Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices

Takuya Sasaki, Tomoe Ishikawa, Reimi Abe, Ryota Nakayama, Akiko Asada, Norio Matsuki, Yuji Ikegaya

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Astrocytes are thought to detect neuronal activity in the form of intracellular calcium elevations; thereby, astrocytes can regulate neuronal excitability and synaptic transmission. Little is known, however, about how the astrocyte calcium signal regulates the activity of neuronal populations. In this study, we addressed this issue using functional multineuron calcium imaging in hippocampal slice cultures. Under normal conditions, CA3 neuronal networks exhibited temporally correlated activity patterns, occasionally generating large synchronization among a subset of cells. The synchronized neuronal activity was correlated with astrocyte calcium events. Calcium buffering by an intracellular injection of a calcium chelator into multiple astrocytes reduced the synaptic strength of unitary transmission between pairs of surrounding pyramidal cells and caused desynchronization of the neuronal networks. Uncaging the calcium in the astrocytes increased the frequency of neuronal synchronization. These data suggest an essential role of the astrocyte calcium signal in the maintenance of basal neuronal function at the circuit level.

Original languageEnglish
Pages (from-to)2771-2783
Number of pages13
JournalJournal of Physiology
Volume592
Issue number13
DOIs
Publication statusPublished - 2014 Jul 1
Externally publishedYes

Fingerprint

Calcium Signaling
Astrocytes
Calcium
Pyramidal Cells
Synaptic Transmission
Maintenance
Injections
Population

ASJC Scopus subject areas

  • Physiology

Cite this

Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices. / Sasaki, Takuya; Ishikawa, Tomoe; Abe, Reimi; Nakayama, Ryota; Asada, Akiko; Matsuki, Norio; Ikegaya, Yuji.

In: Journal of Physiology, Vol. 592, No. 13, 01.07.2014, p. 2771-2783.

Research output: Contribution to journalArticle

Sasaki, Takuya ; Ishikawa, Tomoe ; Abe, Reimi ; Nakayama, Ryota ; Asada, Akiko ; Matsuki, Norio ; Ikegaya, Yuji. / Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices. In: Journal of Physiology. 2014 ; Vol. 592, No. 13. pp. 2771-2783.
@article{09aca5a04d9742e4b1cca76322a1f815,
title = "Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices",
abstract = "Astrocytes are thought to detect neuronal activity in the form of intracellular calcium elevations; thereby, astrocytes can regulate neuronal excitability and synaptic transmission. Little is known, however, about how the astrocyte calcium signal regulates the activity of neuronal populations. In this study, we addressed this issue using functional multineuron calcium imaging in hippocampal slice cultures. Under normal conditions, CA3 neuronal networks exhibited temporally correlated activity patterns, occasionally generating large synchronization among a subset of cells. The synchronized neuronal activity was correlated with astrocyte calcium events. Calcium buffering by an intracellular injection of a calcium chelator into multiple astrocytes reduced the synaptic strength of unitary transmission between pairs of surrounding pyramidal cells and caused desynchronization of the neuronal networks. Uncaging the calcium in the astrocytes increased the frequency of neuronal synchronization. These data suggest an essential role of the astrocyte calcium signal in the maintenance of basal neuronal function at the circuit level.",
author = "Takuya Sasaki and Tomoe Ishikawa and Reimi Abe and Ryota Nakayama and Akiko Asada and Norio Matsuki and Yuji Ikegaya",
year = "2014",
month = "7",
day = "1",
doi = "10.1113/jphysiol.2014.272864",
language = "English",
volume = "592",
pages = "2771--2783",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",
number = "13",

}

TY - JOUR

T1 - Astrocyte calcium signalling orchestrates neuronal synchronization in organotypic hippocampal slices

AU - Sasaki, Takuya

AU - Ishikawa, Tomoe

AU - Abe, Reimi

AU - Nakayama, Ryota

AU - Asada, Akiko

AU - Matsuki, Norio

AU - Ikegaya, Yuji

PY - 2014/7/1

Y1 - 2014/7/1

N2 - Astrocytes are thought to detect neuronal activity in the form of intracellular calcium elevations; thereby, astrocytes can regulate neuronal excitability and synaptic transmission. Little is known, however, about how the astrocyte calcium signal regulates the activity of neuronal populations. In this study, we addressed this issue using functional multineuron calcium imaging in hippocampal slice cultures. Under normal conditions, CA3 neuronal networks exhibited temporally correlated activity patterns, occasionally generating large synchronization among a subset of cells. The synchronized neuronal activity was correlated with astrocyte calcium events. Calcium buffering by an intracellular injection of a calcium chelator into multiple astrocytes reduced the synaptic strength of unitary transmission between pairs of surrounding pyramidal cells and caused desynchronization of the neuronal networks. Uncaging the calcium in the astrocytes increased the frequency of neuronal synchronization. These data suggest an essential role of the astrocyte calcium signal in the maintenance of basal neuronal function at the circuit level.

AB - Astrocytes are thought to detect neuronal activity in the form of intracellular calcium elevations; thereby, astrocytes can regulate neuronal excitability and synaptic transmission. Little is known, however, about how the astrocyte calcium signal regulates the activity of neuronal populations. In this study, we addressed this issue using functional multineuron calcium imaging in hippocampal slice cultures. Under normal conditions, CA3 neuronal networks exhibited temporally correlated activity patterns, occasionally generating large synchronization among a subset of cells. The synchronized neuronal activity was correlated with astrocyte calcium events. Calcium buffering by an intracellular injection of a calcium chelator into multiple astrocytes reduced the synaptic strength of unitary transmission between pairs of surrounding pyramidal cells and caused desynchronization of the neuronal networks. Uncaging the calcium in the astrocytes increased the frequency of neuronal synchronization. These data suggest an essential role of the astrocyte calcium signal in the maintenance of basal neuronal function at the circuit level.

UR - http://www.scopus.com/inward/record.url?scp=84903591527&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84903591527&partnerID=8YFLogxK

U2 - 10.1113/jphysiol.2014.272864

DO - 10.1113/jphysiol.2014.272864

M3 - Article

C2 - 24710057

AN - SCOPUS:84903591527

VL - 592

SP - 2771

EP - 2783

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

IS - 13

ER -