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Behavioral time scale synaptic plasticity underlies CA1 place fields

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Science  08 Sep 2017:
Vol. 357, Issue 6355, pp. 1033-1036
DOI: 10.1126/science.aan3846

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A different form of synaptic plasticity

How do synaptic or other neuronal changes support learning? This subject has been dominated by Hebb's postulate of synaptic change. Although there is strong experimental support for Hebbian plasticity in a number of preparations, alternative ideas have also been developed over the years. Bittner et al. provide in vivo, in vitro, and modeling data to support the view that non-Hebbian plasticity may underlie the formation of hippocampal place fields (see the Perspective by Krupic). Instead of multiple pairings, a single strong Ca2+ plateau potential in neuronal dendrites paired with spatial inputs may be sufficient to produce place cells.

Science, this issue p. 1033; see also p. 974

Abstract

Learning is primarily mediated by activity-dependent modifications of synaptic strength within neuronal circuits. We discovered that place fields in hippocampal area CA1 are produced by a synaptic potentiation notably different from Hebbian plasticity. Place fields could be produced in vivo in a single trial by potentiation of input that arrived seconds before and after complex spiking. The potentiated synaptic input was not initially coincident with action potentials or depolarization. This rule, named behavioral time scale synaptic plasticity, abruptly modifies inputs that were neither causal nor close in time to postsynaptic activation. In slices, five pairings of subthreshold presynaptic activity and calcium (Ca2+) plateau potentials produced a large potentiation with an asymmetric seconds-long time course. This plasticity efficiently stores entire behavioral sequences within synaptic weights to produce predictive place cell activity.

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