External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations.
Electrical oscillations in neuronal network activity are ubiquitous in the brain and have been associated with cognition and behavior. Intriguingly, the amplitude of ongoing oscillations, such as measured in EEG recordings, fluctuates irregularly, with episodes of high amplitude alternating with epi...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2012-01-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002666&type=printable |
| _version_ | 1826799407115272192 |
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| author | Oscar J Avella Gonzalez Karlijn I van Aerde Ronald A J van Elburg Simon-Shlomo Poil Huibert D Mansvelder Klaus Linkenkaer-Hansen Jaap van Pelt Arjen van Ooyen |
| author_facet | Oscar J Avella Gonzalez Karlijn I van Aerde Ronald A J van Elburg Simon-Shlomo Poil Huibert D Mansvelder Klaus Linkenkaer-Hansen Jaap van Pelt Arjen van Ooyen |
| author_sort | Oscar J Avella Gonzalez |
| collection | DOAJ |
| description | Electrical oscillations in neuronal network activity are ubiquitous in the brain and have been associated with cognition and behavior. Intriguingly, the amplitude of ongoing oscillations, such as measured in EEG recordings, fluctuates irregularly, with episodes of high amplitude alternating with episodes of low amplitude. Despite the widespread occurrence of amplitude fluctuations in many frequency bands and brain regions, the mechanisms by which they are generated are poorly understood. Here, we show that irregular transitions between sub-second episodes of high- and low-amplitude oscillations in the alpha/beta frequency band occur in a generic neuronal network model consisting of interconnected inhibitory and excitatory cells that are externally driven by sustained cholinergic input and trains of action potentials that activate excitatory synapses. In the model, we identify the action potential drive onto inhibitory cells, which represents input from other brain areas and is shown to desynchronize network activity, to be crucial for the emergence of amplitude fluctuations. We show that the duration distributions of high-amplitude episodes in the model match those observed in rat prefrontal cortex for oscillations induced by the cholinergic agonist carbachol. Furthermore, the mean duration of high-amplitude episodes varies in a bell-shaped manner with carbachol concentration, just as in mouse hippocampus. Our results suggest that amplitude fluctuations are a general property of oscillatory neuronal networks that can arise through background input from areas external to the network. |
| first_indexed | 2024-04-12T05:38:49Z |
| format | Article |
| id | doaj.art-7276c482e5e9493f98af99a11ef75c59 |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2025-03-17T00:34:35Z |
| publishDate | 2012-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-7276c482e5e9493f98af99a11ef75c592025-02-21T05:32:11ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582012-01-0188e100266610.1371/journal.pcbi.1002666External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations.Oscar J Avella GonzalezKarlijn I van AerdeRonald A J van ElburgSimon-Shlomo PoilHuibert D MansvelderKlaus Linkenkaer-HansenJaap van PeltArjen van OoyenElectrical oscillations in neuronal network activity are ubiquitous in the brain and have been associated with cognition and behavior. Intriguingly, the amplitude of ongoing oscillations, such as measured in EEG recordings, fluctuates irregularly, with episodes of high amplitude alternating with episodes of low amplitude. Despite the widespread occurrence of amplitude fluctuations in many frequency bands and brain regions, the mechanisms by which they are generated are poorly understood. Here, we show that irregular transitions between sub-second episodes of high- and low-amplitude oscillations in the alpha/beta frequency band occur in a generic neuronal network model consisting of interconnected inhibitory and excitatory cells that are externally driven by sustained cholinergic input and trains of action potentials that activate excitatory synapses. In the model, we identify the action potential drive onto inhibitory cells, which represents input from other brain areas and is shown to desynchronize network activity, to be crucial for the emergence of amplitude fluctuations. We show that the duration distributions of high-amplitude episodes in the model match those observed in rat prefrontal cortex for oscillations induced by the cholinergic agonist carbachol. Furthermore, the mean duration of high-amplitude episodes varies in a bell-shaped manner with carbachol concentration, just as in mouse hippocampus. Our results suggest that amplitude fluctuations are a general property of oscillatory neuronal networks that can arise through background input from areas external to the network.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002666&type=printable |
| spellingShingle | Oscar J Avella Gonzalez Karlijn I van Aerde Ronald A J van Elburg Simon-Shlomo Poil Huibert D Mansvelder Klaus Linkenkaer-Hansen Jaap van Pelt Arjen van Ooyen External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations. PLoS Computational Biology |
| title | External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations. |
| title_full | External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations. |
| title_fullStr | External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations. |
| title_full_unstemmed | External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations. |
| title_short | External drive to inhibitory cells induces alternating episodes of high- and low-amplitude oscillations. |
| title_sort | external drive to inhibitory cells induces alternating episodes of high and low amplitude oscillations |
| url | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002666&type=printable |
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