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Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex

Preterm infant brain activity is discontinuous; bursts of activity recorded using EEG (electroencephalography), thought to be driven by subcortical regions, display scale free properties and exhibit a complex temporal ordering known as long-range temporal correlations (LRTCs). During brain developme...

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Detalles Bibliográficos
Autores principales: Hartley, Caroline, Farmer, Simon, Berthouze, Luc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6953763/
https://www.ncbi.nlm.nih.gov/pubmed/31923200
http://dx.doi.org/10.1371/journal.pone.0226772
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author Hartley, Caroline
Farmer, Simon
Berthouze, Luc
author_facet Hartley, Caroline
Farmer, Simon
Berthouze, Luc
author_sort Hartley, Caroline
collection PubMed
description Preterm infant brain activity is discontinuous; bursts of activity recorded using EEG (electroencephalography), thought to be driven by subcortical regions, display scale free properties and exhibit a complex temporal ordering known as long-range temporal correlations (LRTCs). During brain development, activity-dependent mechanisms are essential for synaptic connectivity formation, and abolishing burst activity in animal models leads to weak disorganised synaptic connectivity. Moreover, synaptic pruning shares similar mechanisms to spike-timing dependent plasticity (STDP), suggesting that the timing of activity may play a critical role in connectivity formation. We investigated, in a computational model of leaky integrate-and-fire neurones, whether the temporal ordering of burst activity within an external driving input could modulate connectivity formation in the network. Connectivity evolved across the course of simulations using an approach analogous to STDP, from networks with initial random connectivity. Small-world connectivity and hub neurones emerged in the network structure—characteristic properties of mature brain networks. Notably, driving the network with an external input which exhibited LRTCs in the temporal ordering of burst activity facilitated the emergence of these network properties, increasing the speed with which they emerged compared with when the network was driven by the same input with the bursts randomly ordered in time. Moreover, the emergence of small-world properties was dependent on the strength of the LRTCs. These results suggest that the temporal ordering of burst activity could play an important role in synaptic connectivity formation and the emergence of small-world topology in the developing brain.
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spelling pubmed-69537632020-01-21 Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex Hartley, Caroline Farmer, Simon Berthouze, Luc PLoS One Research Article Preterm infant brain activity is discontinuous; bursts of activity recorded using EEG (electroencephalography), thought to be driven by subcortical regions, display scale free properties and exhibit a complex temporal ordering known as long-range temporal correlations (LRTCs). During brain development, activity-dependent mechanisms are essential for synaptic connectivity formation, and abolishing burst activity in animal models leads to weak disorganised synaptic connectivity. Moreover, synaptic pruning shares similar mechanisms to spike-timing dependent plasticity (STDP), suggesting that the timing of activity may play a critical role in connectivity formation. We investigated, in a computational model of leaky integrate-and-fire neurones, whether the temporal ordering of burst activity within an external driving input could modulate connectivity formation in the network. Connectivity evolved across the course of simulations using an approach analogous to STDP, from networks with initial random connectivity. Small-world connectivity and hub neurones emerged in the network structure—characteristic properties of mature brain networks. Notably, driving the network with an external input which exhibited LRTCs in the temporal ordering of burst activity facilitated the emergence of these network properties, increasing the speed with which they emerged compared with when the network was driven by the same input with the bursts randomly ordered in time. Moreover, the emergence of small-world properties was dependent on the strength of the LRTCs. These results suggest that the temporal ordering of burst activity could play an important role in synaptic connectivity formation and the emergence of small-world topology in the developing brain. Public Library of Science 2020-01-10 /pmc/articles/PMC6953763/ /pubmed/31923200 http://dx.doi.org/10.1371/journal.pone.0226772 Text en © 2020 Hartley et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hartley, Caroline
Farmer, Simon
Berthouze, Luc
Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
title Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
title_full Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
title_fullStr Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
title_full_unstemmed Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
title_short Temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
title_sort temporal ordering of input modulates connectivity formation in a developmental neuronal network model of the cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6953763/
https://www.ncbi.nlm.nih.gov/pubmed/31923200
http://dx.doi.org/10.1371/journal.pone.0226772
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