Manganese-enhanced magnetic resonance imaging (MEMRI) without compromise of the blood-brain barrier detects hypothalamic neuronal activity in vivo

NMR in Biomedicine

Volumn 19, Issue 8, 2006, Pages 1028-1034

  Kuo, Yu Ting ^a,b,c   Herlihy, Amy H ^a   So, Po Wah ^a   Bell, Jimmy D ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Blood brain barrier; Brain; Fasting; Hypothalamus; In vivo magnetic resonance imaging; Manganese; Manganese enhanced magnetic resonance imaging; Mouse

Indexed keywords

BLOOD; BRAIN; MANGANESE; NEUROPHYSIOLOGY; NONINVASIVE MEDICAL PROCEDURES;

BLOOD-BRAIN BARRIER; HYPOTHALAMUS; MANGANESE-ENHANCED MAGNETIC RESONANCE IMAGING; MOUSE;

MAGNETIC RESONANCE IMAGING;

MANGANESE CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BRAIN FUNCTION; CONTROLLED STUDY; DIET RESTRICTION; FUNCTIONAL ASSESSMENT; HYPOTHALAMUS FUNCTION; IMAGE ANALYSIS; IMAGE ENHANCEMENT; IMAGE QUALITY; IN VIVO STUDY; MALE; MOUSE; NON INVASIVE MEASUREMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL;

ANIMALS; BLOOD-BRAIN BARRIER; FASTING; FEMALE; HYPOTHALAMUS; INFUSIONS, INTRAVENOUS; KINETICS; MAGNETIC RESONANCE IMAGING; MALE; MANGANESE; MICE; MODELS, ANIMAL; NEURONS;

ANIMALIA; MURINAE;

EID: 33749501101     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1070     Document Type: Article

References (47)

1. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. USA. 1990; 87: 9868-9872.
2. 2-weighted MRI. NMR Biomed. 1996; 9: 20-23.
3. Chen YC, Galpern WR, Brownell AL, Matthews RT, Bogdanov M, Isacson O, Keltner JR, Beal MF, Rosen BR, Jenkins BG. Detection of dopaminergic neurotransmitter activity using pharmacologic MRI: correlation with PET, microdialysis and behavioral data. Magn. Reson. Med. 1997; 38: 389-398.
4. Jones RA, Muller TB, Haraldseth O, Baptista AM, Oksendal AN. Cerebrovascular changes in rats during ischemia and reperfusion: a comparison of BOLD and first pass bolus tracking techniques. Magn. Reson. Med. 1996; 35: 489-496.
5. Wong EC, Buxton RB, Frank LR. Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed. 1997; 10: 237-249.
6. Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR. A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn. Reson. Med. 1998; 40: 383-396.
7. Wang J, Aguirre GK, Kimberg DY, Roc AC, Li L, Detre JA. Arterial spin labeling perfusion fMRI with very low task frequency. Magn. Reson. Med. 2003; 49: 796-802.
8. Jahng GH, Song E, Zhu XP, Matson GB, Weiner MW, Schaff N. Human brain: reliability and reproducibility of pulsed arterial spin-labeling perfusion MR imaging. Radiology 2005; 234: 909-916
9. Detre JA, Wang J. Technical aspects and utility of fMRI using BOLD and ASL. Clin. Neurophysiol. 2002; 113: 621-634.
10. Aoki I, Tanaka C, Takegami T, Ebisu T, Umeda M, Fukunaga M, Fukuda K, Silva AC, Koretsky AP, Naruse S. Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI). Magn. Reson. Med. 2002; 48: 927-933.
11. Aoki I, Wu YJ, Silva AC, Lynch RM, Koretsky AP. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 2004; 22: 1046-1059.
12. Pautler RG, Koretsky AR Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage 2002; 16: 441-448.
13. Narita K, Kawasaki F, Kita H. Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res. 1990; 510: 289-295.
14. 1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn. Reson. Med. 1997; 38: 378-388.
15. Pautler RG, Silva AC, Koretsky AP. In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 1998; 40: 740-748.
16. Saleem KS, Pauls JM, Augath M, Trinath T, Prause BA, Hashikawa T, Logothetis NK. Magnetic resonance imaging of neuronal connections in the macaque monkey. Neuron 2002; 34: 685-700.
17. Yu X, Wadghiri YZ, Sanes DH, Turnbull DH. In vivo auditory brain mapping in mice with Mn-enhanced MRI. Nat. Neurosci. 2005; 8: 961-968.
18. Muccioli G, Tschop M, Papotti M, Deghenghi R, Heiman M, Ghigo E. Neuroendocrine and peripheral activities of ghrelin: implications in metabolism and obesity. Eur J. Pharmacol. 2002; 440: 235-254.
19. Hussy N, Deleuze C, Desarmenien MG, Moos F C. Osmotic regulation of neuronal activity: a new role for taurine and glial cells in a hypothalamic neuroendocrine structure. Prog. Neurobiol. 2000; 62: 113-134.
20. Toney GM, Chen QH, Cato MJ, Stocker SD. Central osmotic regulation of sympathetic nerve activity. Acta Physiol. Scand. 2003; 177: 43-55.
21. Merchenthaler I. Neurons with access to the general circulation in the central nervous system of the rat: a retrograde tracing study with fluoro-gold. Neuroscience 1991; 44: 655-662.
22. Peruzzo B, Pastor FE, Blazquez JL, Schobitz K, Pelaez B, Amat P, Rodriguez EM. A second look at the barriers of the medial basal hypothalamus. Exp. Brain Res. 2000; 132: 10-26.
23. Rudin M, Weissleder R. Molecular imaging in drug discovery and development. Nat. Rev. Drug Discov. 2003; 2: 123-131.
24. Jaffer FA, Weissleder R. Molecular imaging in the clinical arena. JAMA. 2005; 293: 855-862.
25. Akana SF, Strack AM, Hanson ES, Dallman MF. Regulation of activity in the hypothalamo-pituitary-adrenal axis is integral to a larger hypothalamic system that determines caloric flow. Endocrinology 1994; 135: 1125-1134.
26. 1, contrast. Magn. Reson. Med. 2005; 53: 640-648.
27. 1, relaxation times in mouse brain associated with different modes of systemic administration of manganese chloride. J. Magn. Reson. Imaging 2005; 21: 334-339.
28. Elmquist JK, Elias CF, Saper CB. From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 1999; 22: 221-232.
29. Vrang N, Larsen PJ, Clausen JT, Kristensen P. Neurochemical characterization of hypothalamic cocaine-amphetamine-regulated transcript neurons. J. Neurosci. 1999; 19: RC5.
30. Toshinai K, Mondal MS, Nakazato M, Date Y, Murakami N, Kojima M, Kangawa K, Matsukura S. Upregulation of Ghrelin expression in the stomach upon fasting, insulin-induced hypoglycemia and leptin administration. Biochem. Biophys. Res. Commun. 2001; 281: 1220-1225.
31. Morikawa Y, Ueyama E, Senba E. Fasting-induced activation of mitogen-activated protein kinases (ERK/p38) in the mouse hypothalamus. J. Neuroendocrinol. 2004; 16: 105-112.
32. Diano S, Horvath B, Urbanski HF, Sotonyi P, Horvath TL. Fasting activates the nonhuman primate hypocretin (orexin) system and its postsynaptic targets. Endocrinology 2003; 144: 3774-3778.
33. Angeles-Castellanos M, Aguilar-Roblero R, Escobar C. c-Fos expression in hypothalamic nuclei of food-entrained rats. Am. J. Physiol. Regul. Integr Comp. Physiol. 2004; 286: R158-R165.
34. Fraga IC, Fregoneze JB, Carvalho FL, Dantas KB, Azevedo CS, Pinho CB, de Castro ESE. Acute fluoxetine administration differentially affects brain C-Fos expression in fasted and refed rats. Neuroscience 2005; 134: 327-334.
35. Estacio MA, Yamada S, Tsukamura H, Hirunagi K, Maeda K. Effect of fasting and immobilization stress on estrogen receptor immunoreactivity in the brain in ovariectomized female rats. Brain Res. 1996; 717: 55-61.
36. Challis BG, Pinnock SB, Coll AP, Carter RN, Dickson SL, O'Rahilly S. Acute effects of PYY3-36 on food intake and hypothalamic neuropeptide expression in the mouse. Biochem. Biophys. Res. Commun. 2003; 311: 915-919.
37. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 2002; 418: 650-654.
38. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, Ghatei MA, Bloom SR. Inhibition of food intake in obese subjects by peptide YY3-36. N. Engl. J. Med. 2003; 349: 941-948.
39. Van der Linden A, Verhoye M, Van Meir V, Tindemans I, Eens M, Absil P, Balthazart J. In vivo manganese-enhanced magnetic resonance imaging reveals connections and functional properties of the songbird vocal control system. Neuroscience 2002; 112: 467-474.
40. 2 for dynamic manganese-enhanced MRI. Magn. Reson. Med. 2004; 51: 978-987.
41. Gati IS, Menon RS, Ugurbil K, Rutt BK. Experimental determination of the BOLD field strength dependence in vessels and tissue. Magn. Reson. Med. 1997; 38: 296-302.
42. Dagli MS, Ingeholm JE, Haxby JV. Localization of cardiac-induced signal change in fMRI. Neuroimage 1999; 9: 407-415.
43. Wise RG, Ide K, Poulin MJ, Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 2004; 21: 1652-1664.
44. Gustard S, Williams EJ, Hall LD, Pickard JD, Carpenter TA. Influence of baseline hematocrit on between-subject BOLD signal change using gradient echo and asymmetric spin echo EPI. Magn. Reson. Imaging. 2003; 21: 599-607.
45. Bruhn H, Kleinschmidt A, Boecker H, Merboldt KD, Hanicke W, Frahm J. The effect of acetazolamide on regional cerebral blood oxygenation at rest and under stimulation as assessed by MRI. J. Cereb. Blood Flow Metab. 1994; 14: 742-748.
46. Look DC, Locker DR. Time saving in measurement of NMR and EPR relaxation times. Rev. Sci. Instrum. 1970; 41: 250-251.
47. 1, imaging. Magn. Reson. Med. 1991; 22: 414-424.