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

Summary

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.

Graphical Abstract

Highlights

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  Natural activity patterns in hippocampal GCs in vivo induce PTP at mossy fiber synapses

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  PTP is primarily caused by an increase in the readily releasable vesicle pool

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  PTP is associated with an increase in the number of docked vesicles at active zones

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  Sparse activity extends pool engram lifetime, increasing overlap with short-term memory

Abstract

Vandael et al. report that natural activity patterns induce post-tetanic potentiation (PTP) at hippocampal mossy fiber synapses. PTP is primarily caused by an increase in the readily releasable vesicle pool. PTP is associated with an increase in the docked vesicle pool, revealing a structural correlate of presynaptic plasticity.