Abstract

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.

Highlights

  • The strength of a synapse in relation to action potential threshold is a key factor that defines its role in neuronal information processing

  • Single mossy fiber terminals were stimulated in the tight-seal, bouton-attached configuration (Figure 1A–C), while postsynaptic CA3 pyramidal neurons were simultaneously recorded in the whole-cell configuration at near-physiological temperature (31–34 ̊C)

  • Single unitary excitatory postsynaptic potentials (EPSPs) had a mean latency of 1.06 ± 0.09 ms, a peak amplitude of 9.6 ± 2.4 mV, a 20–80% rise time of 3.6 ± 0.7 ms, and a decay time constant of 134 ± 10 ms (6–8 pairs; Figure 1E–I)

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Summary

Introduction

The strength of a synapse in relation to action potential threshold is a key factor that defines its role in neuronal information processing. In neocortical and hippocampal circuits, it is generally thought that individual synapses are weak, and that temporal or spatial summation of unitary excitatory postsynaptic potentials (EPSPs) is required to reach the firing threshold (London and Hausser, 2005). Whether detonator synapses exist in higher brain regions is presently unclear. Resolving this question has important implications for understanding the nature of information encoding and the rules of synaptic computation (Koch and Segev, 2000; London and Hausser, 2005; Silver, 2010). In a network with strong synapses near detonation, activity of a single connected presynaptic neuron may be sufficient to drive a postsynaptic cell and to initiate a behaviorally relevant output (Brecht et al, 2004)

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