurosci 2003; 3: 186-94.

  34. Addis DR, y col. Characterizing spatial and temporal features of autobiographical memory retrieval networks: a partial least squares approach. Neuroimage 2004; 23: 1460-71.

  35. Bartsch T, Schönfeld R, Müller FJ, Alfke K, Leplow B, Aldenhoff J, Koch JM. Focal lesions of human hippocampal CA1 neurons in transient global amnesia impair place memory. Science 2010; 328: 1412-15.

  36. Churchwell JC, Morris AM, Musso ND, Kesner RP. Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory. Neurobiol Learn Mem 2010; 93: 415-21.

  37. Stone SS, y col. Stimulation of entorhinal cortex promotes adult neurogenesis and facilitates spatial memory. J Neurosci 2011; 31: 13469-84.

  38. Morris RG. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods1984; 11: 47-60.

  39. Moser E, Moser MB, Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J Neurosci 1993; 13: 3916-25.

  40. Laursen B, y col. Impaired hippocampal acetylcholine release parallels spatial memory deficits in Tg2576 mice subjected to basal forebrain cholinergic degeneration. Brain Res 2014; 1543: 253-62.

  41. Hales JB, Ocampo AC, Broadbent NJ, Clark RE. Hippocampal Infusion of Zeta Inhibitory Peptide Impairs Recent, but Not Remote, Recognition Memory in Rats. Neural Plasticity 2015; 501, 847136.

  42. Astur RS, Taylor LB, Mamelak AN, Philpott L, Sutherland RJ. Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav Brain Res 2005; 132: 77-84.

  43. Cornwell BR, Johnson LL, Holroyd T, Carver FW, Grillon C. Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J Neurosci 2008; 28:5983-90.

  44. Strange BA, Witter MP, Lein ES, Moser EI. Functional organization of the hippocampal longitudinal axis. Nature Rev Neurosci 2014; 15: 655-69.

  45. Hales JB, y col. Medial entorhinal cortex lesions only partially disrupt hippocampal place cells and hippocampus-dependent place memory. Cell Rep 2014; 9: 893-01.

  46. O´Keefe JA, Dostrovski J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 1971 34: 171-5.

  47. Hartley T, Lever C, Burgess N, O’Keefe J. Space in the brain: how the hippocampal formation supports spatial cognition. Philos Trans R Soc Lond B Biol Sci 2014; 369: 20120510.

  48. Moser MB, Rowland DC, Moser EI. Place cells, grid cells, and memory. Cold Spring Harb Perspect Med 2015; 7: a021808.

  49. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. Learning enhances adult neurogenesis in the hippocampal formation. Nature Neurosci 1999; 2: 260–5.

  50. Clemenson GD, Deng W, Gage FH. Environmental enrichment and neurogenesis: from mice to humans. Curr Opin Beh Sci 2015; 4: 56- 62.

  51. Cameron HA, Glover LR. Adult Neurogenesis: Beyond Learning and Memory. Annu Rev Psychol 2015; 66: 53-81.

  52. Cameron HA, Mckay RD. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 2001; 435: 406-17.

  53. Fernandes C, y col. Detrimental role of prolonged sleep deprivation on adult neurogenesis. Front Cell Neurosci, 2015; 9:140.

  54. Aimone JB, Deng W, Gage FH. Adult neurogenesis in the dentate gyrus. In Space, Time and Memory in the Hippocampal Formation. Springer Vienna 2015; pp. 409-429.

  55. Eriksson PS, y col. Neurogenesis in the adult human hippocampus. Nature Medicine 1998; 4: 1313-1317.

  56. Gage FH. Mammalian neural stem cells. Science 2000; 287: 1433–38.

  57. Drew LJ, Fusi S, Hen R. Adult neurogenesis in the mammalian hippocampus: Why the dentate gyrus? Learn Mem 2013; 20: 710-29.

  58. De La Rosa Prieto C, De Moya Pinilla M, Saiz-Sanchez D, Ubeda-banon I, Arzate DM, Flores-Cuadrado A, Martinez-Marcos A. Olfactory and cortical projections to bulbar and hippocampal adult-born neurons. Front Neuroanat. 2015; 9:4.

  59. Kempermann G, Jessberger S, Steiner B, Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004; 27:447-52.

  60. Duan L Peng CY, Pan L Kessler JA. Human Pluripotent Stem Cell- Derived Radial Glia Recapitulate Developmental Events and Provide Real-Time Access to Cortical Neurons and Astrocytes. Stem Cells Transl Med. 2015 Apr 1. pii: sctm.2014-0137.

  61. Kirby ED, Kuwahara AA, Messer RL, Wyss-Coray T. Adult hippocampal neural stem and progenitor cells regulate the neurogenic niche by secreting VEGF. Proc Natl Acad Sci U S A 2015; 112: 4128-33.

  62. Toriyama M, y col. Phosphorylation of doublecortin by protein kinase A orchestrates microtubule and actin dynamics to promote neuronal progenitor cell migration. J Biol Chem. 2012; 287:12691-702.

  63. Vukovic J1, Borlikova GG, Ruitenberg MJ, Robinson GJ, Sullivan RK, Walker TL, Bartlett PF. Immature doublecortin-positive hippocampal neurons are important for learning but not for remembering. J Neurosci. 2013; 33: 6603-13.

  64. Espósito 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; 25:10074–86.

  65. Cimadamore F, Amador-Arjona A, Chen C, Huang CT, Terskikh AV. SOX2–LIN28/let-7 pathway regulates proliferation and neurogenesis in neural precursors. Proc Natl Acad Sci U S A 2013; 110: E3017-E26.

  66. Kim HS, y col. PSA-NCAM+ Neural Precursor Cells from Human Embryonic Stem Cells Promote Neural Tissue Integrity and Behavioral Performance in a Rat Stroke Model. Stem Cell Rev 2014; 10: 761-771.

  67. Schmidt-Hieber C, Jonas P, Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 2004; 429:184–87.

  68. Ge S, y col. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006; 439:589–93.

  69. Lledo MP, Alononso M, Grubb MS. Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 2006; 7:179-93.

  70. Kim WR, Christian K, Ming GL, Song H. Time-dependent involvement of adult-born dentate granule cells in behavior. Behav Brain Res 2012; 227: 470-79.

  71. Benarroch EE. Adult neurogenesis in the dentate gyrus general concepts and potential implications. Neurology 2013; 81: 1443-52.

  72. Song J, M Christian K, Ming GL, Song H. Modification of hippocampal circuitry by adult neurogenesis. Dev Neurobiol 2012; 72: 1032-43.

  73. Imayoshi I, Kageyama R. The role of Notch signaling in adult neurogenesis. Mol Neurobiol 2011; 44: 7-12.

  74. Mu L, y col. SoxC transcription factors are required for neuronal differentiation in adult hippocampal neurogenesis. J Neurosci 2012; 32: 3067-80.

  75. Gould E, Vail N, Wagers M, Gross CG. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci U S A 2001; 98:10910-17.

  76. Fabel K, y col. Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci 2009; 3:50.

  77. Kempermann, G. Activity-Based Maintenance of Adult Hippocampal Neurogenesis: Maintaining a Potential for Lifelong Plasticity. In Neural Stem Cells in Development, Adulthood and Disease 2015 (pp. 119-123). Springer New York.

  78. Zhao C, Deng W, Gage FH. Mechanisms and functional implications of adult neurogenesis. Cell 2008;132: 645–60

  79. Clelland D, y col. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009; 325: 210-13.

  80. Speisman RB, y col. Environmental enrichment restores neurogenesis and rapid acquisition in aged rats. Neurobiol Aging 2013; 34: 263-74.

  81. Merritt JR, Rhodes JS. Mouse genetic differences in voluntary wheel running, adult hippocampal neurogenesis and learning on the multistrain- adapted plus water maze. Behav Brain Res 2015; 280: 62-71.

  82. Deng W, Gage FH. The effect of immature adult-born dentate granule cells on hyponeophagial behavior is related to their roles in learning and memory. Front Syst Neurosci 2015; 9.

  83. Opendak M, Gould E. Adult neurogenesis: a substrate for experiencedependent change. Trends Cogn Sci 2015; 19: 151-61.

  84. Trinchero MF, y col. Effects of spaced learning in the water maze on development of dentate granule cells generated in adult mice. Hippocampus 2015. doi: 10.1002/hipo.22438.

  85. Jamal AL, y col. Transplanted dentate progenitor cells show increased survival in an enriched environment, but do not exert a neurotrophic effect on spatial memory within 2 weeks of engraftment. Cell Transplan 2015. http://dx.doi.org/10.3727/096368915X687011

  86. Peters M, Muñoz-López M, Morris RG. Spatial memory and hippocampal enhancement. Current Opinion in Behavioral Sciences 2015. http://dx.doi.org/10.1016/j.cobeha.2015.03.005

  87. Dobrossy MD, y col. Differential effects of learning on neurogenesis: Learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 2003; 8: 974-82.

  88. Leuner B, Mendolia-Loffredo S, Kozorovitskiy Y, Samburg D, Gould E, Shors TJ. Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J Neurosci 2004; 24: 7477-81.

  89. Dupret D, y col. Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS biology 2007; 5: e214.

  90. Dupret D, y col. Spatial relational memory requires hippocampal adult neurogenesis. PloS one 2008; 3: e1959.

  91. Epp JR, Haack AK., Galea LA. Activation and survival of immature neurons in the dentate gyrus with spatial memory is dependent on time of exposure to spatial learning and age of cells at examination. Neurobiol Learn Mem 2011; 95: 316-25.

  92. Lacefield CO, y col. Effects of adult‐generated granule cells on coordinated network activity in the dentate gyrus. Hippocampus 2012; 22: 106-16.

  93. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience 1999; 2: 266-70.

  94. Birch AM, McGarry NB, Kelly ÁM. Short‐term environmental enrichment, in the absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time‐dependent manner. Hippocampus 2013; 23: 437-50.

  95. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature 1997; 386: 493–95.

  96. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS. Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobi 1999; 39: 569-78.

  97. Hillman CH, Erickson KI, Kramer AF. Be smart, exercise your heart: exercise effects on brain and cognition. Nature Rev Neurosci 2008; 9:58–65.

  98. Erickson KI, y col. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci U S A. 2011; 108: 3017-22.

  99. Muotri AR, Zhao C, Marchetto MC, Gage FH. Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus 2009; 19:1002–07.

  100. Kempermann, G. New neurons for’survival of the fittest’. Nat Rev Neurosci. 2012; 13:727-36.

  101. Liu HL, Zhao G, Cai K, Zhao HH, Shi LD. Treadmill exercise prevents decline in spatial learning and memory in APP/PS1 transgenic mice through improvement of hippocampal long-term potentiation. Behav Brain Res. 2011;218:308-14.

  102. O’Callaghan RM, Ohle R, Kelly AM. The effects of forced exercise on hippocampal plasticity in the rat: A comparison of LTP, spatial- and non-spatial learning. Behav Brain Res. 2007; 176:362-6.

  103. Leraci A, Mallei A, Musazzi L, Popoli M. Physical exercise and acute restraint stress differentially modulate hippocampal brain-derived neurotrophic factor transcripts and epigenetic mechanisms in mice. Hippocampus. 2015 Mar 26. doi: 10.1002/hipo.22458.




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