Dynamic functional imaging of brain glucose utilization using fPET-FDG

Villien, Marjorie; Wey, Hsiao-Ying; Mandeville, Joseph B.; Catana, Ciprian; Polimeni, Jonathan R.; Sander, Christin Y.; Zürcher, Nicole R.; Chonde, Daniel B.; Fowler, Joanna S.; Rosen, Bruce R.; Hooker, Jacob M.

doi:10.1016/j.neuroimage.2014.06.025

Title: Dynamic functional imaging of brain glucose utilization using fPET-FDG

Journal Article · Sat Jun 14 00:00:00 EDT 2014 · NeuroImage

DOI:https://doi.org/10.1016/j.neuroimage.2014.06.025· OSTI ID:1281964

Villien, Marjorie ^[1]; Wey, Hsiao-Ying ^[1]; Mandeville, Joseph B. ^[1]; Catana, Ciprian ^[1]; Polimeni, Jonathan R. ^[1]; Sander, Christin Y. ^[2]; Zürcher, Nicole R. ^[1]; Chonde, Daniel B. ^[1]; Fowler, Joanna S. ^[3]; Rosen, Bruce R. ^[4]; Hooker, Jacob M. ^[5]

Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology
Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology; Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Electrical Engineering and Computer Science
Brookhaven National Lab. (BNL), Upton, NY (United States). Biosciences Dept.
Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology; Harvard-Massachusetts Institute of Technology, Cambridge, MA (United States). Division of Health Sciences and Technology
Massachusetts General Hospital, Charlestown, MA (United States). Dept. of Radiology; Brookhaven National Lab. (BNL), Upton, NY (United States). Biosciences Dept.

We report that glucose is the principal source of energy for the brain and yet the dynamic response of glucose utilization to changes in brain activity is still not fully understood. Positron emission tomography (PET) allows quantitative measurement of glucose metabolism using 2-[18F]-fluorodeoxyglucose (FDG). However, FDG PET in its current form provides an integral (or average) of glucose consumption over tens of minutes and lacks the temporal information to capture physiological alterations associated with changes in brain activity induced by tasks or drug challenges. Traditionally, changes in glucose utilization are inferred by comparing two separate scans, which significantly limits the utility of the method. We report a novel method to track changes in FDG metabolism dynamically, with higher temporal resolution than exists to date and within a single session. Using a constant infusion of FDG, we demonstrate that our technique (termed fPET-FDG) can be used in an analysis pipeline similar to fMRI to define within-session differential metabolic responses. We use visual stimulation to demonstrate the feasibility of this method. Ultimately, this new method has a great potential to be used in research protocols and clinical settings since fPET-FDG imaging can be performed with most PET scanners and data acquisition and analysis are straightforward. fPET-FDG is a highly complementary technique to MRI and provides a rich new way to observe functional changes in brain metabolism.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH)

Grant/Contract Number:: SC0008430; P41EB015896; S10RR019933; R01EB014894

OSTI ID:: 1281964

Journal Information:: NeuroImage, Vol. 100, Issue C; ISSN 1053-8119

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 89 works

Citation information provided by
Web of Science

References (31)

Glucose Metabolic Rate Kinetic Model Parameter Determination in Humans: The Lumped Constants and Rate Constants for [ ¹⁸ F]Fluorodeoxyglucose and [ ¹¹ C]Deoxyglucose Reivich, M.; Alavi, A.; Wolf, A. Journal of Cerebral Blood Flow & Metabolism, Vol. 5, Issue 2 https://doi.org/10.1038/jcbfm.1985.24	journal	June 1985
Human brain glucose metabolism may evolve during activation: Findings from a modified FDG PET paradigm Vlassenko, Andrei G.; Rundle, Melissa M.; Mintun, Mark A. NeuroImage, Vol. 33, Issue 4 https://doi.org/10.1016/j.neuroimage.2006.06.065	journal	December 2006
Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Kwong, K. K.; Belliveau, J. W.; Chesler, D. A. Proceedings of the National Academy of Sciences, Vol. 89, Issue 12 https://doi.org/10.1073/pnas.89.12.5675	journal	June 1992
A Strategy for Removing the Bias in the Graphical Analysis Method Logan, Jean; Fowler, Joanna S.; Volkow, Nora D. Journal of Cerebral Blood Flow & Metabolism, Vol. 21, Issue 3 https://doi.org/10.1097/00004647-200103000-00014	journal	March 2001
Calibrated fMRI Hoge, Richard D. NeuroImage, Vol. 62, Issue 2 https://doi.org/10.1016/j.neuroimage.2012.02.022	journal	August 2012
Functional mapping of the human visual cortex by magnetic resonance imaging Belliveau, J.; Kennedy, D.; McKinstry, R. Science, Vol. 254, Issue 5032 https://doi.org/10.1126/science.1948051	journal	November 1991
FreeSurfer Fischl, Bruce NeuroImage, Vol. 62, Issue 2 https://doi.org/10.1016/j.neuroimage.2012.01.021	journal	August 2012
Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Ogawa, S.; Tank, D. W.; Menon, R. Proceedings of the National Academy of Sciences, Vol. 89, Issue 13 https://doi.org/10.1073/pnas.89.13.5951	journal	July 1992
The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Reivich, M.; Kuhl, D.; Wolf, A. Circulation Research, Vol. 44, Issue 1 https://doi.org/10.1161/01.RES.44.1.127	journal	January 1979
Comparison of Bolus and Infusion Methods for Receptor Quantitation: Application to [ ¹⁸ F]Cyclofoxy and Positron Emission Tomography Carson, Richard E.; Channing, Michael A.; Blasberg, Ronald G. Journal of Cerebral Blood Flow & Metabolism, Vol. 13, Issue 1 https://doi.org/10.1038/jcbfm.1993.6	journal	January 1993
Association between cerebral metabolic and structural abnormalities and cognitive performance in schizophrenia Molina, Vicente; Solera, Sara; Sanz, Javier Psychiatry Research: Neuroimaging, Vol. 173, Issue 2 https://doi.org/10.1016/j.pscychresns.2008.09.009	journal	August 2009
Changes in Relative Glucose Metabolic Rate Following Cortisol Administration in Aging Veterans with Posttraumatic Stress Disorder: An FDG-PET Neuroimaging Study Yehuda, Rachel; Harvey, Philip D.; Golier, Julia A. The Journal of Neuropsychiatry and Clinical Neurosciences, Vol. 21, Issue 2 https://doi.org/10.1176/jnp.2009.21.2.132	journal	April 2009
Mapping human visual cortex with positron emission tomography Fox, Peter T.; Mintun, Mark A.; Raichle, Marcus E. Nature, Vol. 323, Issue 6091 https://doi.org/10.1038/323806a0	journal	October 1986
Predicting efficacy of photodynamic therapy by real-time FDG-PET in a mouse tumour model Cauchon, Nicole; Turcotte, Eric; Lecomte, Roger Photochemical & Photobiological Sciences, Vol. 11, Issue 2 https://doi.org/10.1039/c1pp05294b	journal	January 2012
THE [ ¹⁴ C]DEOXYGLUCOSE METHOD FOR THE MEASUREMENT OF LOCAL CEREBRAL GLUCOSE UTILIZATION: THEORY, PROCEDURE, AND NORMAL VALUES IN THE CONSCIOUS AND ANESTHETIZED ALBINO RAT Sokoloff, L.; Reivich, M.; Kennedy, C. Journal of Neurochemistry, Vol. 28, Issue 5 https://doi.org/10.1111/j.1471-4159.1977.tb10649.x	journal	May 1977
Cerebral blood flow and glucose metabolism in healthy volunteers measured using a high-resolution PET scanner Huisman, Marc C.; van Golen, Larissa W.; Hoetjes, Nikie J. EJNMMI Research, Vol. 2, Issue 1 https://doi.org/10.1186/2191-219X-2-63	journal	January 2012
Cerebral metabolism and patterned visual Stimulation: A positron emission tomographic study of the human visual cortex Kushner, M. J.; Rosenquist, A.; Alavi, A. Neurology, Vol. 38, Issue 1 https://doi.org/10.1212/WNL.38.1.89	journal	January 1988
Quantitative functional MRI: Concepts, issues and future challenges Pike, G. Bruce NeuroImage, Vol. 62, Issue 2 https://doi.org/10.1016/j.neuroimage.2011.10.046	journal	August 2012
Concurrent CBF and CMRGlc changes during human brain activation by combined fMRI–PET scanning Newberg, Andrew B.; Wang, Jiongjiong; Rao, Hengyi NeuroImage, Vol. 28, Issue 2 https://doi.org/10.1016/j.neuroimage.2005.06.040	journal	November 2005
Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1 Polimeni, Jonathan R.; Fischl, Bruce; Greve, Douglas N. NeuroImage, Vol. 52, Issue 4 https://doi.org/10.1016/j.neuroimage.2010.05.005	journal	October 2010
Tomographic measurement of local cerebral glucose metabolic rate in humans with (F-18)2-fluoro-2-deoxy-D-glucose: Validation of method Phelps, M. E.; Huang, S. C.; Hoffman, E. J. Annals of Neurology, Vol. 6, Issue 5 https://doi.org/10.1002/ana.410060502	journal	November 1979
A receptor-based model for dopamine-induced fMRI signal Mandeville, Joseph B.; Sander, Christin Y. M.; Jenkins, Bruce G. NeuroImage, Vol. 75 https://doi.org/10.1016/j.neuroimage.2013.02.036	journal	July 2013
Baseline CBF , and BOLD, CBF , and CMRO ₂ fMRI of Visual and Vibrotactile Stimulations in Baboons Wey, Hsiao-Ying; Wang, Danny J.; Duong, Timothy Q. Journal of Cerebral Blood Flow & Metabolism, Vol. 31, Issue 2 https://doi.org/10.1038/jcbfm.2010.154	journal	September 2010
The ¹⁸ F-fluorodeoxyglucose Lumped Constant Determined in Human Brain from Extraction Fractions of ¹⁸ F-fluorodeoxyglucose and Glucose Hasselbalch, Steen G.; Holm, Søren; Pedersen, Hanne S. Journal of Cerebral Blood Flow & Metabolism, Vol. 21, Issue 8 https://doi.org/10.1097/00004647-200108000-00012	journal	August 2001
Nonoxidative glucose consumption during focal physiologic neural activity Fox, P.; Raichle, M.; Mintun, M. Science, Vol. 241, Issue 4864 https://doi.org/10.1126/science.3260686	journal	July 1988
Cocaine-Induced Redoppuction of Glucose Utilization in Human Brain: A Study Using Positron Emission Tomography and [Fluorine 18]-Fluorodeoxyglucose London, Edythe D. Archives of General Psychiatry, Vol. 47, Issue 6 https://doi.org/10.1001/archpsyc.1990.01810180067010	journal	June 1990
Brain work and Brain Imaging Raichle, Marcus E.; Mintun, Mark A. Annual Review of Neuroscience, Vol. 29, Issue 1 https://doi.org/10.1146/annurev.neuro.29.051605.112819	journal	July 2006
Dynamic models of BOLD contrast Buxton, Richard B. NeuroImage, Vol. 62, Issue 2 https://doi.org/10.1016/j.neuroimage.2012.01.012	journal	August 2012
Effects of Chronic Cocaine Self-Administration on Cognition and Cerebral Glucose Utilization in Rhesus Monkeys Gould, Robert W.; Gage, H. Donald; Nader, Michael A. Biological Psychiatry, Vol. 72, Issue 10 https://doi.org/10.1016/j.biopsych.2012.05.001	journal	November 2012
Neurovascular coupling to D2/D3 dopamine receptor occupancy using simultaneous PET/functional MRI Sander, C. Y.; Hooker, J. M.; Catana, C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1220512110	journal	May 2013
Influence of Plasma Glucose Concentration on Lumped Constant of the Deoxyglucose Method: Effects of Hyperglycemia in the Rat Schuier, Franz; Orzi, Francesco; Suda, Sumio Journal of Cerebral Blood Flow & Metabolism, Vol. 10, Issue 6 https://doi.org/10.1038/jcbfm.1990.134	journal	November 1990

Cited By (29)

Translational MR Neuroimaging of Stroke and Recovery Mandeville, Emiri T.; Ayata, Cenk; Zheng, Yi Translational Stroke Research, Vol. 8, Issue 1 https://doi.org/10.1007/s12975-016-0497-z	journal	August 2016
MR-PET head motion correction based on co-registration of multi-contrast MR images Chen, Zhaolin; Sforazzini, Francesco; Baran, Jakub bioRxiv https://doi.org/10.1101/450676	posted_content	January 2018
DREAMM: A Biobehavioral Imaging Methodology for Dynamic In Vivo Whole-Brain Mapping of Cell Type-Specific Functional Networks Michaelides, Michael; Hurd, Yasmin L. Neuropsychopharmacology, Vol. 40, Issue 1 https://doi.org/10.1038/npp.2014.233	journal	December 2014
Combined PET/MRI: from Status Quo to Status Go. Summary Report of the Fifth International Workshop on PET/MR Imaging; February 15–19, 2016; Tübingen, Germany Bailey, D. L.; Pichler, B. J.; Gückel, B. Molecular Imaging and Biology, Vol. 18, Issue 5 https://doi.org/10.1007/s11307-016-0993-2	journal	August 2016
Functional dynamics of dopamine synthesis during monetary reward and punishment processing Hahn, Andreas; Reed, Murray B.; Pichler, Verena bioRxiv https://doi.org/10.1101/2019.12.23.886812	posted_content	December 2020
From simultaneous to synergistic MR‐PET brain imaging: A review of hybrid MR‐PET imaging methodologies Chen, Zhaolin; Jamadar, Sharna D.; Li, Shenpeng Human Brain Mapping, Vol. 39, Issue 12 https://doi.org/10.1002/hbm.24314	journal	August 2018
Positron emission tomography visualized stimulation of the vestibular organ is localized in Heschl's gyrus Devantier, Louise; Hansen, Allan K.; Mølby‐Henriksen, Jens‐Jacob Human Brain Mapping, Vol. 41, Issue 1 https://doi.org/10.1002/hbm.24798	journal	September 2019
Functional dynamics of dopamine synthesis during monetary reward and punishment processing Hahn, Andreas; Reed, Murray B.; Pichler, Verena Journal of Cerebral Blood Flow & Metabolism https://doi.org/10.1177/0271678X211019827	journal	May 2021
Simultaneous EEG–PET–fMRI measurements in disorders of consciousness: an exploratory study on diagnosis and prognosis Golkowski, Daniel; Merz, Katharina; Mlynarcik, Caroline Journal of Neurology, Vol. 264, Issue 9 https://doi.org/10.1007/s00415-017-8591-z	journal	August 2017
Constant Infusion Radiotracer Administration for High Temporal Resolution Positron Emission Tomography (PET) of the Human Brain: Application to [18F]-Fluorodexoyglucose PET (FDG-PET) Jamadar, Sharna D.; Ward, Phillip G. D.; Carey, Alexandra bioRxiv https://doi.org/10.1101/667352	posted_content	June 2019
Analysis of continuous infusion functional PET (fPET) in the human brain Li, Shenpeng; Jamadar, Sharna D.; Ward, Phillip G. D. NeuroImage, Vol. 213 https://doi.org/10.1016/j.neuroimage.2020.116720	journal	June 2020
Effects of flow changes on radiotracer binding: Simultaneous measurement of neuroreceptor binding and cerebral blood flow modulation Sander, Christin Y.; Mandeville, Joseph B.; Wey, Hsiao-Ying Journal of Cerebral Blood Flow & Metabolism, Vol. 39, Issue 1 https://doi.org/10.1177/0271678x17725418	journal	August 2017
Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex Jamadar, Sharna D.; Ward, Phillip G. D.; Li, Shenpeng bioRxiv https://doi.org/10.1101/451468	posted_content	October 2018
Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images? Rajkumar, Ravichandran; Rota Kops, Elena; Mauler, Jörg PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0184743	journal	September 2017
The renaissance of functional 18F-FDG PET brain activation imaging Verger, Antoine; Guedj, Eric European Journal of Nuclear Medicine and Molecular Imaging, Vol. 45, Issue 13 https://doi.org/10.1007/s00259-018-4165-2	journal	September 2018
Simultaneous task-based BOLD-fMRI and [18-F] FDG functional PET for measurement of neuronal metabolism in the human visual cortex Jamadar, Sharna D.; Ward, Phillip GD.; Li, Shenpeng NeuroImage, Vol. 189 https://doi.org/10.1016/j.neuroimage.2019.01.003	journal	April 2019
Imaging mitochondrial complex I activation during a vibrotactile stimulation: A PET study using [ ¹⁸ F]BCPP-EF in the conscious monkey brain Fang, Jingwan; Ohba, Hiroyuki; Hashimoto, Fumio Journal of Cerebral Blood Flow & Metabolism https://doi.org/10.1177/0271678x19900034	journal	January 2020
Inflammation in Post-Traumatic Stress Disorder (PTSD): A Review of Potential Correlates of PTSD with a Neurological Perspective Kim, Tammy D.; Lee, Suji; Yoon, Sujung Antioxidants, Vol. 9, Issue 2 https://doi.org/10.3390/antiox9020107	journal	January 2020
Evaluation of Task-Related Brain Activity: Is There a Role for ¹⁸ F FDG-PET Imaging? Chiaravalloti, Agostino; Micarelli, Alessandro; Ricci, Maria BioMed Research International, Vol. 2019 https://doi.org/10.1155/2019/4762404	journal	July 2019
MR-PET head motion correction based on co-registration of multicontrast MR images Chen, Zhaolin; Sforazzini, Francesco; Baran, Jakub Human Brain Mapping https://doi.org/10.1002/hbm.24497	journal	January 2019
Analysis of continuous infusion functional PET (fPET) in the human brain Li, Shenpeng; Jamadar, Sharna D.; Ward, Phillip G. D. bioRxiv https://doi.org/10.1101/778357	posted_content	September 2019
Simultaneous trimodal PET-MR-EEG imaging: Do EEG caps generate artefacts in PET images? Rajkumar, Ravichandran; Rota Kops, Elena; Mauler, Jörg RWTH Aachen University https://doi.org/10.18154/rwth-conv-222121	text	January 2017
Decoupling of Dopamine Release and Neural Activity in Major Depressive Disorder during Reward Processing Assessed by Simultaneous fPET-fMRI Zhang, Xue; Wang, Fuyixue; Hamilton, J. Paul bioRxiv https://doi.org/10.1101/861534	posted_content	January 2019
Metabolite concentration changes associated with positive and negative BOLD responses in the human visual cortex: A functional MRS study at 7 Tesla Boillat, Yohan; Xin, Lijing; van der Zwaag, Wietske Journal of Cerebral Blood Flow & Metabolism, Vol. 40, Issue 3 https://doi.org/10.1177/0271678x19831022	journal	February 2019
Simultaneous PET-MRI imaging of cerebral blood flow and glucose metabolism in the symptomatic unilateral internal carotid artery/middle cerebral artery steno-occlusive disease Cui, Bixiao; Zhang, Tianhao; Ma, Yan European Journal of Nuclear Medicine and Molecular Imaging, Vol. 47, Issue 7 https://doi.org/10.1007/s00259-019-04551-w	journal	November 2019
Dynamic coupling between fMRI local connectivity and interictal EEG in focal epilepsy: A wavelet analysis approach: Dynamic Coupling between fMRI Local Connectivity and Interictal EEG in Focal Epilepsy Omidvarnia, Amir; Pedersen, Mangor; Vaughan, David N. Human Brain Mapping, Vol. 38, Issue 11 https://doi.org/10.1002/hbm.23723	journal	July 2017
Structure of the Human 4-Hydroxyphenylpyruvic Acid Dioxygenase Gene (HPD) Awata, Hisataka; Endo, Fumio; Matsuda, Ichiro Genomics, Vol. 23, Issue 3 https://doi.org/10.1006/geno.1994.1540	journal	October 1994
Task-relevant brain networks identified with simultaneous PET/MR imaging of metabolism and connectivity Hahn, Andreas; Gryglewski, Gregor; Nics, Lukas Brain Structure and Function https://doi.org/10.1007/s00429-017-1558-0	journal	November 2017
The Effects of Capillary Transit Time Heterogeneity (CTH) on the Cerebral Uptake of Glucose and Glucose Analogs: Application to FDG and Comparison to Oxygen Uptake Angleys, Hugo; Jespersen, Sune N.; Østergaard, Leif Frontiers in Computational Neuroscience, Vol. 10 https://doi.org/10.3389/fncom.2016.00103	journal	October 2016

Similar Records

Mapping of change in cerebral glucose utilization using fluorine-18 fluorodeoxyglucose double injection and the constrained weighted-integration method

Journal Article · Sun Dec 01 00:00:00 EST 1996 · IEEE Transactions on Medical Imaging · OSTI ID:1281964

Murase, K; Kuwabara, Hiroto; Yasuhara, Yoshifumi; +2 more

Rapid ¹⁸F-FDG Uptake in Brain of Awake, Behaving Rat and Anesthetized Chicken has Implications for Behavioral PET Studies in Species With High Metabolisms

Journal Article · Tue Jun 05 00:00:00 EDT 2018 · Frontiers in Behavioral Neuroscience · OSTI ID:1281964

Gold, Maria E. L.; Norell, Mark A.; Budassi, Michael; +2 more

Diminished glucose transport and phosphorylation in Alzheimer`s disease determined by dynamic FDG-PET

Journal Article · Thu Feb 01 00:00:00 EST 1996 · Journal of Nuclear Medicine · OSTI ID:1281964

Piert, M; Koeppe, R A; Giordani, B; +2 more

Related Subjects

60 APPLIED LIFE SCIENCES
47 OTHER INSTRUMENTATION
2-[18F]-fluorodeoxyglucose (FDG)
Glucose utilization
Visual stimulus
MR/PET
PET

Title: Dynamic functional imaging of brain glucose utilization using fPET-FDG

Citation Formats

References (31)

Cited By (29)

Similar Records

Related Subjects