Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Chang, ChihHsiang, Furukawa, Takuma, Asahina, Takahiro, Shimba, Kenta, Kotani, Kiyoshi, Jimbo, Yasuhiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
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
_version_ 1784720932004167680
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
work_keys_str_mv AT changchihhsiang couplingofinvitroneocorticalhippocampalcocultureburstsinducesdifferentspikerhythmsinindividualnetworks
AT furukawatakuma couplingofinvitroneocorticalhippocampalcocultureburstsinducesdifferentspikerhythmsinindividualnetworks
AT asahinatakahiro couplingofinvitroneocorticalhippocampalcocultureburstsinducesdifferentspikerhythmsinindividualnetworks
AT shimbakenta couplingofinvitroneocorticalhippocampalcocultureburstsinducesdifferentspikerhythmsinindividualnetworks
AT kotanikiyoshi couplingofinvitroneocorticalhippocampalcocultureburstsinducesdifferentspikerhythmsinindividualnetworks
AT jimboyasuhiko couplingofinvitroneocorticalhippocampalcocultureburstsinducesdifferentspikerhythmsinindividualnetworks