13 C MRS studies of neuroenergetics and neurotransmitter cycling in humans

Rothman, Douglas L.; De Feyter, Henk M.; de Graaf, Robin A.; Mason, Graeme F.; Behar, Kevin L.

doi:10.1002/nbm.1772

Cited by 290Advanced MRI Techniques and ApplicationsAdvanced NMR Techniques and ApplicationsMetabolomics and Mass Spectrometry Studies

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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13C MRS is presently the only method that provides direct dynamic measurements of glutamate-glutamine cycling in the human brain.
“13 C MRS is presently the only method that provides direct dynamic measurements of glutamate-glutamine cycling in the human brain [10].”
From The effects of ketamine on prefrontal glutamate neurotransmission in healthy and depressed subjects (2018) · cites this paper as [10]
The Introduction says that following 13C label into glutamate and glutamine, combined with metabolic modeling, allows measurement of neurotransmitter cycling rates in the human brain. The Summary and Conclusions calls 13C MRS the only *non-invasive* method for measuring this cycling. The claim omits that qualification and describes the measurement as direct, whereas the paper says it depends on metabolic modeling. (LLM, conf=0.84)
Experimental — accuracy not yet measured
13C MRS is a unique, noninvasive method to measure neurotransmitter cycling and cell-specific neuroenergetics.
“Carbon-13 magnetic resonance spectroscopy ( 13 C MRS) is a unique, noninvasive method to measure neurotransmitter cycling and cell-specific neuroenergetics [8][9][10].”
From The effects of ketamine on prefrontal glutamate neurotransmission in healthy and depressed subjects (2018) · cites this paper as [10]
Glutamate enrichment primarily reflects oxidative energy production through the TCA cycle, while the rate of glutamine enrichment primarily reflects glutamate neurotransmitter cycling.
“Accordingly, the glutamate enrichment primarily reflects oxidative energy production through the TCA cycle, while the rate of glutamine enrichment primarily reflects glutamate neurotransmitter cycling [8,10].”
From The effects of ketamine on prefrontal glutamate neurotransmission in healthy and depressed subjects (2018) · cites this paper as [10]

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Glutamatergic Neurotransmission and Neuronal Glucose Oxidation are Coupled during Intense Neuronal Activation
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Clinical experience with 13C MRS in vivo
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Preliminary Evidence of Low Cortical GABA Levels in Localized1H-MR Spectra of Alcohol-Dependent and Hepatic Encephalopathy Patients
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Magnetic resonance spectroscopy of neurotransmitters in human brain
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Neurometabolism in human epilepsy
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Increased Brain Monocarboxylic Acid Transport and Utilization in Type 1 Diabetes
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Carbon-13 NMR for the assessment of human brain glucose metabolism in vivo
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Human Brain Glycogen Metabolism During and After Hypoglycemia
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Differentiation of Glucose Transport in Human Brain Gray and White Matter
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Detection of metabolites in rabbit brain by 13C NMR spectroscopy following administration of [1‐13C]glucose
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In vivo ^ C NMR measurements of cerebral synthesis as evidence for glutamate-glutamine cycling
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Feasibility of in vivo15N MRS detection of hyperpolarized 15N labeled choline in rats
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[2,4- 13 C 2 ]-β-Hydroxybutyrate Metabolism in Human Brain
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Measurement of human tricarboxylic acid cycle rates during visual activation by 13C magnetic resonance spectroscopy
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1 H NMR Studies of Glucose Transport in the Human Brain
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MR properties of rat sciatic nerve following trauma
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In vivo 13C spectroscopy in the rat brain using hyperpolarized [1-13C]pyruvate and [2-13C]pyruvate
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Regional glucose metabolism and glutamatergic neurotransmission in rat brain in vivo
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Localized in vivo 1H NMR detection of neurotransmitter labeling in rat brain during infusion of [1-13C] D-glucose
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Changes in Glucose Uptake Rather than Lactate Shuttle Take Center Stage in Subserving Neuroenergetics: Evidence from Mathematical Modeling
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Effects of Acute Hyperammonemia on Cerebral Amino Acid Metabolism and pHi In Vivo, Measured by 1H and 31P Nuclear Magnetic Resonance
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Evaluation of Cerebral Acetate Transport and Metabolic Rates in the Rat Brain in vivo Using 1 H-[ 13 C]-NMR
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Glutamatergic and GABAergic Neurotransmitter Cycling and Energy Metabolism in Rat Cerebral Cortex during Postnatal Development
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Deciphering neuron-glia compartmentalization in cortical energy metabolism
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Measurements of the anaplerotic rate in the human cerebral cortex using 13C magnetic resonance spectroscopy and [1‐13C] and [2‐13C] glucose
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Localized proton NMR observation of [3‐13C] lactate in stroke after [1‐13C] glucose infusion
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A comparison of 13C NMR measurements of the rates of glutamine synthesis and the tricarboxylic acid cycle during oral and intravenous administration of [1-13C]glucose
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1‐ 13 C glucose magnetic resonance spectroscopy of pediatric and adult brain disorders
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Measurement of the Tricarboxylic Acid Cycle Rate in Human Grey and White Matter in Vivo by 1 H-[ 13 C] Magnetic Resonance Spectroscopy at 4.1T
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Magnetic field homogenization of the human prefrontal cortex with a set of localized electrical coils
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Robust fully automated shimming of the human brain for high‐field 1H spectroscopic imaging
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MR Spectroscopy in Neurodegenerative Disease
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Lactate turnover in rat glioma measured by in vivo nuclear magnetic resonance spectroscopy.
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15N-NMR Spectroscopy Studies of Ammonia Transport and Glutamine Synthesis in the Hyperammonemic Rat Brain
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Portal-Systemic Encephalopathy: A Disorder of Neuron-Astrocytic Metabolic Trafficking
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Close Coupling between Astrocytic and Neuronal Metabolisms to Fulfill Anaplerotic and Energy Needs in the Rat Brain
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Changes of Blood Flow and Oxygen Consumption in Visual Cortex of Living Humans
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Facilitated transport of glucose from blood to brain in man and the effect of moderate hypoglycaemia on cerebral glucose utilization
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Astrocytes as the Glucose Shunt for Glutamatergic Neurons at High Activity: An In Silico Study
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In vivo 13C magnetic resonance spectroscopy of a human brain tumor after application of 13C-1-enriched glucose
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Basic principles of metabolic modeling of NMR 13C isotopic turnover to determine rates of brain metabolism in vivo
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In vivo evidence for reduced cortical glutamate–glutamine cycling in rats treated with the antidepressant/antipanic drug phenelzine
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[1‐ 13 C] glucose MRS in chronic hepatic encephalopathy in man
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Regional metabolite levels and turnover in the awake rat brain under the influence of nicotine
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Multimodal neuroimaging provides a highly consistent picture of energy metabolism, validating 31 P MRS for measuring brain ATP synthesis
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Sensitivity‐enhanced 13C MR spectroscopy of the human brain at 3 Tesla
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Proton MRS: GABA and glutamate.
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In vivo neurochemical profiling of rat brain by 1H‐[13C] NMR spectroscopy: cerebral energetics and glutamatergic/GABAergic neurotransmission
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Glial Dysfunction in Abstinent Methamphetamine Abusers
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Proposed cycles for functional glutamate trafficking in synaptic neurotransmission
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On the reliability of 13C metabolic modeling with two‐compartment neuronal‐glial models
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Cerebral pyruvate carboxylase flux is unaltered during bicuculline‐seizures
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Glial Alkalinization Detected In Vivo by 1H‐15N Heteronuclear Multiple‐Quantum Coherence‐Transfer NMR in Severely Hyperammonemic Rat
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Theoretical and experimental evaluation of broadband decoupling techniques for in vivo nuclear magnetic resonance spectroscopy
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Dynamically shimmed multivoxel 1H magnetic resonance spectroscopy and multislice magnetic resonance spectroscopic imaging of the human brain
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Alternative 1‐13C glucose infusion protocols for clinical 13C MRS examinations of the brain
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Neuroimaging and neuroenergetics: Brain activations as information-driven reorganization of energy flows
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Novel strategy for cerebral 13C MRS using very low RF power for proton decoupling
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Functional Brain Imaging in the Resting State and during Activation in Alzheimer's Disease: Implications for Disease Mechanisms Involving Oxidative Phosphorylation
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Determination of the Glutamate—Glutamine Cycling Flux Using Two-Compartment Dynamic Metabolic Modeling is Sensitive to Astroglial Dilution
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Glycolysis versus TCA Cycle in the Primate Brain as Measured by Combining 18 F-FDG PET and 13 C-NMR
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GABA Changes with Vigabatrin in the Developing Human Brain
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In vivo13C magnetic resonance spectroscopy of human brain on a clinical 3 T scanner using [2‐13C]glucose infusion and low‐power stochastic decoupling
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Measurement of cerebral oxidative glucose consumption in patients with type 1 diabetes mellitus and hypoglycemia unawareness using 13C nuclear magnetic resonance spectroscopy
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Direct carbon versus proton heteronuclear editing of 2‐13C ethanol in rabbit brain in vivo: A sensitivity comparison
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13C MRS of occipital and frontal lobes at 3 T using a volume coil for stochastic proton decoupling
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13C enrichment of extracellular neurotransmitter glutamate in rat brain--combined mass spectrometry and NMR studies of neurotransmitter turnover and uptake into glia in vivo.
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Ornithine Transcarbamylase Deficiency with Persistent Abnormality in Cerebral Glutamate Metabolism in Adults
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Graded image segmentation of brain tissue in the presence of inhomogeneous radio frequency fields
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Fast Isotopic Exchange between Mitochondria and Cytosol in Brain Revealed by Relayed 13C Magnetization Transfer Spectroscopy
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In Vivo NMR Spectroscopy Studies of Cerebral Metabolism in Rats after Portal-Caval Shunting.
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Effects of Hypercarbia and Porta-Caval Shunting on Amino Acids and High Energy Phosphates of the Rat Brain: a 1H and 31P NMR Study
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Untitled work
Wheeler-Kingshott (2000) · doi:10.1002/1522-2594(200011)44:5
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The Contribution of Ketone Bodies to Basal and Activity-Dependent Neuronal Oxidation in Vivo
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Anterior cingulate Glutamate–Glutamine cycle metabolites are altered in euthymic bipolar I disorder
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Glucose, Lactate, β-Hydroxybutyrate, Acetate, GABA, and Succinate as Substrates for Synthesis of Glutamate and GABA in the Glutamine–Glutamate/GABA Cycle
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Glutamine-Glutamate Cycle Flux Is Similar in Cultured Astrocytes and Brain and Both Glutamate Production and Oxidation Are Mainly Catalyzed by Aspartate Aminotransferase
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Role of Glycogenolysis in Memory and Learning: Regulation by Noradrenaline, Serotonin and ATP
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Glutamate in Pediatric Obsessive-Compulsive Disorder and Response to Cognitive-Behavioral Therapy: Randomized Clinical Trial
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Working Memory Modulates Glutamate Levels in the Dorsolateral Prefrontal Cortex during 1H fMRS
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Carbon (13C) MRS
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Rothman, Douglas L.: In Flux Veritas: Contributions to the Development of in vivo13C MRS
Rothman, D. L. (2011) · Encyclopedia of Magnetic Resonance · doi:10.1002/9780470034590.emrhp1067
Self-citation

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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