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Presynaptic hyperpolarization induces a fast analogue modulation of spike-evoked transmission mediated by axonal sodium channels

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posted on 22.02.2019, 10:36 by S Rama, M Zbili, A Bialowas, L Fronzaroli-Molinieres, N Ankri, E Carlier, V Marra, D Debanne
In the mammalian brain, synaptic transmission usually depends on presynaptic action potentials (APs) in an all-or-none (or digital) manner. Recent studies suggest, however, that subthreshold depolarization in the presynaptic cell facilitates spike-evoked transmission, thus creating an analogue modulation of a digital process (or analogue–digital (AD) modulation). At most synapses, this process is slow and not ideally suited for the fast dynamics of neural networks. We show here that transmission at CA3–CA3 and L5–L5 synapses can be enhanced by brief presynaptic hyperpolarization such as an inhibitory postsynaptic potential (IPSP). Using dual soma–axon patch recordings and live imaging, we find that this hyperpolarization-induced AD facilitation (h-ADF) is due to the recovery from inactivation of Nav channels controlling AP amplitude in the axon. Incorporated in a network model, h-ADF promotes both pyramidal cell synchrony and gamma oscillations. In conclusion, cortical excitatory synapses in local circuits display hyperpolarization-induced facilitation of spike-evoked synaptic transmission that promotes network synchrony.

Funding

This study was supported by the Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Agence Nationale de la Recherche (ANR Blanc ‘REPREK’—11-BSV4-016-01 and ANR Santé & Bien-Etre ‘AXODE’—14-CE13-0003-02), Fondation pour la Recherche Médicale (doctoral grant FDT-2011-0922774 to A.B., postdoctoral grant SPF-2011-1223409 to V.M. and grant DSV-2013-1228768 to D.D.), the Ecole Normale Supérieure (doctoral grant to M.Z.) and the French Ministry of Research (doctoral grant to A.B.).

History

Citation

Nature Communications, 2015, 6, Article number: 10163

Author affiliation

/Organisation/COLLEGE OF LIFE SCIENCES/Biological Sciences/Neuroscience, Psychology and Behaviour

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VoR (Version of Record)

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Nature Communications

Publisher

Nature Research

eissn

2041-1723

Acceptance date

11/11/2015

Copyright date

2015

Available date

22/02/2019

Publisher version

https://www.nature.com/articles/ncomms10163

Language

en

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