The timing for neuronal maturation in the adult hippocampus is modulated by local network activity

Journal of Neuroscience

Volumn 31, Issue 21, 2011, Pages 7715-7728

  Piatti, Verónica C ^a   Davies Sala, M Georgina ^a   Espósito, M Soledad ^a   Mongiat, Lucas A ^a   Trinchero, Mariela F ^a   Schinder, Alejandro F ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; RETROVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; ELECTROENCEPHALOGRAM; EXERCISE; FEMALE; HIPPOCAMPUS; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGE FACTORS; ANIMALS; CELL DIFFERENTIATION; EXERCISE; FEMALE; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; NERVE NET; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; TIME FACTORS;

EID: 79957628653     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1380-11.2011     Document Type: Article

References (78)

1. Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85:523-569.
2. Aimone JB, Wiles J, Gage FH (2006) Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9:723-727.
3. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
4. Ambrogini P, Lattanzi D, Ciuffoli S, Agostini D, Bertini L, Stocchi V, Santi S, Cuppini R (2004) 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.
5. Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus-memory and anxiety. Neurosci Biobehav Rev 28:273-283.
6. Bast T, Feldon J (2003) Hippocampal modulation of sensorimotor processes. Prog Neurobiol 70:319-345.
7. Bast T, Wilson IA, Witter MP, Morris RG (2009) From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol 7:e1000089.
8. Bayer SA (1982) Changes in the total number of dentate granule cells in juvenile and adult rats: a correlated volumetric and 3H-thymidine autoradiographic study. Exp Brain Res 46:315-323.
9. Bergami M, Rimondini R, Santi S, Blum R, Götz M, Canossa M (2008) Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci U S A 105:15570-15575.
10. Bruel-Jungerman E, Davis S, Rampon C, Laroche S (2006) Long-term po-tentiation enhances neurogenesis in the adult dentate gyrus. J Neurosci 26:5888-5893.
11. Burrone J, O'Byrne M, Murthy VN (2002) Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420:414-418.
12. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA (2005) Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15:579-586.
13. Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295-301.
14. Czurkó A, Hirase H, Csicsvari J, Buzsa ́ki G (1999) Sustained activation of hippocampal pyramidal cells by ''space clamping'' in a running wheel. Eur J Neurosci 11:344-352.
15. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Shortterm and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
16. Dolorfo CL, Amaral DG (1998) Entorhinal cortex of the rat: organization of intrinsic connections. J Comp Neurol 398:49-82.
17. Ergorul C, Eichenbaum H (2004) The hippocampus and memory for ''what,'' ''where,'' and ''when.'' Learn Mem 11:397-405.
18. Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074-10086.
19. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19.
20. Flavell SW, Greenberg ME (2008) Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31:563-590.
21. Foster TC, Castro CA, McNaughton BL (1989) Spatial selectivity of rat hippocampal neurons: dependence on preparedness for movement. Science 244:1580-1582.
22. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305:1258-1264.
23. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593.
24. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559-566.
25. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
26. Jagasia R, Steib K, Englberger E, Herold S, Faus-Kessler T, Saxe M, Gage FH, Song H, Lie DC (2009) GABA-cAMP response element-binding protein signaling regulates maturation and survival of newly generated neurons in the adult hippocampus. J Neurosci 29:7966-7977.
27. Jinno S (2011) Topographic differences in adult neurogenesis in the mouse hippocampus: a stereology-based study using endogenous markers. Hippocampus 21:467- 480.
28. Jones SP, Rahimi O, O'Boyle MP, Diaz DL, Claiborne BJ (2003) Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 13:413-427.
29. Jung MW, Wiener SI, McNaughton BL (1994) Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347-7356.
30. Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355-362.
31. Kelsch W, Lin CW, Mosley CP, Lois C (2009) A critical period for activitydependent synaptic development during olfactory bulb adult neurogenesis. J Neurosci 29:11852-11858.
32. Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci U S A 99:10825-10830.
33. Laplagne DA, Espo ́ sito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4:e409.
34. Laplagne DA, Kamienkowski JE, Espo ́ sito MS, Piatti VC, Zhao C, Gage FH, Schinder AF (2007) Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 25:2973-2981.
35. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
36. Lin CW, Sim S, Ainsworth A, Okada M, Kelsch W, Lois C (2010) Genetically increased cell-intrinsic excitability enhances neuronal integration into adult brain circuits. Neuron 65:32-39.
37. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323:1074-1077.
38. Markwardt SJ, Wadiche JI, Overstreet-Wadiche LS (2009) Input-specific GABAergic signaling to newborn neurons in adult dentate gyrus. J Neurosci 29:15063-15072.
39. Maurer AP, Vanrhoads SR, Sutherland GR, Lipa P, McNaughton BL (2005) Self-motion and the origin of differential spatial scaling along the septotemporal axis of the hippocampus. Hippocampus 15:841- 852.
40. Merkle FT, Mirzadeh Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317:381-384.
41. Mongiat LA, Espó sito MS, Lombardi G, Schinder AF (2009) Reliable activation of immature neurons in the adult hippocampus. PLoS One 4:e5320.
42. Morgenstern NA, Lombardi G, Schinder AF (2008) Newborn granule cells in the aging dentate gyrus. J Physiol 586:3751-3757.
43. Moser MB, Moser EI, Forrest E, Andersen P, Morris RG (1995) Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A 92:9697-9701.
44. Overstreet-Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94:4528-4532.
45. Overstreet-Wadiche LS, Bensen AL, Westbrook GL (2006a) Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 26:2326-2334.
46. Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL (2006b) Seizures accelerate functional integration of adult-generated granule cells. J Neurosci 26:4095-4103.
47. Parent JM, Lowenstein DH (2002) Seizure-induced neurogenesis: are more new neurons good for an adult brain? Prog Brain Res 135:121-131.
48. Paxinos G, Franklin KBJ (1997) The mouse brain in stereotaxic coordinates. San Diego: Academic.
49. Petrovich GD, Canteras NS, Swanson LW (2001) Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Brain Res Rev 38:247-289.
50. Piatti VC, Espósito MS, Schinder AF (2006) The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist 12:463-468.
51. Platel JC, Dave KA, Gordon V, Lacar B, Rubio ME, Bordey A (2010) NMDA receptors activated by subventricular zone astrocytic glutamate are critical for neuroblast survival prior to entering a synaptic network. Neuron 65:859-872.
52. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA (2006) Integration of new neurons into functional neural networks. J Neurosci 26:12237-12241.
53. Schinder AF, Poo M (2000) The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23:639-645.
54. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429:184-187.
55. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.
56. Seress L, Pokorny J (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J Anat 133:181-195.
57. Shen K, Scheiffele P (2010) Genetics and cell biology of building specific synaptic connectivity. Annu Rev Neurosci 33:473-507.
58. Snyder JS, Kee N, Wojtowicz JM (2001) Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85:2423-2431.
59. Snyder JS, Radik R, Wojtowicz JM, Cameron HA (2009a) Anatomical gradients of adult neurogenesis and activity: young neurons in the ventral dentate gyrus are activated by water maze training. Hippocampus 19:360-370.
60. Snyder JS, Ramchand P, Rabbett S, Radik R, Wojtowicz JM, Cameron HA (2009b) Septo-temporal gradients of neurogenesis and activity in 13- month-old rats. Neurobiol Aging. Advance online publication. Retrieved May 4, 2011. doi:10.1016/j.neurobiolaging.2009.05.022.
61. Spitzer NC (2006) Electrical activity in early neuronal development. Nature 444:707-712.
62. Tashiro A, Sandler VM, Toni N, Zhao C, Gage FH (2006) NMDA-receptormediated, cell-specific integration of new neurons in adult dentate gyrus. Nature 442:929-933.
63. Tashiro A, Makino H, Gage FH (2007) Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 27:3252-3259.
64. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, Cusick A, Riley ZL, Sunkin SM, Bernard A, Puchalski RB, Gage FH, Jones AR, Bajic VB, Hawrylycz MJ, Lein ES (2008) Genomic anatomy of the hippocampus. Neuron 60:1010-1021.
65. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH (2007) Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10:727-734.
66. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901-907.
67. Treves A, Tashiro A, Witter ME, Moser EI (2008) What is the mammalian dentate gyrus good for? Neuroscience 154:1155-1172.
68. Trommald M, Hulleberg G (1997) Dimensions and density of dendritic spines from rat dentate granule cells based on reconstructions from serial electron micrographs. J Comp Neurol 377:15-28.
69. van Praag H, Kempermann G, Gage FH (1999) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
70. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
71. Vazdarjanova A, Ramirez-Amaya V, Insel N, Plummer TK, Rosi S, Chowdhury S, Mikhael D, Worley PF, Guzowski JF, Barnes CA (2006) Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain. J Comp Neurol 498:317-329.
72. Verwer RW, Meijer RJ, Van Uum HF, Witter MP (1997) Collateral projections from the rat hippocampal formation to the lateral and medial prefrontal cortex. Hippocampus 7:397-402.
73. Wang JW, David DJ, Monckton JE, Battaglia F, Hen R (2008) Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 28:1374-1384.
74. Wang S, Scott BW, Wojtowicz JM (2000) Heterogenous properties of dentate granule neurons in the adult rat. J Neurobiol 42:248-257.
75. Whishaw IQ, Vanderwolf CH (1973) Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behav Biol 8:461-484.
76. Zhao C, Teng EM, Summers RG Jr, Ming GL, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3-11.
77. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.
78. Zweifel LS, Kuruvilla R, Ginty DD (2005) Functions and mechanisms of retrograde neurotrophin signalling. Nat Rev Neurosci 6:615-625.