Brief Subthreshold Events Can Act as Hebbian Signals for Long-Term Plasticity

Elodie Fino,Laurent Venance,Jean-Michel Deniau,Olivier Jacques Manzoni

doi:10.1371/journal.pone.0006557

Elodie Fino, Laurent Venance + Show 2 more

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https://doi.org/10.1371/journal.pone.0006557

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Journal: PloS one	Publication Date: Aug 7, 2009
Citations: 63	License type: CC BY 4.0

Affiliation: Inserm, Collège de France, Sorbonne Université

Abstract

BackgroundAction potentials are thought to be determinant for the induction of long-term synaptic plasticity, the cellular basis of learning and memory. However, neuronal activity does not lead systematically to an action potential but also, in many cases, to synaptic depolarizing subthreshold events. This is particularly exemplified in corticostriatal information processing. Indeed, the striatum integrates information from the whole cerebral cortex and, due to the membrane properties of striatal medium spiny neurons, cortical inputs do not systematically trigger an action potential but a wide range of subthreshold postsynaptic depolarizations. Accordingly, we have addressed the following question: does a brief subthreshold event act as a Hebbian signal and induce long-term synaptic efficacy changes?Methodology/Principal FindingsHere, using perforated patch-clamp recordings on rat brain corticostriatal slices, we demonstrate, that brief (30 ms) subthreshold depolarizing events in quasi-coincidence with presynaptic activity can act as Hebbian signals and are sufficient to induce long-term synaptic plasticity at corticostriatal synapses. This “subthreshold-depolarization dependent plasticity” (SDDP) induces strong, significant and bidirectional long-term synaptic efficacy changes at a very high occurrence (81%) for time intervals between pre- and postsynaptic stimulations (Δt) of −110<Δt<+110 ms. Such subthreshold depolarizations are able to induce robust long-term depression (cannabinoid type-1 receptor-activation dependent) as well as long-term potentiation (NMDA receptor-activation dependent).Conclusion/SignificanceOur data show the existence of a robust, reliable and timing-dependent bidirectional long-term plasticity induced by brief subthreshold events paired with presynaptic activity. The existence of a subthreshold-depolarization dependent plasticity extends considerably, beyond the action potential, the neuron's capabilities to express long-term synaptic efficacy changes.

Highlights

Learning and memory are thought to involve long-term synaptic efficacy changes [1,2,3]
The key role of the action potential is exemplified by spike-timing dependent plasticity (STDP), in which the timing between pre- and postsynaptic action potentials rules the induction of long-term synaptic efficacy changes [4,5,6,7,8]
Depending on the Dt, we observed the induction of subthresholddepolarization long-term depression (sdLTD) or subthresholddepolarization long-term potentiation (sdLTP) for post-pre sequences, depending on the medium-sized spiny neurons (MSNs) state of excitability, whereas pre-post sequences induced mainly sdLTD

Summary

Introduction

Learning and memory are thought to involve long-term synaptic efficacy changes [1,2,3]. We have tested here the effect of brief postsynaptic subthreshold depolarizations on the induction of long-term synaptic plasticity and their ability to act as Hebbian signals. Action potentials are thought to be determinant for the induction of long-term synaptic plasticity, the cellular basis of learning and memory. Neuronal activity does not lead systematically to an action potential and, in many cases, to synaptic depolarizing subthreshold events. This is exemplified in corticostriatal information processing. We have addressed the following question: does a brief subthreshold event act as a Hebbian signal and induce long-term synaptic efficacy changes?

Methods

Results

Conclusion