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Stably maintained dendritic spines are associated with lifelong memories

Nature volume 462, pages 920–924 (2009)Cite this article

Abstract

Changes in synaptic connections are considered essential for learning and memory formation1,2,3,4,5,6. However, it is unknown how neural circuits undergo continuous synaptic changes during learning while maintaining lifelong memories. Here we show, by following postsynaptic dendritic spines over time in the mouse cortex7,8, that learning and novel sensory experience lead to spine formation and elimination by a protracted process. The extent of spine remodelling correlates with behavioural improvement after learning, suggesting a crucial role of synaptic structural plasticity in memory formation. Importantly, a small fraction of new spines induced by novel experience, together with most spines formed early during development and surviving experience-dependent elimination, are preserved and provide a structural basis for memory retention throughout the entire life of an animal. These studies indicate that learning and daily sensory experience leave minute but permanent marks on cortical connections and suggest that lifelong memories are stored in largely stably connected synaptic networks.

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Figure 1: Motor learning and novel sensory experience promote rapid dendritic spine formation.
Figure 2: A fraction of newly formed spines persists over weeks and correlates with performance after learning.
Figure 3: Novel experience promotes spine elimination.
Figure 4: Maintenance of daily formed new spines and spines formed during early development throughout life.
Figure 5: Spine maintenance in different cell types and cortical layers.

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Acknowledgements

This work was supported by National Institutes of Health R01 NS047325 and a Dart Foundation Fellowship to W.-B.G. and by an Ellison/AFAR Postdoctoral Fellowship to G.Y. We thank members of the Gan laboratory for their comments.

Author Contributions G.Y. and W.-B.G. conceived the experiments. G.Y. performed and analysed most experiments on motor cortex and all the experiments on barrel cortex. F.P. conducted and analysed some of the experiments on motor cortex. G.Y. and W.-B.G. performed the data fitting. W.-B.G. wrote the manuscript.

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Authors and Affiliations

  1. Department of Physiology and Neuroscience, Molecular Neurobiology Program, The Helen and Martin Kimmel Center for Biology and Medicine at the Skirball Institute of Biomolecular Medicine, New York University School of Medicine, New York, New York 10016, USA,

    Guang Yang, Feng Pan & Wen-Biao Gan

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  1. Guang Yang
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  2. Feng Pan
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  3. Wen-Biao Gan
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Corresponding author

Correspondence to Wen-Biao Gan.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-7 with Legends, Supplementary Tables a and b, Supplementary Data, a Supplementary Discussion and Supplementary References. (PDF 539 kb)

Supplementary Movie 1

This movie file shows mice in Cage 1 which is a bead-string hanging enriched cage in which 200 strings of plastic beads were evenly hung from the top of the cage grid. The mice need to navigate through the bead-strings to get access to food and water. (MOV 8759 kb)

Supplementary Movie 2

This movie file shows mice in Cage 2 which is a bead-string hanging enriched cage in which 200 strings of plastic beads were evenly hung from the top of the cage grid. The mice need to navigate through the bead-strings to get access to food and water. (MOV 9169 kb)

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Yang, G., Pan, F. & Gan, WB. Stably maintained dendritic spines are associated with lifelong memories . Nature 462, 920–924 (2009). https://doi.org/10.1038/nature08577

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