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

Sylvain Rama, Mickaël Zbili, Andrzej Bialowas, Laure Fronzaroli-Molinieres, Norbert Ankri, Edmond Carlier, Vincenzo Marra and Dominique Debanne ()
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Sylvain Rama: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Mickaël Zbili: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Andrzej Bialowas: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Laure Fronzaroli-Molinieres: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Norbert Ankri: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Edmond Carlier: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Vincenzo Marra: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord
Dominique Debanne: INSERM, UMR_S 1072, Faculté de Médecine Secteur Nord

Nature Communications, 2015, vol. 6, issue 1, 1-12

Abstract: Abstract 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.

Date: 2015
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DOI: 10.1038/ncomms10163

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