Metaplasticity at CA1 Synapses by Homeostatic Control of Presynaptic Release Dynamics

Cell Rep. 2017 Oct 31;21(5):1293-1303. doi: 10.1016/j.celrep.2017.10.025.

Abstract

Hebbian and homeostatic forms of plasticity operate on different timescales to regulate synaptic strength. The degree of mechanistic overlap between these processes and their mutual influence are still incompletely understood. Here, we report that homeostatic synaptic strengthening induced by prolonged network inactivity compromised the ability of CA1 synapses to exhibit LTP. This effect could not be accounted for by an obvious deficit in the postsynaptic capacity for LTP expression, since neither the fraction of silent synapses nor the ability to induce LTP by two-photon glutamate uncaging were reduced by the homeostatic process. Rather, optical quantal analysis reveals that homeostatically strengthened synapses display a reduced capacity to maintain glutamate release fidelity during repetitive stimulation, ultimately impeding the induction, and thus expression, of LTP. By regulating the short-term dynamics of glutamate release, the homeostatic process thus influences key aspects of dynamic network function and exhibits features of metaplasticity.

Keywords: LTP; homeostatic plasticity; iGluSNFR; metaplasticity; synapse.

MeSH terms

  • Animals
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / metabolism*
  • Female
  • Glutamic Acid / metabolism
  • In Vitro Techniques
  • Long-Term Potentiation / drug effects
  • Male
  • Microscopy, Fluorescence, Multiphoton
  • Neuronal Plasticity / physiology*
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, AMPA / metabolism
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Synaptic Potentials / drug effects
  • Tetrodotoxin / toxicity

Substances

  • Receptors, AMPA
  • Receptors, N-Methyl-D-Aspartate
  • Glutamic Acid
  • Tetrodotoxin