Synaptic Transmission Optimization Predicts Expression Loci of Long-Term Plasticity

Neuron. 2017 Sep 27;96(1):177-189.e7. doi: 10.1016/j.neuron.2017.09.021.


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.

Keywords: endocannabinoids; excitation-inhibition balance; expression loci; inhibitory plasticity; long-term synaptic plasticity; nitric oxide; retrograde messengers; synaptic transmission; theory.

MeSH terms

  • 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*