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13 C MRS studies of neuroenergetics and neurotransmitter cycling in humans

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Rothman, Douglas L., De Feyter, Henk M., de Graaf, Robin A., Mason, Graeme F., Behar, Kevin L.·2011·NMR in Biomedicine

DOI 10.1002/nbm.1772PMC PMC3651027

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Abstract

In the last 25 years, 13 C MRS has been established as the only noninvasive method for the measurement of glutamate neurotransmission and cell‐specific neuroenergetics. Although technically and experimentally challenging, 13 C MRS has already provided important new information on the relationship between neuroenergetics and neuronal function, the energy cost of brain function, the high neuronal activity in the resting brain state and how neuroenergetics and neurotransmitter cycling are altered in neurological and psychiatric disease. In this article, the current state of 13 C MRS as it is applied to the study of neuroenergetics and neurotransmitter cycling in humans is reviewed. The focus is predominantly on recent findings in humans regarding metabolic pathways, applications to clinical research and the technical status of the method. Results from in vivo 13 C MRS studies in animals are discussed from the standpoint of the validation of MRS measurements of neuroenergetics and neurotransmitter cycling, and where they have helped to identify key questions to address in human research. Controversies concerning the relationship between neuroenergetics and neurotransmitter cycling and factors having an impact on the accurate determination of fluxes through mathematical modeling are addressed. We further touch upon different 13 C‐labeled substrates used to study brain metabolism, before reviewing a number of human brain diseases investigated using 13 C MRS. Future technological developments are discussed that will help to overcome the limitations of 13 C MRS, with special attention given to recent developments in hyperpolarized 13 C MRS. Copyright © 2011 John Wiley & Sons, Ltd.

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Lin, M. T., & Beal, M. F. (2006) · Nature · doi:10.1038/nature05292 · Cited by 6,455
The Synaptic Organization of the Brain
(2004) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195159561.001.1 · Cited by 3,574
An Energy Budget for Signaling in the Grey Matter of the Brain
Attwell, D., & Laughlin, S. B. (2001) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200110000-00001 · Cited by 3,543
Knockout of Glutamate Transporters Reveals a Major Role for Astroglial Transport in Excitotoxicity and Clearance of Glutamate
Rothstein, J. D., Dykes-Hoberg, M., Pardo, C. A., Bristol, L. A., Jin, L., Kuncl, R. W., Kanai, Y., Hediger, M. A., Wang, Y., Schielke, J. P., et al. (1996) · Neuron · doi:10.1016/s0896-6273(00)80086-0 · Cited by 2,534
Nonoxidative Glucose Consumption During Focal Physiologic Neural Activity
Fox, P. T., Raichle, M. E., Mintun, M. A., & Dence, C. (1988) · Science · doi:10.1126/science.3260686 · Cited by 1,796
Brain Metabolism during Fasting*
Owen, O. E., Morgan, A. P., Kemp, H. G., Sullivan, J. M., Herrera, M. G., & Cahill, G. F. (1967) · Journal of Clinical Investigation · doi:10.1172/jci105650 · Cited by 1,662
Brain energy metabolism
Siesjö, B. K. (1978) · Medical Entomology and Zoology · Cited by 1,426
Energy on demand.
Magistretti, P. J., Pellerin, L., Rothman, D. L., & Shulman, R. G. (1999) · Science · doi:10.1126/science.283.5401.496 · Cited by 1,170
Self-citation
The release and uptake of excitatory amino acids
Nicholls, D. G., & Attwell, D. (1990) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(90)90129-v · Cited by 1,092
Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity.
Sibson, N. R., Dhankhar, A., Mason, G. F., Rothman, D. L., Behar, K. L., & Shulman, R. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.1.316 · Cited by 897
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Authors: Rothman, D. L., De Feyter, H. M., de Graaf, R. A., Mason, G. F., & Behar, K. L.
Affiliations: Yale University (US)
Department of Diagnostic Radiology, Magnetic Resonance Research Center Yale University School of Medicine New Haven CT USA
Corresponding author: Rothman, Douglas L.
ORCID: Rothman, Douglas L.
Mason, Graeme F.
Behar, Kevin L.
Venue: NMR in Biomedicine
Publisher: Wiley
Published: 2011-08-31
Volume: 24
Issue: 8
Pages: 943-957
ISSN: 0952-3480 (ISSN-L)
1099-1492
DOI: 10.1002/nbm.1772
PMC: PMC3651027
OpenAlex: W2147937603
Cited by: 290
References: 156
Citations by year: 2026: 18 · 2025: 16 · 2024: 17 · 2023: 11 · 2022: 15 · 2021: 40 · 2020: 14 · 2019: 16 · 2018: 21 · 2017: 26 · 2016: 27 · 2015: 14 · 2014: 24 · 2013: 20 · 2012: 10
FWCI: 2.82
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: NMR in Biomedicine (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (1r01mh095104-01, R01-EB000473)
National Institute on Alcohol Abuse and Alcoholism (R21AA018210, R21AA019803)
National Institute on Aging (R01AG034953)
National Institute of Mental Health (R01-MH95104, R01-MH095104)
National Institute on Drug Abuse (R01DA021785)
National Institute of Diabetes and Digestive and Kidney Diseases (R01DK027121)
National Institute of Neurological Disorders and Stroke (P30NS052519)
National Institute of Biomedical Imaging and Bioengineering (R01EB000473, R01EB009336, R41EB008296)
Topics: Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Physical Sciences › Chemistry › Spectroscopy › Advanced NMR Techniques and Applications
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Keywords: 13C NMR, neuroenergetics, glutamatergic neurotransmission, brain energy metabolism, metabolic flux, hyperpolarized 13C, 13C-labeled substrates, brain disorders, resting-state brain activity, in vivo brain metabolism
MeSH terms: Aging, Alzheimer Disease, Animals, Brain, Carbon Isotopes, Citric Acid Cycle, Energy Metabolism, Glutamine, Humans, Neurons, Magnetic Resonance Spectroscopy, Neurotransmitter Agents, Glutamic Acid

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13 C MRS studies of neuroenergetics and neurotransmitter cycling in humans

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