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Open Access 01-07-2018 | Original Article

Is visual activation associated with changes in cerebral high-energy phosphate levels?

Authors: Bart L. van de Bank, Marnix C. Maas, Lauren J. Bains, Arend Heerschap, Tom W. J. Scheenen

Published in: Brain Structure and Function | Issue 6/2018

Abstract

Phosphorus magnetic resonance spectroscopy (³¹P MRS) has been employed before to assess phosphocreatine (PCr) and other high-energy phosphates in the visual cortex during visual stimulation with inconsistent results. We performed functional ³¹P MRS imaging in the visual cortex and control regions during a visual stimulation paradigm at an unprecedented sensitivity, exploiting a dedicated RF coil design at a 7 T MR system. Visual stimulation in a 3 min 24 s on–off paradigm in eight young healthy adults generated a clear BOLD effect with traditional ¹H functional MRI in the visual cortex (average z score 9.9 ± 0.2). However, no significant event-related changes in any of the ³¹P metabolite concentrations, linewidths (7.9 ± 1.8 vs 7.8 ± 1.9 Hz) or tissue pH (7.07 ± 0.13 vs 7.06 ± 0.07) were detectable. Overall, our study of ³¹P MRSI in 15 cm³ voxels had a detection threshold for changes in PCr, Pi and γ-ATP between stimulation and rest of 5, 17 and 10%, respectively. In individual subjects, the mean coefficients of variance for PCr and Pi levels of control voxels were 6 ± 3 and 19 ± 8% (three time point average of 3 min 24 s). Altogether this indicates that energy supply for neuronal activation at this temporal resolution does not drain global PCr resources.

Adanyeguh IM, Rinaldi D, Henry PG, Caillet S, Valabregue R, Durr A, Mochel F (2015) Triheptanoin improves brain energy metabolism in patients with Huntington disease. Neurology 84(5):490–495. https://doi.org/10.1212/WNL.0000000000001214 CrossRefPubMedPubMedCentral

Andres RH, Ducray AD, Schlattner U, Wallimann T, Widmer HR (2008) Functions and effects of creatine in the central nervous system. Brain Res Bull 76(4):329–343. https://doi.org/10.1016/j.brainresbull.2008.02.035 CrossRefPubMed

Aubert A, Costalat R (2002) A model of the coupling between brain electrical activity, metabolism, and hemodynamics: application to the interpretation of functional neuroimaging. NeuroImage 17(3):1162–1181CrossRefPubMed

Barreto FR, Costa TB, Landim RC, Castellano G, Salmon CE (2014) (31)P-MRS using visual stimulation protocols with different durations in healthy young adult subjects. Neurochem Res 39(12):2343–2350. https://doi.org/10.1007/s11064-014-1433-9 CrossRefPubMed

Chen W, Zhu XH, Adriany G, Ugurbil K (1997) Increase of creatine kinase activity in the visual cortex of human brain during visual stimulation: a 31P magnetization transfer study. Magn Reson Med 38(4):551–557CrossRefPubMed

Harris JJ, Jolivet R, Attwell D (2012) Synaptic energy use and supply. Neuron 75(5):762–777. https://doi.org/10.1016/j.neuron.2012.08.019 CrossRefPubMed

Kan HE, Veltien A, Arnts H, Nabuurs CI, Luijten B, de Haan A, Wieringa B, Heerschap A (2009) Gated dynamic 31P MRS shows reduced contractile phosphocreatine breakdown in mice deficient in cytosolic creatine kinase and adenylate kinase. NMR Biomed 22(5):523–531. https://doi.org/10.1002/nbm.1364 CrossRefPubMed

Kato T, Murashita J, Shioiri T, Hamakawa H, Inubushi T (1996) Effect of photic stimulation on energy metabolism in the human brain measured by 31P-MR spectroscopy. J Neuropsychiatr Clin Neurosci 8(4):417–422CrossRef

Kato T, Murashita J, Shioiri T, Terada M, Inubushi T, Kato N (1998) Photic stimulation-induced alteration of brain energy metabolism measured by 31P-MR spectroscopy in patients with MELAS. J Neurol Sci 155(2):182–185CrossRefPubMed

Kemp GJ (2000) Non-invasive methods for studying brain energy metabolism: what they show and what it means. Dev Neurosci 22(5–6):418–428. https://doi.org/10.1159/000017471 CrossRefPubMed

Kim SY, Chen W, Ongur D, Du F (2017) Rapid and simultaneous measurement of phosphorus metabolite pool size ratio and reaction kinetics of enzymes in vivo. J Magn Reson Imaging. https://doi.org/10.1002/jmri.25744 CrossRefPubMedPubMedCentral

Lagemaat MW, van de Bank BL, Sati P, Li S, Maas MC, Scheenen TW (2016) Repeatability of (31) P MRSI in the human brain at 7 T with and without the nuclear Overhauser effect. NMR Biomed 29(3):256–263. https://doi.org/10.1002/nbm.3455 CrossRefPubMed

Lee B-Y, Zhu X-H, Chen W (2014) Elevated ATP synthase and creatine kinase activities in human visual cortex during visual stimulation: a 31P NMR magnetization transfer study at 7T. In: Proceedings of the annual meeting of the ISMRM, abstract 12, Milan

Mangia S, Tkac I, Gruetter R, Van de Moortele PF, Maraviglia B, Ugurbil K (2007) Sustained neuronal activation raises oxidative metabolism to a new steady-state level: evidence from 1H NMR spectroscopy in the human visual cortex. J Cereb Blood Flow Metab 27(5):1055–1063. https://doi.org/10.1038/sj.jcbfm.9600401 CrossRefPubMed

Mochel F, N’Guyen TM, Deelchand D, Rinaldi D, Valabregue R, Wary C, Carlier PG, Durr A, Henry PG (2012) Abnormal response to cortical activation in early stages of Huntington disease. Mov Disord 27(7):907–910. https://doi.org/10.1002/mds.25009 CrossRefPubMed

Murashita J, Kato T, Shioiri T, Inubushi T, Kato N (1999) Age-dependent alteration of metabolic response to photic stimulation in the human brain measured by 31P MR-spectroscopy. Brain Res 818(1):72–76CrossRefPubMed

Murashita J, Kato T, Shioiri T, Inubushi T, Kato N (2000) Altered brain energy metabolism in lithium-resistant bipolar disorder detected by photic stimulated 31P-MR spectroscopy. Psychol Med 30(1):107–115CrossRefPubMed

Naressi A, Couturier C, Devos JM, Janssen M, Mangeat C, de Beer R, Graveron-Demilly D (2001) Java-based graphical user interface for the MRUI quantitation package. Magma (New York) 12(2–3):141–152

Petroff OA, Prichard JW, Behar KL, Alger JR, den Hollander JA, Shulman RG (1985) Cerebral intracellular pH by 31P nuclear magnetic resonance spectroscopy. Neurology 35(6):781–788CrossRefPubMed

Rango M, Castelli A, Scarlato G (1997) Energetics of 3.5 s neural activation in humans: a 31P MR spectroscopy study. Magn Reson Med 38(6):878–883CrossRefPubMed

Rango M, Bonifati C, Bresolin N (2006) Parkinson’s disease and brain mitochondrial dysfunction: a functional phosphorus magnetic resonance spectroscopy study. J Cereb Blood Flow Metab 26(2):283–290. https://doi.org/10.1038/sj.jcbfm.9600192 CrossRefPubMed

Rodgers CT, Robson MD (2016) Coil combination for receive array spectroscopy: are data-driven methods superior to methods using computed field maps? Magn Reson Med 75(2):473–487. https://doi.org/10.1002/mrm.25618 CrossRefPubMed

Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C, Weiner MW (1992) Effect of photic stimulation on human visual cortex lactate and phosphates using 1H and 31P magnetic resonance spectroscopy. J Cereb Blood Flow Metab 12(4):584–592. https://doi.org/10.1038/jcbfm.1992.82 CrossRefPubMed

Scheenen TW, Heerschap A, Klomp DW (2008) Towards 1H-MRSI of the human brain at 7T with slice-selective adiabatic refocusing pulses. Magma (New York) 21(1–2):95–101. https://doi.org/10.1007/s10334-007-0094-y CrossRef

Shaka AJ, Keeler J, Freeman R (1983) Evaluation of a new broadband decoupling sequence: WALTZ-16. J Magn Reson 53(2):313–340. https://doi.org/10.1016/0022-2364(83)90035-5 CrossRef

Stefan D, Cesare FD, Andrasescu A, Popa E, Lazariev A, Vescovo E, Strbak O, Williams S, Starcuk Z, Cabanas M, Ormondt Dv, Graveron-Demilly D (2009) Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Meas Sci Technol 20(10):104035CrossRef

van de Bank BL, Orzada S, Smits F, Lagemaat MW, Rodgers CT, Bitz AK, Scheenen TWJ (2015) Optimized 31P MRS in the human brain at 7 T with a dedicated RF coil setup. NMR Biomed 28(11):1570–1578. https://doi.org/10.1002/nbm.3422 CrossRefPubMedPubMedCentral

Vanhamme L, van den Boogaart A, Van Huffel S (1997) Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 129(1):35–43. https://doi.org/10.1006/jmre.1997.1244 CrossRefPubMed

Vidyasagar R, Kauppinen RA (2008) 31P magnetic resonance spectroscopy study of the human visual cortex during stimulation in mild hypoxic hypoxia. Exp Brain Res 187(2):229–235. https://doi.org/10.1007/s00221-008-1298-8 CrossRefPubMed

Yuksel C, Du F, Ravichandran C, Goldbach JR, Thida T, Lin P, Dora B, Gelda J, O’Connor L, Sehovic S, Gruber S, Ongur D, Cohen BM (2015) Abnormal high-energy phosphate molecule metabolism during regional brain activation in patients with bipolar disorder. Mol Psychiatr 20(9):1079–1084. https://doi.org/10.1038/mp.2015.13 CrossRef

Zhu XH, Du F, Zhang N, Zhang Y, Lei H, Zhang X, Qiao H, Ugurbil K, Chen W (2009) Advanced in vivo heteronuclear mrs approaches for studying brain bioenergetics driven by mitochondria. Methods Mol Biol 489:317–357. https://doi.org/10.1007/978-1-59745-543-5_15 CrossRefPubMedPubMedCentral

Zhu XH, Qiao H, Du F, Xiong Q, Liu X, Zhang X, Ugurbil K, Chen W (2012) Quantitative imaging of energy expenditure in human brain. NeuroImage 60(4):2107–2117. https://doi.org/10.1016/j.neuroimage.2012.02.013 CrossRefPubMedPubMedCentral

Title: Is visual activation associated with changes in cerebral high-energy phosphate levels?
Authors: Bart L. van de Bank
Marnix C. Maas
Lauren J. Bains
Arend Heerschap
Tom W. J. Scheenen
Publication date: 01-07-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 6/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1656-7

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Is visual activation associated with changes in cerebral high-energy phosphate levels?

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