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Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain

Author

Listed:
  • Yann Humeau

    (Friedrich Miescher Institute)

  • Hamdy Shaban

    (Friedrich Miescher Institute)

  • Stephanie Bissière

    (Friedrich Miescher Institute)

  • Andreas Lüthi

    (Friedrich Miescher Institute
    University of Basel)

Abstract

The induction of associative synaptic plasticity in the mammalian central nervous system classically depends on coincident presynaptic and postsynaptic activity1,2. According to this principle, associative homosynaptic long-term potentiation (LTP) of excitatory synaptic transmission can be induced only if synaptic release occurs during postsynaptic depolarization1,2. In contrast, heterosynaptic plasticity in mammals is considered to rely on activity-independent, non-associative processes3,4,5,6,7,8. Here we describe a novel mechanism underlying the induction of associative LTP in the lateral amygdala (LA). Simultaneous activation of converging cortical and thalamic afferents specifically induced associative, N-methyl-d-aspartate (NMDA)-receptor-dependent LTP at cortical, but not at thalamic, inputs. Surprisingly, the induction of associative LTP at cortical inputs was completely independent of postsynaptic activity, including depolarization, postsynaptic NMDA receptor activation or an increase in postsynaptic Ca2+ concentration, and did not require network activity. LTP expression was mediated by a persistent increase in the presynaptic probability of release at cortical afferents. Our study shows the presynaptic induction and expression of heterosynaptic and associative synaptic plasticity on simultaneous activity of converging afferents. Our data indicate that input specificity of associative LTP can be determined exclusively by presynaptic properties.

Suggested Citation

  • Yann Humeau & Hamdy Shaban & Stephanie Bissière & Andreas Lüthi, 2003. "Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain," Nature, Nature, vol. 426(6968), pages 841-845, December.
  • Handle: RePEc:nat:nature:v:426:y:2003:i:6968:d:10.1038_nature02194
    DOI: 10.1038/nature02194
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    Cited by:

    1. Rou-Gang Xie & Wen-Guang Chu & Da-Lu Liu & Xu Wang & Sui-Bin Ma & Fei Wang & Fu-Dong Wang & Zhen Lin & Wen-Bin Wu & Na Lu & Ying-Ying Liu & Wen-Juan Han & Hui Zhang & Zhan-Tao Bai & San-Jue Hu & Hui-R, 2022. "Presynaptic NMDARs on spinal nociceptor terminals state-dependently modulate synaptic transmission and pain," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    2. Madeleine R. Wilcox & Aparna Nigam & Nathan G. Glasgow & Chamali Narangoda & Matthew B. Phillips & Dhilon S. Patel & Samaneh Mesbahi-Vasey & Andreea L. Turcu & Santiago Vázquez & Maria G. Kurnikova & , 2022. "Inhibition of NMDA receptors through a membrane-to-channel path," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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