Optogenetic astrocyte activation evokes BOLD fMRI response with oxygen consumption without neuronal activity modulation

Norio Takata, Yuki Sugiura, Keitaro Yoshida, Miwako Koizumi, Nishida Hiroshi, Kurara Honda, Ryutaro Yano, Yuji Komaki, Ko Matsui, Makoto Suematsu, Masaru Mimura, Hideyuki Okano, Kenji Tanaka

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Functional magnetic resonance imaging (fMRI) based on the blood oxygenation level-dependent (BOLD) signal has been used to infer sites of neuronal activation in the brain. A recent study demonstrated, however, unexpected BOLD signal generation without neuronal excitation, which led us to hypothesize the presence of another cellular source for BOLD signal generation. Collective assessment of optogenetic activation of astrocytes or neurons, fMRI in awake mice, electrophysiological measurements, and histochemical detection of neuronal activation, coherently suggested astrocytes as another cellular source. Unexpectedly, astrocyte-evoked BOLD signal accompanied oxygen consumption without modulation of neuronal activity. Imaging mass spectrometry of brain sections identified synthesis of acetyl-carnitine via oxidative glucose metabolism at the site of astrocyte-, but not neuron-evoked BOLD signal. Our data provide causal evidence that astrocytic activation alone is able to evoke BOLD signal response, which may lead to reconsideration of current interpretation of BOLD signal as a marker of neuronal activation.

Original languageEnglish
Pages (from-to)2013-2023
Number of pages11
JournalGLIA
Volume66
Issue number9
DOIs
Publication statusPublished - 2018 Sep 1

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Optogenetics
Oxygen Consumption
Astrocytes
Magnetic Resonance Imaging
Acetylcarnitine
Neurons
Brain
Mass Spectrometry
Glucose

Keywords

  • astrocytes
  • BOLD
  • fMRI
  • imaging mass spectrometry
  • optogenetics

ASJC Scopus subject areas

  • Neurology
  • Cellular and Molecular Neuroscience

Cite this

Optogenetic astrocyte activation evokes BOLD fMRI response with oxygen consumption without neuronal activity modulation. / Takata, Norio; Sugiura, Yuki; Yoshida, Keitaro; Koizumi, Miwako; Hiroshi, Nishida; Honda, Kurara; Yano, Ryutaro; Komaki, Yuji; Matsui, Ko; Suematsu, Makoto; Mimura, Masaru; Okano, Hideyuki; Tanaka, Kenji.

In: GLIA, Vol. 66, No. 9, 01.09.2018, p. 2013-2023.

Research output: Contribution to journalArticle

Takata, N, Sugiura, Y, Yoshida, K, Koizumi, M, Hiroshi, N, Honda, K, Yano, R, Komaki, Y, Matsui, K, Suematsu, M, Mimura, M, Okano, H & Tanaka, K 2018, 'Optogenetic astrocyte activation evokes BOLD fMRI response with oxygen consumption without neuronal activity modulation', GLIA, vol. 66, no. 9, pp. 2013-2023. https://doi.org/10.1002/glia.23454
Takata, Norio ; Sugiura, Yuki ; Yoshida, Keitaro ; Koizumi, Miwako ; Hiroshi, Nishida ; Honda, Kurara ; Yano, Ryutaro ; Komaki, Yuji ; Matsui, Ko ; Suematsu, Makoto ; Mimura, Masaru ; Okano, Hideyuki ; Tanaka, Kenji. / Optogenetic astrocyte activation evokes BOLD fMRI response with oxygen consumption without neuronal activity modulation. In: GLIA. 2018 ; Vol. 66, No. 9. pp. 2013-2023.
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