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Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states

Understanding the neurovascular coupling (NVC) underlying hemodynamic changes in epilepsy is crucial to properly interpreting functional brain imaging signals associated with epileptic events. However, how excitatory and inhibitory neurons affect vascular responses in different epileptic states rema...

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Autores principales: Lim, Hyun-Kyoung, You, Nayeon, Bae, Sungjun, Kang, Bok-Man, Shon, Young-Min, Kim, Seong-Gi, Suh, Minah
Formato: Online Artículo Texto
Lenguaje:English
Publicado: SAGE Publications 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8054729/
https://www.ncbi.nlm.nih.gov/pubmed/32669018
http://dx.doi.org/10.1177/0271678X20934071
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author Lim, Hyun-Kyoung
You, Nayeon
Bae, Sungjun
Kang, Bok-Man
Shon, Young-Min
Kim, Seong-Gi
Suh, Minah
author_facet Lim, Hyun-Kyoung
You, Nayeon
Bae, Sungjun
Kang, Bok-Man
Shon, Young-Min
Kim, Seong-Gi
Suh, Minah
author_sort Lim, Hyun-Kyoung
collection PubMed
description Understanding the neurovascular coupling (NVC) underlying hemodynamic changes in epilepsy is crucial to properly interpreting functional brain imaging signals associated with epileptic events. However, how excitatory and inhibitory neurons affect vascular responses in different epileptic states remains unknown. We conducted real-time in vivo measurements of cerebral blood flow (CBF), vessel diameter, and excitatory and inhibitory neuronal calcium signals during recurrent focal seizures. During preictal states, decreases in CBF and arteriole diameter were closely related to decreased γ-band local field potential (LFP) power, which was linked to relatively elevated excitatory and reduced inhibitory neuronal activity levels. Notably, this preictal condition was followed by a strengthened ictal event. In particular, the preictal inhibitory activity level was positively correlated with coherent oscillating activity specific to inhibitory neurons. In contrast, ictal states were characterized by elevated synchrony in excitatory neurons. Given these findings, we suggest that excitatory and inhibitory neurons differentially contribute to shaping the ictal and preictal neural states, respectively. Moreover, the preictal vascular activity, alongside with the γ-band, may reflect the relative levels of excitatory and inhibitory neuronal activity, and upcoming ictal activity. Our findings provide useful insights into how perfusion signals of different epileptic states are related in terms of NVC.
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spelling pubmed-80547292021-05-03 Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states Lim, Hyun-Kyoung You, Nayeon Bae, Sungjun Kang, Bok-Man Shon, Young-Min Kim, Seong-Gi Suh, Minah J Cereb Blood Flow Metab Original Articles Understanding the neurovascular coupling (NVC) underlying hemodynamic changes in epilepsy is crucial to properly interpreting functional brain imaging signals associated with epileptic events. However, how excitatory and inhibitory neurons affect vascular responses in different epileptic states remains unknown. We conducted real-time in vivo measurements of cerebral blood flow (CBF), vessel diameter, and excitatory and inhibitory neuronal calcium signals during recurrent focal seizures. During preictal states, decreases in CBF and arteriole diameter were closely related to decreased γ-band local field potential (LFP) power, which was linked to relatively elevated excitatory and reduced inhibitory neuronal activity levels. Notably, this preictal condition was followed by a strengthened ictal event. In particular, the preictal inhibitory activity level was positively correlated with coherent oscillating activity specific to inhibitory neurons. In contrast, ictal states were characterized by elevated synchrony in excitatory neurons. Given these findings, we suggest that excitatory and inhibitory neurons differentially contribute to shaping the ictal and preictal neural states, respectively. Moreover, the preictal vascular activity, alongside with the γ-band, may reflect the relative levels of excitatory and inhibitory neuronal activity, and upcoming ictal activity. Our findings provide useful insights into how perfusion signals of different epileptic states are related in terms of NVC. SAGE Publications 2020-07-15 2021-05 /pmc/articles/PMC8054729/ /pubmed/32669018 http://dx.doi.org/10.1177/0271678X20934071 Text en © The Author(s) 2020 https://creativecommons.org/licenses/by-nc/4.0/This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
spellingShingle Original Articles
Lim, Hyun-Kyoung
You, Nayeon
Bae, Sungjun
Kang, Bok-Man
Shon, Young-Min
Kim, Seong-Gi
Suh, Minah
Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
title Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
title_full Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
title_fullStr Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
title_full_unstemmed Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
title_short Differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
title_sort differential contribution of excitatory and inhibitory neurons in shaping neurovascular coupling in different epileptic neural states
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8054729/
https://www.ncbi.nlm.nih.gov/pubmed/32669018
http://dx.doi.org/10.1177/0271678X20934071
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