Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

被引:78
作者
Phan, Anna [1 ,2 ]
Suschkov, Sarah [1 ,2 ]
Molinaro, Luke [1 ,2 ]
Reynolds, Kathryn [1 ,2 ]
Lymer, Jennifer M. [1 ,2 ]
Bailey, Craig D. C. [2 ,3 ]
Kow, Lee-Ming [4 ]
MacLusky, Neil J. [2 ,3 ]
Pfaff, Donald W. [4 ]
Choleris, Elena [1 ,2 ]
机构
[1] Univ Guelph, Dept Psychol, Guelph, ON N1G 2W1, Canada
[2] Univ Guelph, Neurosci Program, Guelph, ON N1G 2W1, Canada
[3] Univ Guelph, Dept Biomed Sci, Guelph, ON N1G 2W1, Canada
[4] Rockefeller Univ, Lab Neurobiol & Behav, New York, NY 10065 USA
基金
加拿大自然科学与工程研究理事会; 加拿大创新基金会;
关键词
immature synapse; short-term memory; structural plasticity; synaptic plasticity; signal-to-noise ratio; LONG-TERM POTENTIATION; DENDRITIC SPINES; SYNAPTIC-TRANSMISSION; NEUROTROPHIC FACTOR; DORSAL HIPPOCAMPUS; FEMALE RATS; ESTRADIOL; BRAIN; PLASTICITY; RECEPTORS;
D O I
10.1073/pnas.1522150112
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Dramatic increases in hippocampal spine synapse density are known to occur within minutes of estrogen exposure. Until now, it has been assumed that enhanced spinogenesis increased excitatory input received by the CA1 pyramidal neurons, but how this facilitated learning and memory was unclear. Delivery of 17a-estradiol or an estrogen receptor (ER)-alpha (but not ER-beta) agonist into the dorsal hippocampus rapidly improved general discrimination learning in female mice. The same treatments increased CA1 dendritic spines in hippocampal sections over a time course consistent with the learning acquisition phase. Surprisingly, estrogen-activated spinogenesis was associated with a decrease in CA1 hippocampal excitatory input, rapidly and transiently reducing CA1 AMPA activity via a mechanism likely reflecting AMPA receptor internalization and creation of silent or immature synapses. We propose that estrogens promote hippocampally mediated learning via a mechanism resembling some of the broad features of normal development, an initial overproduction of functionally immature connections being subsequently pruned by experience.
引用
收藏
页码:16018 / 16023
页数:6
相关论文
共 34 条
  • [1] Impermanence of dendritic spines in live adult CA1 hippocampus
    Attardo, Alessio
    Fitzgerald, James E.
    Schnitzer, Mark J.
    [J]. NATURE, 2015, 523 (7562) : 592 - +
  • [2] A novel form of synaptic plasticity in field CA3 of hippocampus requires GPER1 activation and BDNF release
    Briz, Victor
    Liu, Yan
    Zhu, Guoqi
    Bi, Xiaoning
    Baudry, Michel
    [J]. JOURNAL OF CELL BIOLOGY, 2015, 210 (07) : 1225 - 1237
  • [3] Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain
    Cornil, CA
    Dalla, C
    Papadopoulou-Daifoti, Z
    Baillien, M
    Balthazart, J
    [J]. BEHAVIOURAL BRAIN RESEARCH, 2006, 166 (01) : 110 - 123
  • [4] Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze
    Dong, Zhifang
    Bai, Yanrui
    Wu, Xiaoyan
    Li, Hongjie
    Gong, Bo
    Howland, John G.
    Huang, Yan
    He, Wenting
    Li, Tingyu
    Wang, Yu Tian
    [J]. NEUROPHARMACOLOGY, 2013, 64 : 65 - 73
  • [5] Noise in the nervous system
    Faisal, A. Aldo
    Selen, Luc P. J.
    Wolpert, Daniel M.
    [J]. NATURE REVIEWS NEUROSCIENCE, 2008, 9 (04) : 292 - 303
  • [6] SOME OBSERVATIONS ON BIOLOGICAL NOISE
    FATT, P
    KATZ, B
    [J]. NATURE, 1950, 166 (4223) : 597 - 598
  • [7] Franklin K., 2001, MOUSE BRAIN STEREOTA
  • [8] Rapid effects of the G-protein coupled oestrogen receptor (GPER) on learning and dorsal hippocampus dendritic spines in female mice
    Gabor, Christopher
    Lymer, Jennifer
    Phan, Anna
    Choleris, Elena
    [J]. PHYSIOLOGY & BEHAVIOR, 2015, 149 : 53 - 60
  • [9] AMPA-silent synapses in brain development and pathology
    Hanse, Eric
    Seth, Henrik
    Riebe, Ilse
    [J]. NATURE REVIEWS NEUROSCIENCE, 2013, 14 (12) : 839 - 850
  • [10] BRAIN-DERIVED NEUROTROPHIC FACTOR-ESTROGEN INTERACTIONS IN THE HIPPOCAMPAL MOSSY FIBER PATHWAY: IMPLICATIONS FOR NORMAL BRAIN FUNCTION AND DISEASE
    Harte-Hargrove, L. C.
    Maclusky, N. J.
    Scharfman, H. E.
    [J]. NEUROSCIENCE, 2013, 239 : 46 - 66