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Structural basis of long-term potentiation in single dendritic spines

Author

Listed:
  • Masanori Matsuzaki

    (National Institute for Physiological Sciences and The Graduate University of Advanced Studies (Sokendai))

  • Naoki Honkura

    (National Institute for Physiological Sciences and The Graduate University of Advanced Studies (Sokendai))

  • Graham C. R. Ellis-Davies

    (Drexel University College of Medicine)

  • Haruo Kasai

    (National Institute for Physiological Sciences and The Graduate University of Advanced Studies (Sokendai))

Abstract

Dendritic spines of pyramidal neurons in the cerebral cortex undergo activity-dependent structural remodelling1,2,3,4,5 that has been proposed to be a cellular basis of learning and memory6. How structural remodelling supports synaptic plasticity4,5, such as long-term potentiation7, and whether such plasticity is input-specific at the level of the individual spine has remained unknown. We investigated the structural basis of long-term potentiation using two-photon photolysis of caged glutamate at single spines of hippocampal CA1 pyramidal neurons8. Here we show that repetitive quantum-like photorelease (uncaging) of glutamate induces a rapid and selective enlargement of stimulated spines that is transient in large mushroom spines but persistent in small spines. Spine enlargement is associated with an increase in AMPA-receptor-mediated currents at the stimulated synapse and is dependent on NMDA receptors, calmodulin and actin polymerization. Long-lasting spine enlargement also requires Ca2+/calmodulin-dependent protein kinase II. Our results thus indicate that spines individually follow Hebb's postulate for learning. They further suggest that small spines are preferential sites for long-term potentiation induction, whereas large spines might represent physical traces of long-term memory.

Suggested Citation

  • Masanori Matsuzaki & Naoki Honkura & Graham C. R. Ellis-Davies & Haruo Kasai, 2004. "Structural basis of long-term potentiation in single dendritic spines," Nature, Nature, vol. 429(6993), pages 761-766, June.
    • Handle: RePEc:nat:nature:v:429:y:2004:i:6993:d:10.1038_nature02617
    DOI: 10.1038/nature02617
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    Cited by:

    1. Sergio Luengo-Sanchez & Isabel Fernaud-Espinosa & Concha Bielza & Ruth Benavides-Piccione & Pedro Larrañaga & Javier DeFelipe, 2018. "3D morphology-based clustering and simulation of human pyramidal cell dendritic spines," PLOS Computational Biology, Public Library of Science, vol. 14(6), pages 1-22, June.
    2. Min Lee & Hyungseok C. Moon & Hyeonjeong Jeong & Dong Wook Kim & Hye Yoon Park & Yongdae Shin, 2024. "Optogenetic control of mRNA condensation reveals an intimate link between condensate material properties and functions," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Roberto Ogelman & Luis E. Gomez Wulschner & Victoria M. Hoelscher & In-Wook Hwang & Victoria N. Chang & Won Chan Oh, 2024. "Serotonin modulates excitatory synapse maturation in the developing prefrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Michael Fauth & Florentin Wörgötter & Christian Tetzlaff, 2015. "The Formation of Multi-synaptic Connections by the Interaction of Synaptic and Structural Plasticity and Their Functional Consequences," PLOS Computational Biology, Public Library of Science, vol. 11(1), pages 1-29, January.
    5. Daria Antonenko & Anna Elisabeth Fromm & Friederike Thams & Ulrike Grittner & Marcus Meinzer & Agnes Flöel, 2023. "Microstructural and functional plasticity following repeated brain stimulation during cognitive training in older adults," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. María del Carmen Rodríguez-Martínez & Alba De la Plana Maestre & Juan Antonio Armenta-Peinado & Miguel Ángel Barbancho & Natalia García-Casares, 2021. "Evidence of Animal-Assisted Therapy in Neurological Diseases in Adults: A Systematic Review," IJERPH, MDPI, vol. 18(24), pages 1-17, December.
    7. Hiromu Takizawa & Noriko Hiroi & Akira Funahashi, 2012. "Mathematical Modeling of Sustainable Synaptogenesis by Repetitive Stimuli Suggests Signaling Mechanisms In Vivo," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-22, December.
    8. David M Santucci & Sridhar Raghavachari, 2008. "The Effects of NR2 Subunit-Dependent NMDA Receptor Kinetics on Synaptic Transmission and CaMKII Activation," PLOS Computational Biology, Public Library of Science, vol. 4(10), pages 1-16, October.
    9. Moritz Deger & Moritz Helias & Stefan Rotter & Markus Diesmann, 2012. "Spike-Timing Dependence of Structural Plasticity Explains Cooperative Synapse Formation in the Neocortex," PLOS Computational Biology, Public Library of Science, vol. 8(9), pages 1-13, September.
    10. Ojasee Bapat & Tejas Purimetla & Sarah Kruessel & Monil Shah & Ruolin Fan & Christina Thum & Fiona Rupprecht & Julian D. Langer & Vidhya Rangaraju, 2024. "VAP spatially stabilizes dendritic mitochondria to locally support synaptic plasticity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Isabel Espadas & Jenna L. Wingfield & Yoshihisa Nakahata & Kaushik Chanda & Eddie Grinman & Ilika Ghosh & Karl E. Bauer & Bindu Raveendra & Michael A. Kiebler & Ryohei Yasuda & Vidhya Rangaraju & Sath, 2024. "Synaptically-targeted long non-coding RNA SLAMR promotes structural plasticity by increasing translation and CaMKII activity," Nature Communications, Nature, vol. 15(1), pages 1-24, December.

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