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.

Mossy fiber synapses on CA3 pyramidal cells are 'conditional detonators' that reliably discharge postsynaptic targets. The 'conditional' nature implies that burst activity in dentate gyrus granule cells is required for detonation. Whether single unitary excitatory postsynaptic potentials (EPSPs) trigger spikes in CA3 neurons remains unknown. Mossy fiber synapses exhibit both pronounced short-term facilitation and uniquely large post-tetanic potentiation (PTP). We tested whether PTP could convert mossy fiber synapses from subdetonator into detonator mode, using a recently developed method to selectively and noninvasively stimulate individual presynaptic terminals in rat brain slices. Unitary EPSPs failed to initiate a spike in CA3 neurons under control conditions, but reliably discharged them after induction of presynaptic short-term plasticity. Remarkably, PTP switched mossy fiber synapses into full detonators for tens of seconds. Plasticity-dependent detonation may be critical for efficient coding, storage, and recall of information in the granule cell–CA3 cell network.DOI: http://dx.doi.org/10.7554/eLife.17977.001

Summary Unipolar brush cells (UBCs) of the dorsal cochlear nucleus (DCN) and vestibular cerebellar cortex receive glutamatergic mossy fiber input on an elaborate brush-like dendrite. Two subtypes of UBC have been established based on immunohistochemical markers and physiological profiles, but the relation of these subtypes to the response to mossy fiber input is not clear. We examined the synaptic physiology of auditory UBCs in mouse brain slices, identifying two response profiles and correlated each with a specific UBC subtype. One subtype had a striking biphasic excitatory response mediated by AMPAR and mGluR1α. The second was mGluR1α negative and was dominated by a strongly inhibitory outward K+ current. These two subtypes up-or downregulated spontaneous firing, respectively. By analogy to the retina, we propose that UBCs comprise ON and OFF cells with respect to their response to glutamatergic input, and may therefore provide distinct parallel processing of multisensory input to their targets.

Highlights d Functional EM may be applied to acute brain slices and organotypic slice cultures d Docked vesicle pool and RRP are overlapping d Smaller-diameter vesicles have higher release probability than larger vesicles d Endocytic pits after moderate stimulation suggest fast endocytosis