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Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks
Brain-state alternation is important for long-term memory formation. Each brain state can be identified with a specific process in memory formation, e.g., encoding during wakefulness or consolidation during sleeping. The hippocampal-neocortical dialogue was proposed as a hypothetical framework for s...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9168126/ https://www.ncbi.nlm.nih.gov/pubmed/35677356 http://dx.doi.org/10.3389/fnins.2022.873664 |
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author | Chang, ChihHsiang Furukawa, Takuma Asahina, Takahiro Shimba, Kenta Kotani, Kiyoshi Jimbo, Yasuhiko |
author_facet | Chang, ChihHsiang Furukawa, Takuma Asahina, Takahiro Shimba, Kenta Kotani, Kiyoshi Jimbo, Yasuhiko |
author_sort | Chang, ChihHsiang |
collection | PubMed |
description | Brain-state alternation is important for long-term memory formation. Each brain state can be identified with a specific process in memory formation, e.g., encoding during wakefulness or consolidation during sleeping. The hippocampal-neocortical dialogue was proposed as a hypothetical framework for systems consolidation, which features different cross-frequency couplings between the hippocampus and distributed neocortical regions in different brain states. Despite evidence supporting this hypothesis, little has been reported about how information is processed with shifts in brain states. To address this gap, we developed an in vitro neocortical-hippocampal coculture model to study how activity coupling can affect connections between coupled networks. Neocortical and hippocampal neurons were cultured in two different compartments connected by a micro-tunnel structure. The network activity of the coculture model was recorded by microelectrode arrays underlying the substrate. Rhythmic bursting was observed in the spontaneous activity and electrical evoked responses. Rhythmic bursting activity in one compartment could couple to that in the other via axons passing through the micro-tunnels. Two types of coupling patterns were observed: slow-burst coupling (neocortex at 0.1–0.5 Hz and hippocampus at 1 Hz) and fast burst coupling (neocortex at 20–40 Hz and hippocampus at 4–10 Hz). The network activity showed greater synchronicity in the slow-burst coupling, as indicated by changes in the burstiness index. Network synchronicity analysis suggests the presence of different information processing states under different burst activity coupling patterns. Our results suggest that the hippocampal-neocortical coculture model possesses multiple modes of burst activity coupling between the cortical and hippocampal parts. With the addition of external stimulation, the neocortical-hippocampal network model we developed can elucidate the influence of state shifts on information processing. |
format | Online Article Text |
id | pubmed-9168126 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-91681262022-06-07 Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks Chang, ChihHsiang Furukawa, Takuma Asahina, Takahiro Shimba, Kenta Kotani, Kiyoshi Jimbo, Yasuhiko Front Neurosci Neuroscience Brain-state alternation is important for long-term memory formation. Each brain state can be identified with a specific process in memory formation, e.g., encoding during wakefulness or consolidation during sleeping. The hippocampal-neocortical dialogue was proposed as a hypothetical framework for systems consolidation, which features different cross-frequency couplings between the hippocampus and distributed neocortical regions in different brain states. Despite evidence supporting this hypothesis, little has been reported about how information is processed with shifts in brain states. To address this gap, we developed an in vitro neocortical-hippocampal coculture model to study how activity coupling can affect connections between coupled networks. Neocortical and hippocampal neurons were cultured in two different compartments connected by a micro-tunnel structure. The network activity of the coculture model was recorded by microelectrode arrays underlying the substrate. Rhythmic bursting was observed in the spontaneous activity and electrical evoked responses. Rhythmic bursting activity in one compartment could couple to that in the other via axons passing through the micro-tunnels. Two types of coupling patterns were observed: slow-burst coupling (neocortex at 0.1–0.5 Hz and hippocampus at 1 Hz) and fast burst coupling (neocortex at 20–40 Hz and hippocampus at 4–10 Hz). The network activity showed greater synchronicity in the slow-burst coupling, as indicated by changes in the burstiness index. Network synchronicity analysis suggests the presence of different information processing states under different burst activity coupling patterns. Our results suggest that the hippocampal-neocortical coculture model possesses multiple modes of burst activity coupling between the cortical and hippocampal parts. With the addition of external stimulation, the neocortical-hippocampal network model we developed can elucidate the influence of state shifts on information processing. Frontiers Media S.A. 2022-05-23 /pmc/articles/PMC9168126/ /pubmed/35677356 http://dx.doi.org/10.3389/fnins.2022.873664 Text en Copyright © 2022 Chang, Furukawa, Asahina, Shimba, Kotani and Jimbo. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Neuroscience Chang, ChihHsiang Furukawa, Takuma Asahina, Takahiro Shimba, Kenta Kotani, Kiyoshi Jimbo, Yasuhiko Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks |
title | Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks |
title_full | Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks |
title_fullStr | Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks |
title_full_unstemmed | Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks |
title_short | Coupling of in vitro Neocortical-Hippocampal Coculture Bursts Induces Different Spike Rhythms in Individual Networks |
title_sort | coupling of in vitro neocortical-hippocampal coculture bursts induces different spike rhythms in individual networks |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9168126/ https://www.ncbi.nlm.nih.gov/pubmed/35677356 http://dx.doi.org/10.3389/fnins.2022.873664 |
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