Synaptic Transmission Optimization Predicts Expression Loci of Long-Term Plasticity

Rui Ponte Costa, Zahid Padamsey, James A D'Amour, Nigel J Emptage, Robert C Froemke, Tim P Vogels

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Abstract

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 languageEnglish
Pages (from-to)177-189.e7
Number of pages21
JournalNeuron
Volume96
Issue number1
Early online date27 Sep 2017
DOIs
Publication statusPublished - 27 Sep 2017

Keywords

  • Animals
  • Hippocampus/physiology
  • Long-Term Potentiation/physiology
  • Long-Term Synaptic Depression/physiology
  • Models, Neurological
  • Neocortex/physiology
  • Neural Inhibition/physiology
  • Neuronal Plasticity/physiology
  • Synaptic Transmission/physiology

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    Costa, R. P., Padamsey, Z., D'Amour, J. A., Emptage, N. J., Froemke, R. C., & Vogels, T. P. (2017). Synaptic Transmission Optimization Predicts Expression Loci of Long-Term Plasticity. Neuron, 96(1), 177-189.e7. https://doi.org/10.1016/j.neuron.2017.09.021