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Astrocytic and neuronal oxidative metabolism are coupled to the rate of glutamate–glutamine cycle in the tree shrew visual cortex
Author(s) -
Sonnay Sarah,
Poirot Jordan,
Just Nathalie,
Clerc AnneCatherine,
Gruetter Rolf,
Rainer Gregor,
Duarte João M. N.
Publication year - 2018
Publication title -
glia
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.954
H-Index - 164
eISSN - 1098-1136
pISSN - 0894-1491
DOI - 10.1002/glia.23259
Subject(s) - glutamatergic , glutamine , biology , glutamate receptor , neurotransmission , phosphocreatine , glutamic acid , stimulation , neuroscience , medicine , endocrinology , biochemistry , energy metabolism , amino acid , receptor
Astrocytes play an important role in glutamatergic neurotransmission, namely by clearing synaptic glutamate and converting it into glutamine that is transferred back to neurons. The rate of this glutamate–glutamine cycle (V NT ) has been proposed to couple to that of glucose utilization and of neuronal tricarboxylic acid (TCA) cycle. In this study, we tested the hypothesis that glutamatergic neurotransmission is also coupled to the TCA cycle rate in astrocytes. For that we investigated energy metabolism by means of magnetic resonance spectroscopy (MRS) in the primary visual cortex of tree shrews ( Tupaia belangeri ) under light isoflurane anesthesia at rest and during continuous visual stimulation. After identifying the activated cortical volume by blood oxygenation level‐dependent functional magnetic resonance imaging, 1 H MRS was performed to measure stimulation‐induced variations in metabolite concentrations. Relative to baseline, stimulation of cortical activity for 20 min caused a reduction of glucose concentration by −0.34 ± 0.09 µmol/g ( p < 0.001), as well as a −9% ± 1% decrease of the ratio of phosphocreatine‐to‐creatine ( p < 0.05). Then 13 C MRS during [1,6‐ 13 C]glucose infusion was employed to measure fluxes of energy metabolism. Stimulation of glutamatergic activity, as indicated by a 20% increase of V NT , resulted in increased TCA cycle rates in neurons by 12% ( V TCAn , p < 0.001) and in astrocytes by 24% ( V TCAg , p = 0.007). We further observed linear relationships between V NT and bothV TCAn andV TCAg . Altogether, these results suggest that in the tree shrew primary visual cortex glutamatergic neurotransmission is linked to overall glucose oxidation and to mitochondrial metabolism in both neurons and astrocytes.