Short-Term Plasticity at Hippocampal Mossy Fiber Synapses Is Induced by Natural Activity Patterns and Associated with Vesicle Pool Engram Formation

Neuron. 2020 Aug 5;107(3):509-521.e7. doi: 10.1016/j.neuron.2020.05.013. Epub 2020 Jun 2.


Post-tetanic potentiation (PTP) is an attractive candidate mechanism for hippocampus-dependent short-term memory. Although PTP has a uniquely large magnitude at hippocampal mossy fiber-CA3 pyramidal neuron synapses, it is unclear whether it can be induced by natural activity and whether its lifetime is sufficient to support short-term memory. We combined in vivo recordings from granule cells (GCs), in vitro paired recordings from mossy fiber terminals and postsynaptic CA3 neurons, and "flash and freeze" electron microscopy. PTP was induced at single synapses and showed a low induction threshold adapted to sparse GC activity in vivo. PTP was mainly generated by enlargement of the readily releasable pool of synaptic vesicles, allowing multiplicative interaction with other plasticity forms. PTP was associated with an increase in the docked vesicle pool, suggesting formation of structural "pool engrams." Absence of presynaptic activity extended the lifetime of the potentiation, enabling prolonged information storage in the hippocampal network.

Keywords: dentate gyrus granule cells; docked vesicle pool; electron microscopy; flash and freeze; hippocampal mossy fiber synapses; in vivo recording; post-tetanic potentiation; presynaptic and paired recording; readily releasable pool; superbursts.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • CA3 Region, Hippocampal / cytology
  • Dentate Gyrus / cytology
  • Memory, Short-Term / physiology*
  • Mice
  • Microscopy, Electron
  • Mossy Fibers, Hippocampal / metabolism*
  • Mossy Fibers, Hippocampal / physiology
  • Mossy Fibers, Hippocampal / ultrastructure
  • Neuronal Plasticity / physiology*
  • Patch-Clamp Techniques
  • Pyramidal Cells / metabolism*
  • Pyramidal Cells / physiology
  • Pyramidal Cells / ultrastructure
  • Rats
  • Synapses / metabolism*
  • Synapses / physiology
  • Synaptic Potentials / physiology
  • Synaptic Vesicles / metabolism*