Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Fahmeed Hyder; Peter Herman; Christopher J. Bailey; Arne Møller; Ronen Globinsky; Robert K Fulbright; Douglas L Rothman; Albert Gjedde

doi:10.1177/0271678x15625349

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Fahmeed Hyder, Peter Herman, Christopher J. Bailey, Arne Møller, Ronen Globinsky, Robert K Fulbright, Douglas L Rothman, Albert Gjedde

Department of Neuroscience

36 Citations (Scopus)

Abstract

Regionally variable rates of aerobic glycolysis in brain networks identified by resting-state functional magnetic resonance imaging (R-fMRI) imply regionally variable adenosine triphosphate (ATP) regeneration. When regional glucose utilization is not matched to oxygen delivery, affected regions have correspondingly variable rates of ATP and lactate production. We tested the extent to which aerobic glycolysis and oxidative phosphorylation power R-fMRI networks by measuring quantitative differences between the oxygen to glucose index (OGI) and the oxygen extraction fraction (OEF) as measured by positron emission tomography (PET) in normal human brain (resting awake, eyes closed). Regionally uniform and correlated OEF and OGI estimates prevailed, with network values that matched the gray matter means, regardless of size, location, and origin. The spatial agreement between oxygen delivery (OEFâ ‰-0.4) and glucose oxidation (OGI â ‰- 5.3) suggests that no specific regions have preferentially high aerobic glycolysis and low oxidative phosphorylation rates, with globally optimal maximum ATP turnover rates (V ATP â ‰- 9.4 μmol/g/min), in good agreement with 31 P and 13 C magnetic resonance spectroscopy measurements. These results imply that the intrinsic network activity in healthy human brain powers the entire gray matter with ubiquitously high rates of glucose oxidation. Reports of departures from normal brain-wide homogeny of oxygen extraction fraction and oxygen to glucose index may be due to normalization artefacts from relative PET measurements.

Original language	English
Journal	Journal of Cerebral Blood Flow and Metabolism
Volume	36
Issue number	5
Pages (from-to)	903-916
Number of pages	14
ISSN	0271-678X
DOIs	https://doi.org/10.1177/0271678x15625349
Publication status	Published - 2015

Keywords

Adenosine Triphosphate/metabolism
Brain/metabolism
Glucose/analysis
Glycolysis/physiology
Gray Matter/metabolism
Humans
Magnetic Resonance Imaging
Male
Oxidation-Reduction
Oxidative Phosphorylation
Oxygen/analysis
Positron-Emission Tomography

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1177/0271678x15625349

0271678X15625349Final published version, 1.8 MB

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Hyder, F., Herman, P., Bailey, C. J., Møller, A., Globinsky, R., Fulbright, R. K., Rothman, D. L., & Gjedde, A. (2015). Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis. Journal of Cerebral Blood Flow and Metabolism, 36(5), 903-916. https://doi.org/10.1177/0271678x15625349

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain : No evidence of regional differences of aerobic glycolysis. / Hyder, Fahmeed; Herman, Peter; Bailey, Christopher J. et al.

In: Journal of Cerebral Blood Flow and Metabolism, Vol. 36, No. 5, 2015, p. 903-916.

Research output: Contribution to journal › Journal article › Research › peer-review

Hyder, F, Herman, P, Bailey, CJ, Møller, A, Globinsky, R, Fulbright, RK, Rothman, DL & Gjedde, A 2015, 'Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis', Journal of Cerebral Blood Flow and Metabolism, vol. 36, no. 5, pp. 903-916. https://doi.org/10.1177/0271678x15625349

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abstract = "Regionally variable rates of aerobic glycolysis in brain networks identified by resting-state functional magnetic resonance imaging (R-fMRI) imply regionally variable adenosine triphosphate (ATP) regeneration. When regional glucose utilization is not matched to oxygen delivery, affected regions have correspondingly variable rates of ATP and lactate production. We tested the extent to which aerobic glycolysis and oxidative phosphorylation power R-fMRI networks by measuring quantitative differences between the oxygen to glucose index (OGI) and the oxygen extraction fraction (OEF) as measured by positron emission tomography (PET) in normal human brain (resting awake, eyes closed). Regionally uniform and correlated OEF and OGI estimates prevailed, with network values that matched the gray matter means, regardless of size, location, and origin. The spatial agreement between oxygen delivery (OEF{\^a} ‰-0.4) and glucose oxidation (OGI {\^a} ‰- 5.3) suggests that no specific regions have preferentially high aerobic glycolysis and low oxidative phosphorylation rates, with globally optimal maximum ATP turnover rates (V ATP {\^a} ‰- 9.4 μmol/g/min), in good agreement with 31 P and 13 C magnetic resonance spectroscopy measurements. These results imply that the intrinsic network activity in healthy human brain powers the entire gray matter with ubiquitously high rates of glucose oxidation. Reports of departures from normal brain-wide homogeny of oxygen extraction fraction and oxygen to glucose index may be due to normalization artefacts from relative PET measurements.",

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T1 - Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain

T2 - No evidence of regional differences of aerobic glycolysis

AU - Hyder, Fahmeed

AU - Herman, Peter

AU - Bailey, Christopher J.

AU - Møller, Arne

AU - Globinsky, Ronen

AU - Fulbright, Robert K

AU - Rothman, Douglas L

AU - Gjedde, Albert

N1 - © The Author(s) 2016.

PY - 2015

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N2 - Regionally variable rates of aerobic glycolysis in brain networks identified by resting-state functional magnetic resonance imaging (R-fMRI) imply regionally variable adenosine triphosphate (ATP) regeneration. When regional glucose utilization is not matched to oxygen delivery, affected regions have correspondingly variable rates of ATP and lactate production. We tested the extent to which aerobic glycolysis and oxidative phosphorylation power R-fMRI networks by measuring quantitative differences between the oxygen to glucose index (OGI) and the oxygen extraction fraction (OEF) as measured by positron emission tomography (PET) in normal human brain (resting awake, eyes closed). Regionally uniform and correlated OEF and OGI estimates prevailed, with network values that matched the gray matter means, regardless of size, location, and origin. The spatial agreement between oxygen delivery (OEFâ ‰-0.4) and glucose oxidation (OGI â ‰- 5.3) suggests that no specific regions have preferentially high aerobic glycolysis and low oxidative phosphorylation rates, with globally optimal maximum ATP turnover rates (V ATP â ‰- 9.4 μmol/g/min), in good agreement with 31 P and 13 C magnetic resonance spectroscopy measurements. These results imply that the intrinsic network activity in healthy human brain powers the entire gray matter with ubiquitously high rates of glucose oxidation. Reports of departures from normal brain-wide homogeny of oxygen extraction fraction and oxygen to glucose index may be due to normalization artefacts from relative PET measurements.

AB - Regionally variable rates of aerobic glycolysis in brain networks identified by resting-state functional magnetic resonance imaging (R-fMRI) imply regionally variable adenosine triphosphate (ATP) regeneration. When regional glucose utilization is not matched to oxygen delivery, affected regions have correspondingly variable rates of ATP and lactate production. We tested the extent to which aerobic glycolysis and oxidative phosphorylation power R-fMRI networks by measuring quantitative differences between the oxygen to glucose index (OGI) and the oxygen extraction fraction (OEF) as measured by positron emission tomography (PET) in normal human brain (resting awake, eyes closed). Regionally uniform and correlated OEF and OGI estimates prevailed, with network values that matched the gray matter means, regardless of size, location, and origin. The spatial agreement between oxygen delivery (OEFâ ‰-0.4) and glucose oxidation (OGI â ‰- 5.3) suggests that no specific regions have preferentially high aerobic glycolysis and low oxidative phosphorylation rates, with globally optimal maximum ATP turnover rates (V ATP â ‰- 9.4 μmol/g/min), in good agreement with 31 P and 13 C magnetic resonance spectroscopy measurements. These results imply that the intrinsic network activity in healthy human brain powers the entire gray matter with ubiquitously high rates of glucose oxidation. Reports of departures from normal brain-wide homogeny of oxygen extraction fraction and oxygen to glucose index may be due to normalization artefacts from relative PET measurements.

KW - Adenosine Triphosphate/metabolism

KW - Brain/metabolism

KW - Glucose/analysis

KW - Glycolysis/physiology

KW - Gray Matter/metabolism

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Oxidation-Reduction

KW - Oxidative Phosphorylation

KW - Oxygen/analysis

KW - Positron-Emission Tomography

U2 - 10.1177/0271678x15625349

DO - 10.1177/0271678x15625349

M3 - Journal article

C2 - 26755443

SN - 0271-678X

VL - 36

SP - 903

EP - 916

JO - Journal of Cerebral Blood Flow and Metabolism

JF - Journal of Cerebral Blood Flow and Metabolism

IS - 5

ER -

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Abstract

Keywords

UN SDGs

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