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Computational analysis of network activity and spatial reach of sharp wave-ripples

Network oscillations of different frequencies, durations and amplitudes are hypothesized to coordinate information processing and transfer across brain areas. Among these oscillations, hippocampal sharp wave-ripple complexes (SPW-Rs) are one of the most prominent. SPW-Rs occurring in the hippocampus...

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Autores principales: Canakci, Sadullah, Toy, Muhammed Faruk, Inci, Ahmet Fatih, Liu, Xin, Kuzum, Duygu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5600383/
https://www.ncbi.nlm.nih.gov/pubmed/28915251
http://dx.doi.org/10.1371/journal.pone.0184542
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author Canakci, Sadullah
Toy, Muhammed Faruk
Inci, Ahmet Fatih
Liu, Xin
Kuzum, Duygu
author_facet Canakci, Sadullah
Toy, Muhammed Faruk
Inci, Ahmet Fatih
Liu, Xin
Kuzum, Duygu
author_sort Canakci, Sadullah
collection PubMed
description Network oscillations of different frequencies, durations and amplitudes are hypothesized to coordinate information processing and transfer across brain areas. Among these oscillations, hippocampal sharp wave-ripple complexes (SPW-Rs) are one of the most prominent. SPW-Rs occurring in the hippocampus are suggested to play essential roles in memory consolidation as well as information transfer to the neocortex. To-date, most of the knowledge about SPW-Rs comes from experimental studies averaging responses from neuronal populations monitored by conventional microelectrodes. In this work, we investigate spatiotemporal characteristics of SPW-Rs and how microelectrode size and distance influence SPW-R recordings using a biophysical model of hippocampus. We also explore contributions from neuronal spikes and synaptic potentials to SPW-Rs based on two different types of network activity. Our study suggests that neuronal spikes from pyramidal cells contribute significantly to ripples while high amplitude sharp waves mainly arise from synaptic activity. Our simulations on spatial reach of SPW-Rs show that the amplitudes of sharp waves and ripples exhibit a steep decrease with distance from the network and this effect is more prominent for smaller area electrodes. Furthermore, the amplitude of the signal decreases strongly with increasing electrode surface area as a result of averaging. The relative decrease is more pronounced when the recording electrode is closer to the source of the activity. Through simulations of field potentials across a high-density microelectrode array, we demonstrate the importance of finding the ideal spatial resolution for capturing SPW-Rs with great sensitivity. Our work provides insights on contributions from spikes and synaptic potentials to SPW-Rs and describes the effect of measurement configuration on LFPs to guide experimental studies towards improved SPW-R recordings.
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spelling pubmed-56003832017-09-22 Computational analysis of network activity and spatial reach of sharp wave-ripples Canakci, Sadullah Toy, Muhammed Faruk Inci, Ahmet Fatih Liu, Xin Kuzum, Duygu PLoS One Research Article Network oscillations of different frequencies, durations and amplitudes are hypothesized to coordinate information processing and transfer across brain areas. Among these oscillations, hippocampal sharp wave-ripple complexes (SPW-Rs) are one of the most prominent. SPW-Rs occurring in the hippocampus are suggested to play essential roles in memory consolidation as well as information transfer to the neocortex. To-date, most of the knowledge about SPW-Rs comes from experimental studies averaging responses from neuronal populations monitored by conventional microelectrodes. In this work, we investigate spatiotemporal characteristics of SPW-Rs and how microelectrode size and distance influence SPW-R recordings using a biophysical model of hippocampus. We also explore contributions from neuronal spikes and synaptic potentials to SPW-Rs based on two different types of network activity. Our study suggests that neuronal spikes from pyramidal cells contribute significantly to ripples while high amplitude sharp waves mainly arise from synaptic activity. Our simulations on spatial reach of SPW-Rs show that the amplitudes of sharp waves and ripples exhibit a steep decrease with distance from the network and this effect is more prominent for smaller area electrodes. Furthermore, the amplitude of the signal decreases strongly with increasing electrode surface area as a result of averaging. The relative decrease is more pronounced when the recording electrode is closer to the source of the activity. Through simulations of field potentials across a high-density microelectrode array, we demonstrate the importance of finding the ideal spatial resolution for capturing SPW-Rs with great sensitivity. Our work provides insights on contributions from spikes and synaptic potentials to SPW-Rs and describes the effect of measurement configuration on LFPs to guide experimental studies towards improved SPW-R recordings. Public Library of Science 2017-09-15 /pmc/articles/PMC5600383/ /pubmed/28915251 http://dx.doi.org/10.1371/journal.pone.0184542 Text en © 2017 Canakci 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
Canakci, Sadullah
Toy, Muhammed Faruk
Inci, Ahmet Fatih
Liu, Xin
Kuzum, Duygu
Computational analysis of network activity and spatial reach of sharp wave-ripples
title Computational analysis of network activity and spatial reach of sharp wave-ripples
title_full Computational analysis of network activity and spatial reach of sharp wave-ripples
title_fullStr Computational analysis of network activity and spatial reach of sharp wave-ripples
title_full_unstemmed Computational analysis of network activity and spatial reach of sharp wave-ripples
title_short Computational analysis of network activity and spatial reach of sharp wave-ripples
title_sort computational analysis of network activity and spatial reach of sharp wave-ripples
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5600383/
https://www.ncbi.nlm.nih.gov/pubmed/28915251
http://dx.doi.org/10.1371/journal.pone.0184542
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