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Locally dynamic synaptic learning rules in pyramidal neuron dendrites

Abstract

Long-term potentiation (LTP) of synaptic transmission underlies aspects of learning and memory. LTP is input-specific at the level of individual synapses, but neural network models predict interactions between plasticity at nearby synapses. Here we show in mouse hippocampal pyramidal cells that LTP at individual synapses reduces the threshold for potentiation at neighbouring synapses. After input-specific LTP induction by two-photon glutamate uncaging or by synaptic stimulation, subthreshold stimuli, which by themselves were too weak to trigger LTP, caused robust LTP and spine enlargement at neighbouring spines. Furthermore, LTP induction broadened the presynaptic–postsynaptic spike interval for spike-timing-dependent LTP within a dendritic neighbourhood. The reduction in the threshold for LTP induction lasted 10 min and spread over 10 µm of dendrite. These local interactions between neighbouring synapses support clustered plasticity models of memory storage and could allow for the binding of behaviourally linked information on the same dendritic branch.

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Figure 1: Crosstalk with pairing-induced LTP.
Figure 2: Crosstalk in unperturbed neurons.
Figure 3: Crosstalk with synaptically induced plasticity.
Figure 4: Crosstalk with spike-timing-dependent LTP.
Figure 5: Spatial and temporal scales of crosstalk.
Figure 6: Signalling underlying crosstalk.

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Acknowledgements

We thank H. Zhong and R. Yasuda for discussions, T. O’Connor for programming assistance, K. H. Wang for destabilized EGFP DNA, and R. Malinow and J. Magee for comments on the manuscript. This work was supported by HHMI, by the NIH, and by a David and Fanny Luke Fellowship (C.D.H.).

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Correspondence to Karel Svoboda.

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Supplementary Information

This file contains Supplementary Notes on glutamate uncaging-evoked spine Ca2+ signals and glutamate-independent effects of uncaging and Supplementary Figures 1-4 with Legends. (PDF 2606 kb)

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Harvey, C., Svoboda, K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450, 1195–1200 (2007). https://doi.org/10.1038/nature06416

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