Experience-specific functional modification of the dentate gyrus through adult neurogenesis: A critical period during an immature stage

被引:387
作者
Tashiro, Ayumu [1 ]
Makino, Hiroshi [1 ]
Gage, Fred H. [1 ]
机构
[1] Salk Inst Biol Studies, Genet Lab, La Jolla, CA 92037 USA
关键词
enriched environment; c-fos; zif268; immediate early gene; dentate gyrus; hippocampus; memory; neurogenesis;
D O I
10.1523/JNEUROSCI.4941-06.2007
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Neural circuits in the dentate gyrus are continuously modified by adult neurogenesis, whose level is affected by the animal's experience. However, it is not known whether this experience-dependent anatomical modification alters the functional properties of the dentate gyrus. Here, using the expression of immediate early gene products, c-fos and Zif268, as indicators of recently activated neurons, we show that previous exposure to an enriched environment increases the total number of new neurons and the number of new neurons responding to reexposure to the same environment. The increase in the density of activated new neurons occurred specifically in response to exposure to the same environment but not to a different experience. Furthermore, we found that these experience-specific modifications are affected exclusively by previous exposure around the second week after neuronal birth but not later than 3 weeks. Thus, the animal's experience within a critical period during an immature stage of new neurons determines the survival and population response of the new neurons and may affect later neural representation of the experience in the dentate gyrus. This experience-specific functional modification through adult neurogenesis could be a mechanism by which new neurons exert a long-term influence on the function of the dentate gyrus related to learning and memory.
引用
收藏
页码:3252 / 3259
页数:8
相关论文
共 38 条
[1]   Potential role for adult neurogenesis in the encoding of time in new memories [J].
Aimone, James B. ;
Wiles, Janet ;
Gage, Fred H. .
NATURE NEUROSCIENCE, 2006, 9 (06) :723-727
[2]   New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment [J].
Bruel-Jungerman, E ;
Laroche, S ;
Rampon, C .
EUROPEAN JOURNAL OF NEUROSCIENCE, 2005, 21 (02) :513-521
[3]   RAPID INCREASE OF AN IMMEDIATE EARLY GENE MESSENGER-RNA IN HIPPOCAMPAL-NEURONS BY SYNAPTIC NMDA RECEPTOR ACTIVATION [J].
COLE, AJ ;
SAFFEN, DW ;
BARABAN, JM ;
WORLEY, PF .
NATURE, 1989, 340 (6233) :474-476
[4]   Short-term and long-term survival of new neurons in the rat dentate gyrus [J].
Dayer, AG ;
Ford, AA ;
Cleaver, KM ;
Yassaee, M ;
Cameron, HA .
JOURNAL OF COMPARATIVE NEUROLOGY, 2003, 460 (04) :563-572
[5]  
Fleischmann A, 2003, J NEUROSCI, V23, P9116
[6]   Mammalian neural stem cells [J].
Gage, FH .
SCIENCE, 2000, 287 (5457) :1433-1438
[7]   Learning enhances adult neurogenesis in the hippocampal formation [J].
Gould, E ;
Beylin, A ;
Tanapat, P ;
Reeves, A ;
Shors, TJ .
NATURE NEUROSCIENCE, 1999, 2 (03) :260-265
[8]   Neurogenesis in adult mammals: Some progress and problems [J].
Gould, E ;
Gross, CG .
JOURNAL OF NEUROSCIENCE, 2002, 22 (03) :619-623
[9]   New neurons in old brains: learning to survive? [J].
Greenough, WT ;
Cohen, NJ ;
Juraska, JM .
NATURE NEUROSCIENCE, 1999, 2 (03) :203-205
[10]   Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes Arc, c-fos, and zif268 [J].
Guzowski, JF ;
Setlow, B ;
Wagner, EK ;
McGaugh, JL .
JOURNAL OF NEUROSCIENCE, 2001, 21 (14) :5089-5098