Metabolic and Hemodynamic Events after Changes in Neuronal Activity: Current Hypotheses, Theoretical Predictions and in vivo NMR Experimental Findings

Mangia, Silvia; Giove, Federico; Tkáč, Ivan; Logothetis, Nikos K; Henry, Pierre-Gilles; Olman, Cheryl A; Maraviglia, Bruno; Di Salle, Francesco; Uğurbil, Kâmil

doi:10.1038/jcbfm.2008.134

Cited by 161Advanced MRI Techniques and ApplicationsNeuroscience and Neuropharmacology ResearchMetabolomics and Mass Spectrometry Studies

Metabolic and Hemodynamic Events after Changes in Neuronal Activity: Current Hypotheses, Theoretical Predictions and in vivo NMR Experimental Findings

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Mangia, Silvia, Giove, Federico, Tkáč, Ivan, Logothetis, Nikos K, Henry, Pierre-Gilles, Olman, Cheryl A, Maraviglia, Bruno, Di Salle, Francesco +1 more·2009·Journal of Cerebral Blood Flow & Metabolism

DOI 10.1038/jcbfm.2008.134PMC PMC2743443

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Abstract

Unraveling the energy metabolism and the hemodynamic outcomes of excitatory and inhibitory neuronal activity is critical not only for our basic understanding of overall brain function, but also for the understanding of many brain disorders. Methodologies of magnetic resonance spectroscopy (MRS) and magnetic resonance imaging (MRI) are powerful tools for the noninvasive investigation of brain metabolism and physiology. However, the temporal and spatial resolution of in vivo MRS and MRI is not suitable to provide direct evidence for hypotheses that involve metabolic compartmentalization between different cell types, or to untangle the complex neuronal microcircuitry, which results in changes of electrical activity. This review aims at describing how the current models of brain metabolism, mainly built on the basis of in vitro evidence, relate to experimental findings recently obtained in vivo by 1 H MRS, 13 C MRS, and MRI. The hypotheses related to the role of different metabolic substrates, the metabolic neuron—glia interactions, along with the available theoretical predictions of the energy budget of neurotransmission will be discussed. In addition, the cellular and network mechanisms that characterize different types of increased and suppressed neuronal activity will be considered within the sensitivity-constraints of MRS and MRI.

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The metabolic response to stimulation includes an oxidative component (CMRO2) and a nonoxidative component (lactate accumulation).
“The metabolic response to stimulation includes an oxidative component, as measured by the cerebral metabolic rate of oxygen (CMRO2), and a nonoxidative component, as reflected by lactate accumulation (Mangia et al., 2009).”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Mangia et al., 2009
Section B.3 reports both increased oxygen consumption and lactate accumulation during stimulation. But it interprets the observed lactate increase as consistent with increased oxidative metabolism, not as a measure of a nonoxidative component. No page number is available in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measured
An overall switch toward inhibition is expected to reduce the energy request of the brain, thus impacting on metabolic rates independently of BOLD response.
“In fact, an overall switch toward inhibition is expected to reduce the energy request of the brain, thus impacting on metabolic rates independently of BOLD response (Mangia et al., 2009).”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Mangia et al., 2009
Section F.4 predicts that increased inhibition lowers energy demand in the neocortex and reports a change in lactate response despite a persistent BOLD response. But the claim extends that prediction to the brain generally; section F.2 describes cases in which inhibitory activity increased energy consumption. (LLM, conf=0.85)
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The relative metabolic demand of inhibition and excitation
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Competition between glucose and lactate as oxidative energy substrates in both neurons and astrocytes: a comparative NMR study
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“Additionally, studies performed with real-time confocal microscopy indicated that glutamate stimulates glucose transporters in cultured hippocampal astrocytes (Loaiza et al, 2003), and inhibits glucose transporters in hippocampal neurons (Porras et al, 2004).”
Relationship of spikes, synaptic activity, and local changes of cerebral blood flow
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Do active cerebral neurons really use lactate rather than glucose?
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“Notably, linking glucose consumptions in an B1:1 way with the Glu–Gln cycle in the context of the ANLSH implicitly neglects the intervention of neuronal glutamate uptake, which occurs during neurotransmission (Bak et al, 2006; Danbolt, 2001; Drejer et al, 1982; Waagepetersen et al, 2005).”
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Ultrahigh field magnetic resonance imaging and spectroscopy
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Increased glucose metabolism during long-duration recurrent inhibition of hippocampal pyramidal cells
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Stimulation‐induced [14C]2‐deoxyglucose labeling of synaptic activity in the central auditory system
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Brain lactate kinetics: Modeling evidence for neuronal lactate uptake upon activation
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How accurate is magnetic resonance imaging of brain function?
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Proton T2 relaxation study of water, N‐acetylaspartate, and creatine in human brain using Hahn and Carr‐Purcell spin echoes at 4T and 7T
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Evidence for the Mitochondrial Lactate Oxidation Complex in Rat Neurons: Demonstration of an Essential Component of Brain Lactate Shuttles
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Food for Thought: Challenging the Dogmas
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Assignment of the water slow-diffusing component in the central nervous system using q-space diffusion MRS: Implications for fiber tract imaging
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GABA uptake into astrocytes is not associated with significant metabolic cost: Implications for brain imaging of inhibitory transmission
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Glucose is Necessary to Maintain Neurotransmitter Homeostasis during Synaptic Activity in Cultured Glutamatergic Neurons
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Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex
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Nutrition during brain activation: does cell-to-cell lactate shuttling contribute significantly to sweet and sour food for thought?
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In vivo 1 H‐[ 13 C]‐NMR spectroscopy of cerebral metabolism
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Direct in vivo measurement of human cerebral GABA concentration using MEGA‐editing at 7 Tesla
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Generalized Sensory Stimulation of Conscious Rats Increases Labeling of Oxidative Pathways of Glucose Metabolism When the Brain Glucose???Oxygen Uptake Ratio Rises
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Selective Uptake of [ 14 C]2-Deoxyglucose by Neurons and Astrocytes: High-Resolution Microautoradiographic Imaging by Cellular 14 C-Trajectography Combined with Immunohistochemistry
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Du F Zhang Y Friedman M Zhu XH Ugurbil K Chen W Study of correlation between brain activity and ATP metabolic rates by means of 31P magnetization transfer and electroencephalograph measurement 2006 2125 Proceedings Meeting International Society Magnetic Resonance in Medicine Seattle
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Authors: Mangia, S., Giove, F., Tkáč, I., Logothetis, N. K., Henry, P.-G., Olman, C. A., Maraviglia, B., Di Salle, F., & Uğurbil, K.
Affiliations: University of Minnesota (US)
Centro Ricerche Enrico Fermi (IT)
Max Planck Institute for Biological Cybernetics (DE)
Department of Neuroscience, University of Pisa, Pisa, Italy
Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, Minneapolis, Minnesota, USA
Corresponding author: Mangia, Silvia
ORCID: Mangia, Silvia
Giove, Federico
Tkáč, Ivan
Logothetis, Nikos K
Henry, Pierre-Gilles
Olman, Cheryl A
Maraviglia, Bruno
Venue: Journal of Cerebral Blood Flow & Metabolism
Publisher: SAGE Publications
Published: 2008-11-12
Volume: 29
Issue: 3
Pages: 441-463
ISSN: 0271-678X (ISSN-L)
1559-7016
DOI: 10.1038/jcbfm.2008.134
PMC: PMC2743443
OpenAlex: W2168128459
Cited by: 161
References: 197
Citations by year: 2026: 4 · 2025: 5 · 2024: 5 · 2023: 6 · 2022: 9 · 2021: 3 · 2020: 6 · 2019: 6 · 2018: 11 · 2017: 7 · 2016: 8 · 2015: 8 · 2014: 11 · 2013: 9 · 2012: 19
FWCI: 1.97
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.sagepub.com/page/policies/text-and-data-mining-license (tdm)
Locations: Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Research Publications (Maastricht University) (submittedVersion, other-oa)
Max Planck Institute for Plasma Physics (submittedVersion)
IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
Research Explorer (The University of Manchester) (submittedVersion)
Funders: W. M. Keck Foundation
National Institutes of Health
National Institute of Neurological Disorders and Stroke (R01 NS 38672, R01NS038672, P30NS057091)
National Center for Research Resources (P41RR008079, P41RR08079)
Topics: Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Keywords: brain energy metabolism, neuronal activity, excitatory and inhibitory neurons, metabolic compartmentation, neuron-glia interactions, cerebral blood flow, hemodynamics, 1H magnetic resonance spectroscopy, 13C NMR, in vivo brain imaging
MeSH terms: Animals, Brain, Energy Metabolism, Glucose, Humans, Lactates, Magnetic Resonance Imaging, Microcirculation, Models, Neurological, Synaptic Transmission, Neurons, Magnetic Resonance Spectroscopy, Oxidation-Reduction, Sensitivity and Specificity, Vasodilation

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Metabolic and Hemodynamic Events after Changes in Neuronal Activity: Current Hypotheses, Theoretical Predictions and in vivo NMR Experimental Findings

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