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Long-term modifications of neuronal connections are critical for reliable memory storage in the brain. However, their locus of expression-pre- or postsynaptic-is highly variable. Here we introduce a theoretical framework in which long-term plasticity performs an optimization of the postsynaptic response statistics toward a given mean with minimal variance. Consequently, the state of the synapse at the time of plasticity induction determines the ratio of pre- and postsynaptic modifications. Our theory explains the experimentally observed expression loci of the hippocampal and neocortical synaptic potentiation studies we examined. Moreover, the theory predicts presynaptic expression of long-term depression, consistent with experimental observations. At inhibitory synapses, the theory suggests a statistically efficient excitatory-inhibitory balance in which changes in inhibitory postsynaptic response statistics specifically target the mean excitation. Our results provide a unifying theory for understanding the expression mechanisms and functions of long-term synaptic transmission plasticity.

Original publication

DOI

10.1016/j.neuron.2017.09.021

Type

Journal article

Journal

Neuron

Publication Date

27/09/2017

Volume

96

Pages

177 - 189.e7

Keywords

endocannabinoids, excitation-inhibition balance, expression loci, inhibitory plasticity, long-term synaptic plasticity, nitric oxide, retrograde messengers, synaptic transmission, theory, Animals, Hippocampus, Long-Term Potentiation, Long-Term Synaptic Depression, Models, Neurological, Neocortex, Neural Inhibition, Neuronal Plasticity, Synaptic Transmission