Limits on activation-induced temperature and metabolic changes in the human primary visual cortex

Magnetic Resonance in Medicine

Volumn 56, Issue 2, 2006, Pages 348-355

  Katz Brull, Rachel ^a   Alsop, David C ^a   Marquis, Robert P ^a   Lenkinski, Robert E ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

Brain activation; Cerebral blood flow; Magnetic resonance spectroscopy; N acetylaspartate; Temperature

Indexed keywords

AMINO ACIDS; BRAIN; CHEMICAL ACTIVATION; HEMODYNAMICS; MAGNETIC RESONANCE; MAGNETIC RESONANCE SPECTROSCOPY; METABOLISM; NEURONS; TEMPERATURE;

BRAIN ACTIVATION; CEREBRAL BLOOD FLOW; MAGNETIC RESONANCE SPECTROSCOPIES (MRS); N-ACETYLASPARTATE; OXIDATIVE METABOLISM; PRIMARY VISUAL CORTEX; TEMPERATURE DECREASE; THERMAL EQUILIBRIUMS;

BLOOD;

CHOLINE; GLUTAMIC ACID; GLUTAMINE; INOSITOL; LACTIC ACID; N ACETYLASPARTIC ACID;

ACTIVATION INDUCED TEMPERATURE; ADULT; AEROBIC METABOLISM; ARTICLE; BRAIN BLOOD FLOW; BRAIN MAPPING; BRAIN METABOLISM; CONTROLLED STUDY; COOLING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUCOSE UTILIZATION; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; INTERMETHOD COMPARISON; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; TEMPERATURE MEASUREMENT; THEORETICAL MODEL; THERMOREGULATION; VISUAL CORTEX; VISUAL STIMULATION;

EID: 33746703198     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.20972     Document Type: Article

References (40)

1. Buxton RB. An introduction to functional magnetic resonance imaging: principles and techniques. Cambridge: Cambridge University Press; 2002. p 3-41.
2. Erickson KM, Lanier WL. Anesthetic technique influences brain temperature, independently of core temperature, during craniotomy in cats. Anesth Analg 2003;96:1460-1466,
3. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001;412:150-157.
4. Prichard J, Rothman D, Novotny E, Petroff O, Kuwabara T, Avison M, Howseman A, Hanstock C, Shulman R. Lactate rise detected by H-1-NMR in human visual-cortex during physiological stimulation. Proc Natl Acad Sci USA 1991;88:5829-5831.
5. Sappey-Marinier D, Calabrese G, Fein G, Hugg JW, Biggins C, Weiner MW. Effect of photic-stimulation on human visual-cortex lactate and phosphates using H-1 and P-31 magnetic-resonance spectroscopy. J Cereb Blood Flow Metab 1992;12:584-592.
6. Frahm J, Kruger G, Merboldt KD, Kleinschmidt A. Dynamic uncoupling and recoupling of perfusion and oxidative metabolism during focal brain activation in man. Magn Reson Med 1996;35:143-148.
7. Urrila AS, Hakkarainen T, Heikkinen T, Vuori T, Stenberg D, Hakkinen AM, Lundbom T, Porkka-Heiskanen T. Metabolic imaging of human cognition: an fMRI/H-1-MRS study of brain lactate response to silent word generation. J Cereb Blood Flow Metab 2003;23:942-948.
8. Richards TL, Dager SR, Corina D, Serafini S, Heide AC, Steury K, Strauss W, Hayes CE, Abbott RD, Craft S, Shaw D, Posse S, Berninger VW. Dyslexic children have abnormal brain lactate response to reading-related language tasks. AJNR Am J Neuroradiol 1999;20:1393-1398.
9. Yablonskiy DA, Ackerman JJH, Raichle ME. Coupling between changes in human brain temperature and oxidative metabolism during prolonged visual stimulation. Proc Natl Acad Sci USA 2000;97:7603-7608.
10. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 2004;305:99-103.
11. Cady EB, Dsouza PC, Penrice J, Lorek A. The estimation of local brain temperature by in-vivo H-1 magnetic-resonance spectroscopy. Magn Reson Med 1995;33:862-867.
12. Corbett RJ, Laptook AR, Tollefsbol G, Kim B. Validation of a noninvasive method to measure brain temperature in vivo using 1H NMR spectroscopy. J Neurochem 1995;64:1224-1230.
13. Knight-Scott J, Haley AP, Rossmiller SR, Farace E, Mai VM, Christopher JM, Manning CA, Simnad VI, Siragy HM. Molality as a unit of measure for expressing 1H MRS brain metabolite concentrations in vivo. Magn Reson Imaging 2003;21:787-797.
14. Pouwels PJ, Brockmann K, Kruse B, Wilken B, Wick M, Hanefeld F, Frahm J. Regional age dependence of human brain metabolites from infancy to adulthood as detected by quantitative localized proton MRS. Pediatr Res 1999;46:474-485.
15. Kanowski M, Kaufmann J, Braun J, Bernarding J, Tempelmann C. Quantitation of simulated short echo time 1H human brain spectra by LCModel and AMARES. Magn Reson Med 2004;51:904-912.
16. Collins CM, Smith MB, Turner R. Model of local temperature changes in brain upon functional activation. J Appl Physiol 2004;97:2051-2055.
17. Ecker RD, Goerss SJ, Meyer FB, Cohen-Gadol AA, Britton JW, Levine JA. Vision of the future: initial experience with intraoperative real-time high-resolution dynamic infrared imaging. J Neurosurg 2002;97:1460-1471.
18. Gorbach AM, Heiss J, Kufta C, Sato S, Fedio P, Kammerer WA, Solomon J, Oldfield EH. Intraoperative infrared functional imaging of human brain. Ann Neurol 2003;54:297-309.
19. Fox PT, Raichle ME, Mintun MA, Dence C. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988;241:462-464.
20. Chhina N, Kuestermann E, Halliday J, Simpson LJ, Macdonald IA, Bachelard HS, Morris PG. Measurement of human tricarboxylic acid cycle rates during visual activation by (13)C magnetic resonance spectroscopy. J Neurosci Res 2001;66:737-746.
21. Ritchie JM, Keynes RD. The production and absorption of heat associated with electrical activity in nerve and electric organ. Q Rev Biophys 1985;18:451-476.
22. Duong TQ, Yacoub E, Adriany G, Hu X, Ugurbil K, Kim SG. Microvascular BOLD contribution at 4 and 7 T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn Reson Med 2003;49:1019-1027.
23. Boxerman JL, Hamberg LM, Rosen BR, Weisskoff RM. MR contrast due to intravascular magnetic susceptibility perturbations. Magn Reson Med 1995;34:555-566.
24. Silvennoinen MJ, Clingman CS, Golay X, Kauppinen RA, van Zijl PC. Comparison of the dependence of blood R2 and R2* on oxygen saturation at 1.5 and 4.7 Tesla. Magn Reson Med 2003;49:47-60.
25. Yablonskiy DA, Haacke EM. Theory of NMR signal behavior in magnetically inhomogeneous tissues: the static dephasing regime. Magn Reson Med 1994;32:749-763.
26. Zhu XH, Chen W. Observed BOLD effects on cerebral metabolite resonances in human visual cortex during visual stimulation: a functional H-1 MRS study at 4 T. Magn Reson Med 2001;46:841-847.
27. Chen W, Zhu XH, Gruetter R, Seaquist ER, Adriany G, Ugurbil K. Study of tricarboxylic acid cycle flux changes in human visual cortex during hemifield visual stimulation using H-1-{C-13} MRS and fMRI. Magn Reson Med 2001;45:349-355.
28. 13C NMR studies. Brain Res 1993;610:16-23.
29. Dudley RE, Nelson SR, Samson F. Influence of chloralose on brain regional glucose utilization. Brain Res 1982;233:173-180.
30. Hyder F, Chase JR, Behar KL, Mason GF, Siddeek M, Rothman DL, Shulman RG. Increased tricarboxylic acid cycle flux in rat brain during forepaw stimulation detected with 1H [13C] NMR. Proc Natl Acad Sci USA 1996;93:7612-7617.
31. Sokoloff L. Relationships among local functional activity, energy metabolism, and blood flow in the central nervous system. Fed Proc 1981;40:2311-2316.
32. Ueki M, Linn F, Hossmann KA. Functional activation of cerebral blood-flow and metabolism before and after global-ischemia of rat-brain. J Cereb Blood Flow Metab 1988;8:486-494.
33. Cohen DM, Wei JN, Smith EO, Gao XL, Quast MJ, Sokoloff L. A method for measuring cerebral glucose metabolism in vivo by C-13-NMR spectroscopy. Magn Reson Med 2002;48:1063-1067.
34. Sibson NR, Dhankhar A, Mason GF, Rothman DL, Behar KL, Shulman RG. Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc Natl Acad Sci USA 1998;95:316-321.
35. Merboldt KD, Bruhn H, Hanicke W, Michaelis T, Frahm J. Decrease of glucose in the human visual-cortex during photic-stimulation. Magn Reson Med 1992;25:187-194.
36. Boucard CC, Mostert JP, Cornelissen FW, De Keyser J, Oudkerk M, Sijens PE. Visual stimulation, 1H MR spectroscopy and fMRI of the human visual pathways. Eur Radiol 2005;15:47-52.
37. Mangia S, Garreffa G, Bianciardi M, Giove F, Di Salle F, Maraviglia B. The aerobic brain: lactate decrease at the onset of neural activity. Neuroscience 2003;118:7-10.
38. Kauppinen RA, Eleff SM, Ulatowski JA, Kraut M, Scher B, van Zijl PC. Visual activation in alpha-chloralose-anaesthetized cats does not cause lactate accumulation in the visual cortex as detected by [1H]NMR difference spectroscopy. Eur J Neurosci 1997;9:654-661.
39. Gruetter R, Seaquist ER, Kim S, Ugurbil K. Localized in vivo C-13-NMR of glutamate metabolism in the human brain: initial results at 4 Tesla. Dev Neurosci 1998;20:380-388.
40. Pfeuffer J, Tkac I, Choi IY, Merkle H, Ugurbil K, Garwood M, Gruetter R. Localized in vivo H-1 NMR detection of neurotransmitter labeling in rat brain during infusion of 1-C-13 D-glucose. Magn Reson Med 1999;41:1077-1083.