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Compartmentalised energy metabolism supporting glutamatergic neurotransmission in response to increased activity in the rat cerebral cortex : A 13C MRS study in vivo at 14.1 T

Sonnay, Sarah LU ; Duarte, João Mn LU orcid ; Just, Nathalie and Gruetter, Rolf (2016) In Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism 36(5). p.40-928
Abstract

Many tissues exhibit metabolic compartmentation. In the brain, while there is no doubt on the importance of functional compartmentation between neurons and glial cells, there is still debate on the specific regulation of pathways of energy metabolism at different activity levels. Using (13)C magnetic resonance spectroscopy (MRS) in vivo, we determined fluxes of energy metabolism in the rat cortex under α-chloralose anaesthesia at rest and during electrical stimulation of the paws. Compared to resting metabolism, the stimulated rat cortex exhibited increased glutamate-glutamine cycle (+67 nmol/g/min, +95%, P < 0.001) and tricarboxylic (TCA) cycle rate in both neurons (+62 nmol/g/min, +12%, P < 0.001) and astrocytes (+68 nmol/g/min,... (More)

Many tissues exhibit metabolic compartmentation. In the brain, while there is no doubt on the importance of functional compartmentation between neurons and glial cells, there is still debate on the specific regulation of pathways of energy metabolism at different activity levels. Using (13)C magnetic resonance spectroscopy (MRS) in vivo, we determined fluxes of energy metabolism in the rat cortex under α-chloralose anaesthesia at rest and during electrical stimulation of the paws. Compared to resting metabolism, the stimulated rat cortex exhibited increased glutamate-glutamine cycle (+67 nmol/g/min, +95%, P < 0.001) and tricarboxylic (TCA) cycle rate in both neurons (+62 nmol/g/min, +12%, P < 0.001) and astrocytes (+68 nmol/g/min, +22%, P = 0.072). A minor, non-significant modification of the flux through pyruvate carboxylase was observed during stimulation (+5 nmol/g/min, +8%). Altogether, this increase in metabolism amounted to a 15% (67 nmol/g/min, P < 0.001) increase in CMRglc(ox), i.e. the oxidative fraction of the cerebral metabolic rate of glucose. In conclusion, stimulation of the glutamate-glutamine cycle under α-chloralose anaesthesia is associated to similar enhancement of neuronal and glial oxidative metabolism.

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author
; ; and
publishing date
type
Contribution to journal
publication status
published
keywords
Animals, Astrocytes, Carbon Isotopes, Cell Compartmentation, Cerebral Cortex, Electric Stimulation, Energy Metabolism, Glutamic Acid, Magnetic Resonance Imaging, Neuroglia, Neurons, Rats, Synaptic Transmission, Journal Article
in
Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism
volume
36
issue
5
pages
13 pages
publisher
Nature Publishing Group
external identifiers
  • pmid:26823472
  • scopus:84964974516
ISSN
1559-7016
DOI
10.1177/0271678X16629482
language
English
LU publication?
no
id
e1f067dd-6cf3-4625-ac52-34c016428ada
date added to LUP
2017-10-19 15:08:36
date last changed
2024-06-10 01:50:31
@article{e1f067dd-6cf3-4625-ac52-34c016428ada,
  abstract     = {{<p>Many tissues exhibit metabolic compartmentation. In the brain, while there is no doubt on the importance of functional compartmentation between neurons and glial cells, there is still debate on the specific regulation of pathways of energy metabolism at different activity levels. Using (13)C magnetic resonance spectroscopy (MRS) in vivo, we determined fluxes of energy metabolism in the rat cortex under α-chloralose anaesthesia at rest and during electrical stimulation of the paws. Compared to resting metabolism, the stimulated rat cortex exhibited increased glutamate-glutamine cycle (+67 nmol/g/min, +95%, P &lt; 0.001) and tricarboxylic (TCA) cycle rate in both neurons (+62 nmol/g/min, +12%, P &lt; 0.001) and astrocytes (+68 nmol/g/min, +22%, P = 0.072). A minor, non-significant modification of the flux through pyruvate carboxylase was observed during stimulation (+5 nmol/g/min, +8%). Altogether, this increase in metabolism amounted to a 15% (67 nmol/g/min, P &lt; 0.001) increase in CMRglc(ox), i.e. the oxidative fraction of the cerebral metabolic rate of glucose. In conclusion, stimulation of the glutamate-glutamine cycle under α-chloralose anaesthesia is associated to similar enhancement of neuronal and glial oxidative metabolism.</p>}},
  author       = {{Sonnay, Sarah and Duarte, João Mn and Just, Nathalie and Gruetter, Rolf}},
  issn         = {{1559-7016}},
  keywords     = {{Animals; Astrocytes; Carbon Isotopes; Cell Compartmentation; Cerebral Cortex; Electric Stimulation; Energy Metabolism; Glutamic Acid; Magnetic Resonance Imaging; Neuroglia; Neurons; Rats; Synaptic Transmission; Journal Article}},
  language     = {{eng}},
  number       = {{5}},
  pages        = {{40--928}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism}},
  title        = {{Compartmentalised energy metabolism supporting glutamatergic neurotransmission in response to increased activity in the rat cerebral cortex : A 13C MRS study in vivo at 14.1 T}},
  url          = {{http://dx.doi.org/10.1177/0271678X16629482}},
  doi          = {{10.1177/0271678X16629482}},
  volume       = {{36}},
  year         = {{2016}},
}