Modulation of synaptic transmission in neocortex by network activities

Crochet, Sylvain; Chauvette, Sylvain; Boucetta, Sofiane; Timofeev, Igor

doi:10.1111/j.1460-9568.2005.03932.x

Cited by 106Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionMemory and Neural Mechanisms

Modulation of synaptic transmission in neocortex by network activities

Crochet, Sylvain, Chauvette, Sylvain, Boucetta, Sofiane, Timofeev, Igor·2005·European Journal of Neuroscience

DOI 10.1111/j.1460-9568.2005.03932.x

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Abstract

Neocortical neurons integrate inputs from thousands of presynaptic neurons that fire in vivo with frequencies that can reach 20 Hz. An important issue in understanding cortical integration is to determine the actual impact of presynaptic firing on postsynaptic neuron in the context of an active network. We used dual intracellular recordings from synaptically connected neurons or microstimulation to study the properties of spontaneous and evoked single‐axon excitatory postsynaptic potentials (EPSPs) in vivo, in barbiturate or ketamine−xylazine anaesthetized cats. We found that active states of the cortical network were associated with higher variability and decrease in amplitude and duration of the EPSPs owing to a shunting effect. Moreover, the number of apparent failures markedly increased during active states as compared with silent states. Single‐axon EPSPs in vivo showed mainly paired‐pulse facilitation, and the paired‐pulse ratio increased during active states as compare to silent states, suggesting a decrease in release probability during active states. Raising extracellular Ca 2+ concentration to 2.5–3.0 m m by reverse microdialysis reduced the number of apparent failures and significantly increased the mean amplitude of individual synaptic potentials. Quantitative analysis of spontaneous synaptic activity suggested that the proportion of presynaptic activity that impact at the soma of a cortical neuron in vivo was low because of a high failure rate, a shunting effect and probably dendritic filtering. We conclude that during active states of cortical network, the efficacy of synaptic transmission in individual synapses is low, thus safe transmission of information requires synchronized activity of a large population of presynaptic neurons.

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Extracellular Ca2+ concentrations are increased during the downstate, which enhances synaptic efficacy, such that a single spike generated in this condition may effectively excite the whole network.
“Moreover, extracellular Ca 2ϩ concentrations are increased during the downstate, which enhances synaptic efficacy, such that a single spike generated in this condition may effectively excite the whole network (238, 790), in particular when such spikes originate from neurons in deep cortical layers with larger numbers of synaptic contacts to other neurons (188).”
From About Sleep's Role in Memory (2013) · cites this paper as [238]

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“Moreover, extracellular Ca(2) concentrations are increased during the downstate, which enhances synaptic efficacy, such that a single spike generated in this condition may effectively excite the whole network (238, 790), in particular when such spikes originate from neurons in deep cortical layers with larger numbers…”
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Authors: Crochet, S., Chauvette, S., Boucetta, S., & Timofeev, I.
Affiliations: Université Laval (CA)
Corresponding author: Timofeev, Igor
ORCID: Crochet, Sylvain
Chauvette, Sylvain
Timofeev, Igor
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2005-02
Volume: 21
Issue: 4
Pages: 1030-1044
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/j.1460-9568.2005.03932.x
OpenAlex: W1821334170
Cited by: 106
References: 81
Citations by year: 2026: 2 · 2025: 4 · 2024: 3 · 2023: 3 · 2021: 3 · 2020: 4 · 2019: 8 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 4 · 2014: 6 · 2013: 5 · 2012: 9
FWCI: 3.00
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 36 d)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Corpus Université Laval (Université Laval) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: synaptic transmission, neocortex, cortical network activity, excitatory postsynaptic potentials, shunting inhibition, synaptic failure, paired-pulse facilitation, release probability, extracellular calcium, spontaneous synaptic activity, synaptic integration
MeSH terms: Action Potentials, Animals, Axons, Calcium, Cats, Dose-Response Relationship, Drug, Electric Stimulation, Electroencephalography, Nerve Net, Synaptic Transmission, Neurons, Microdialysis, Neocortex, Excitatory Postsynaptic Potentials

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Modulation of synaptic transmission in neocortex by network activities

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