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Glia. 2018 Sep;66(9):2013-2023. doi: 10.1002/glia.23454. Epub 2018 May 30.

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

Author information

1
Department of Neuropsychiatry, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo, 160-8582, Japan.
2
Central Institute for Experimental Animals (CIEA), 3-25-12, Tonomachi, Kawasaki, Kanagawa, 210-0821, Japan.
3
Department of Biochemistry, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo, 160-8582, Japan.
4
Department of Physiology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo, 160-8582, Japan.
5
Super-network Brain Physiology, Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi, 980-8575, Japan.
6
Laboratory for Marmoset Neural Architecture, RIKEN Brain Science Institute, Wako, Saitama, 351-0198, Japan.

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.

KEYWORDS:

BOLD; astrocytes; fMRI; imaging mass spectrometry; optogenetics

PMID:
29845643
DOI:
10.1002/glia.23454

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