Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.

Small-World Networks (SWNs) represent a fundamental model for the comprehension of many complex man-made and biological networks. In the central nervous system, SWN models have been shown to fit well both anatomical and functional maps at the macroscopic level. However, the functional microscopic le...

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Main Authors: Antonio G Zippo, Riccardo Storchi, Sara Nencini, Gian Carlo Caramenti, Maurizio Valente, Gabriele Eliseo M Biella
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS Computational Biology
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23785273/pdf/?tool=EBI
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spelling doaj-65e6c561206d4fdca9a0290f7256e70e2021-04-21T15:09:22ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582013-01-0196e100310410.1371/journal.pcbi.1003104Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.Antonio G ZippoRiccardo StorchiSara NenciniGian Carlo CaramentiMaurizio ValenteGabriele Eliseo M BiellaSmall-World Networks (SWNs) represent a fundamental model for the comprehension of many complex man-made and biological networks. In the central nervous system, SWN models have been shown to fit well both anatomical and functional maps at the macroscopic level. However, the functional microscopic level, where the nodes of a network are represented by single neurons, is still poorly understood. At this level, although recent evidences suggest that functional connection graphs exhibit small-world organization, it is not known whether and how these maps, potentially distributed in multiple brain regions, change across different conditions, such as spontaneous and stimulus-evoked activities. We addressed these questions by analyzing the data from simultaneous multi-array extracellular recordings in three brain regions of rats, diversely involved in somatosensory information processing: the ventropostero-lateral thalamic nuclei, the primary somatosensory cortex and the centro-median thalamic nuclei. From both spike and Local Field Potential (LFP) recordings, we estimated the functional connection graphs by using the Normalized Compression Similarity for spikes and the Phase Synchrony for LFPs. Then, by using graph-theoretical statistics, we characterized the functional topology both during spontaneous activity and sensory stimulation. Our main results show that: (i) spikes and LFPs show SWN organization during spontaneous activity; (ii) after stimulation onset, while substantial functional graph reconfigurations occur both in spike and LFPs, small-worldness is nonetheless preserved; (iii) the stimulus triggers a significant increase of inter-area LFP connections without modifying the topology of intra-area functional connections. Finally, investigating computationally the functional substrate that supports the observed phenomena, we found that (iv) the fundamental concept of cell assemblies, transient groups of activating neurons, can be described by small-world networks. Our results suggest that activity of neurons from multiple areas of the rat somatosensory system contributes to the integration of local computations arisen in distributed functional cell assemblies according to the principles of SWNs.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23785273/pdf/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Antonio G Zippo
Riccardo Storchi
Sara Nencini
Gian Carlo Caramenti
Maurizio Valente
Gabriele Eliseo M Biella
spellingShingle Antonio G Zippo
Riccardo Storchi
Sara Nencini
Gian Carlo Caramenti
Maurizio Valente
Gabriele Eliseo M Biella
Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
PLoS Computational Biology
author_facet Antonio G Zippo
Riccardo Storchi
Sara Nencini
Gian Carlo Caramenti
Maurizio Valente
Gabriele Eliseo M Biella
author_sort Antonio G Zippo
title Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
title_short Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
title_full Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
title_fullStr Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
title_full_unstemmed Neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
title_sort neuronal functional connection graphs among multiple areas of the rat somatosensory system during spontaneous and evoked activities.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2013-01-01
description Small-World Networks (SWNs) represent a fundamental model for the comprehension of many complex man-made and biological networks. In the central nervous system, SWN models have been shown to fit well both anatomical and functional maps at the macroscopic level. However, the functional microscopic level, where the nodes of a network are represented by single neurons, is still poorly understood. At this level, although recent evidences suggest that functional connection graphs exhibit small-world organization, it is not known whether and how these maps, potentially distributed in multiple brain regions, change across different conditions, such as spontaneous and stimulus-evoked activities. We addressed these questions by analyzing the data from simultaneous multi-array extracellular recordings in three brain regions of rats, diversely involved in somatosensory information processing: the ventropostero-lateral thalamic nuclei, the primary somatosensory cortex and the centro-median thalamic nuclei. From both spike and Local Field Potential (LFP) recordings, we estimated the functional connection graphs by using the Normalized Compression Similarity for spikes and the Phase Synchrony for LFPs. Then, by using graph-theoretical statistics, we characterized the functional topology both during spontaneous activity and sensory stimulation. Our main results show that: (i) spikes and LFPs show SWN organization during spontaneous activity; (ii) after stimulation onset, while substantial functional graph reconfigurations occur both in spike and LFPs, small-worldness is nonetheless preserved; (iii) the stimulus triggers a significant increase of inter-area LFP connections without modifying the topology of intra-area functional connections. Finally, investigating computationally the functional substrate that supports the observed phenomena, we found that (iv) the fundamental concept of cell assemblies, transient groups of activating neurons, can be described by small-world networks. Our results suggest that activity of neurons from multiple areas of the rat somatosensory system contributes to the integration of local computations arisen in distributed functional cell assemblies according to the principles of SWNs.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23785273/pdf/?tool=EBI
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