Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus

被引:165
作者
Bagot, Rosemary C. [1 ,2 ]
van Hasselt, Felisa N. [2 ]
Champagne, Danielle L. [3 ]
Meaney, Michael J. [1 ]
Krugers, Harm J. [2 ]
Joels, Marian [2 ]
机构
[1] McGill Univ, Douglas Mental Hlth Univ Inst, Verdun, PQ H4H 1R3, Canada
[2] Univ Amsterdam, SILS CNS, Amsterdam, Netherlands
[3] Leiden Univ, Med Ctr, LACDR, Leiden, Netherlands
关键词
Synaptic plasticity; Hippocampus; Maternal care; Stress; Contextual fear learning; LONG-TERM POTENTIATION; GLUCOCORTICOID-RECEPTOR ACTIVATION; INDIVIDUAL-DIFFERENCES; PYRAMIDAL NEURONS; GENE-EXPRESSION; SPATIAL MEMORY; CORTICOSTERONE; FEAR; AMYGDALA; RESPONSES;
D O I
10.1016/j.nlm.2009.03.004
中图分类号
B84 [心理学]; C [社会科学总论]; Q98 [人类学];
学科分类号
03 ; 0303 ; 030303 ; 04 ; 0402 ;
摘要
Maternal care in the rat influences hippocampal development, synaptic plasticity and cognition. Previous studies, however, have examined animals under minimally stressful conditions. Here we tested the hypothesis that maternal care influences hippocampal function differently when this structure is exposed to corticosteroid and noradrenergic hormones, which are elevated during the early phase of a stress response. In the adult male offspring of Long-Evans dams characterised as high or low in maternal care (high LG and low LG) we (1) examined basal dendritic morphology in the dentate gyrus by Golgi staining; (2) investigated rapid modulation of in vitro long term-potentiation (LTP) in the dentate gyrus by glucocorticoid and beta-adrenergic stimulation; (3) examined hippocampal and amygdala-dependent learning under stress using contextual and cued fear conditioning. We found differences in hippocampal dentate gyrus morphology in adult offspring of high and low LG mothers, with less dendritic complexity in low LG offspring. Under basal conditions LTP was lower in slices from low compared with high LG offspring. Hippocampal LTP was rapidly increased by either corticosterone (100 nM) or isoproterenol (1.0 mu M) in low LG offspring, suggesting improved dentate plasticity during stress. This was mirrored in hippocampal but not amygdala-dependent learning, as low LG offspring showed enhanced contextual but not cued fear conditioning. We suggest that decreased pup LG during postnatal life may be adaptive in high-threat environments, potentially enhancing hippocampal function in the offspring under conditions of adversity. (C) 2009 Elsevier Inc. All rights reserved.
引用
收藏
页码:292 / 300
页数:9
相关论文
共 66 条
[1]   Metaplasticity: tuning synapses and networks for plasticity [J].
Abraham, Wickliffe C. .
NATURE REVIEWS NEUROSCIENCE, 2008, 9 (05) :387-399
[2]   A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress [J].
Akirav, I ;
Kozenicky, M ;
Tal, D ;
Sandi, C ;
Venero, C ;
Richter-Levin, G .
LEARNING & MEMORY, 2004, 11 (02) :188-195
[3]   Opposite effects of glucocorticoid receptor activation on hippocampal CA1 dendritic complexity in chronically stressed and handled animals [J].
Alfarez, D. N. ;
Karst, H. ;
Velzing, E. H. ;
Joels, M. ;
Krugers, H. J. .
HIPPOCAMPUS, 2008, 18 (01) :20-28
[4]  
[Anonymous], NATURE, DOI DOI 10.1038/361031A0.[
[5]   Contribution of sex differences in the acute stress response to sex differences in water maze performance in the rat [J].
Beiko, J ;
Lander, R ;
Hampson, E ;
Boon, F ;
Cain, DP .
BEHAVIOURAL BRAIN RESEARCH, 2004, 151 (1-2) :239-253
[6]   CROUCHING AS AN INDEX OF FEAR [J].
BLANCHARD, RJ ;
BLANCHARD, DC .
JOURNAL OF COMPARATIVE AND PHYSIOLOGICAL PSYCHOLOGY, 1969, 67 (03) :370-+
[7]   Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy [J].
Boekhoorn, K ;
Terwel, D ;
Biemans, B ;
Borghgraef, P ;
Wiegert, O ;
Ramakers, GJA ;
de Vos, K ;
Krugers, H ;
Tomiyama, T ;
Mori, H ;
Joels, M ;
van Leuven, F ;
Lucassen, PJ .
JOURNAL OF NEUROSCIENCE, 2006, 26 (13) :3514-3523
[8]  
Borde M, 2000, HIPPOCAMPUS, V10, P198
[9]   Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression [J].
Bredy, TW ;
Zhang, TY ;
Grant, RJ ;
Diorio, J ;
Meaney, MJ .
EUROPEAN JOURNAL OF NEUROSCIENCE, 2004, 20 (05) :1355-1362
[10]   Partial reversal of the effect of maternal care on cognitive function through environmental enrichment [J].
Bredy, TW ;
Humpartzoomian, RA ;
Cain, DP ;
Meaney, MJ .
NEUROSCIENCE, 2003, 118 (02) :571-576