Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation

Neuronal timing with millisecond precision is critical for many brain functions such as sensory perception, learning and memory formation. At the level of the chemical synapse, the synaptic delay is determined by the presynaptic release probability (<i>Pr</i>) and the waveform of the pre...

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Main Authors: Sami Boudkkazi, Dominique Debanne
Format: Article
Language:English
Published: MDPI AG 2024-03-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/13/7/573
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author Sami Boudkkazi
Dominique Debanne
author_facet Sami Boudkkazi
Dominique Debanne
author_sort Sami Boudkkazi
collection DOAJ
description Neuronal timing with millisecond precision is critical for many brain functions such as sensory perception, learning and memory formation. At the level of the chemical synapse, the synaptic delay is determined by the presynaptic release probability (<i>Pr</i>) and the waveform of the presynaptic action potential (AP). For instance, paired-pulse facilitation or presynaptic long-term potentiation are associated with reductions in the synaptic delay, whereas paired-pulse depression or presynaptic long-term depression are associated with an increased synaptic delay. Parallelly, the AP broadening that results from the inactivation of voltage gated potassium (Kv) channels responsible for the repolarization phase of the AP delays the synaptic response, and the inactivation of sodium (Nav) channels by voltage reduces the synaptic latency. However, whether synaptic delay is modulated during depolarization-induced analogue–digital facilitation (d-ADF), a form of context-dependent synaptic facilitation induced by prolonged depolarization of the presynaptic neuron and mediated by the voltage-inactivation of presynaptic Kv1 channels, remains unclear. We show here that despite <i>Pr</i> being elevated during d-ADF at pyramidal L5-L5 cell synapses, the synaptic delay is surprisingly unchanged. This finding suggests that both <i>Pr</i>- and AP-dependent changes in synaptic delay compensate for each other during d-ADF. We conclude that, in contrast to other short- or long-term modulations of presynaptic release, synaptic timing is not affected during d-ADF because of the opposite interaction of <i>Pr</i>- and AP-dependent modulations of synaptic delay.
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spelling doaj.art-1898d2c5394e46f1a8c7a7db39f0af302024-04-12T13:16:25ZengMDPI AGCells2073-44092024-03-0113757310.3390/cells13070573Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital FacilitationSami Boudkkazi0Dominique Debanne1Physiology Institute, University of Freiburg, 79104 Freiburg, GermanyUnité de Neurobiologie des Canaux Ioniques et de la Synapse (UNIS), Institut National de la Santé et de la Recherche Médicale (INSERM), Aix-Marseille University, 13015 Marseille, FranceNeuronal timing with millisecond precision is critical for many brain functions such as sensory perception, learning and memory formation. At the level of the chemical synapse, the synaptic delay is determined by the presynaptic release probability (<i>Pr</i>) and the waveform of the presynaptic action potential (AP). For instance, paired-pulse facilitation or presynaptic long-term potentiation are associated with reductions in the synaptic delay, whereas paired-pulse depression or presynaptic long-term depression are associated with an increased synaptic delay. Parallelly, the AP broadening that results from the inactivation of voltage gated potassium (Kv) channels responsible for the repolarization phase of the AP delays the synaptic response, and the inactivation of sodium (Nav) channels by voltage reduces the synaptic latency. However, whether synaptic delay is modulated during depolarization-induced analogue–digital facilitation (d-ADF), a form of context-dependent synaptic facilitation induced by prolonged depolarization of the presynaptic neuron and mediated by the voltage-inactivation of presynaptic Kv1 channels, remains unclear. We show here that despite <i>Pr</i> being elevated during d-ADF at pyramidal L5-L5 cell synapses, the synaptic delay is surprisingly unchanged. This finding suggests that both <i>Pr</i>- and AP-dependent changes in synaptic delay compensate for each other during d-ADF. We conclude that, in contrast to other short- or long-term modulations of presynaptic release, synaptic timing is not affected during d-ADF because of the opposite interaction of <i>Pr</i>- and AP-dependent modulations of synaptic delay.https://www.mdpi.com/2073-4409/13/7/573neuronal timingsynaptic transmissionsynaptic latencycontext-dependent facilitationneocortexlocal circuits
spellingShingle Sami Boudkkazi
Dominique Debanne
Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation
Cells
neuronal timing
synaptic transmission
synaptic latency
context-dependent facilitation
neocortex
local circuits
title Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation
title_full Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation
title_fullStr Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation
title_full_unstemmed Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation
title_short Enhanced Release Probability without Changes in Synaptic Delay during Analogue–Digital Facilitation
title_sort enhanced release probability without changes in synaptic delay during analogue digital facilitation
topic neuronal timing
synaptic transmission
synaptic latency
context-dependent facilitation
neocortex
local circuits
url https://www.mdpi.com/2073-4409/13/7/573
work_keys_str_mv AT samiboudkkazi enhancedreleaseprobabilitywithoutchangesinsynapticdelayduringanaloguedigitalfacilitation
AT dominiquedebanne enhancedreleaseprobabilitywithoutchangesinsynapticdelayduringanaloguedigitalfacilitation