The effects of glutamate receptor agonists and antagonists on mouse hypothalamic and hippocampal neuronal activity shown through manganese enhanced MRI

NeuroImage

Volumn 59, Issue 2, 2012, Pages 968-978

  Hankir, Mohammed K ^a   Parkinson, James R ^a   Bloom, Stephen R ^a   Bell, Jimmy D ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Blood CSF barrier; Glutamate; Hypothalamus; Manganese enhanced MRI; Neuronal activity

Indexed keywords

DIZOCILPINE; GLUTAMATE RECEPTOR AGONIST; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMATE SODIUM; IONOTROPIC RECEPTOR AGONIST; MAGNESIUM ION; MANGANESE;

ARCUATE NUCLEUS; ARTICLE; BLOOD CEREBROSPINAL FLUID BARRIER; BRAIN REGION; CELL ACTIVITY; CONTROLLED STUDY; HIPPOCAMPUS; HYPOTHALAMUS; IMAGE ANALYSIS; ION TRANSPORT; LATERAL BRAIN VENTRICLE; NERVE CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; SUPRACHIASMATIC NUCLEUS;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; CONTRAST MEDIA; EXCITATORY AMINO ACID ANTAGONISTS; HIPPOCAMPUS; HYPOTHALAMUS; MAGNETIC RESONANCE IMAGING; MALE; MANGANESE; MICE; MICE, INBRED C57BL; NEURONS; RECEPTORS, GLUTAMATE; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 83055188039     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.08.063     Document Type: Article

References (46)

1. Aoki I., Wu Y.J., Silva A.C., Lynch R.M., Koretsky A.P. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. NeuroImage 2004, 22:1046-1059.
2. Chaudhri O.B., Parkinson J.R., Kuo Y.T., Druce M.R., Herlihy A.H., Bell J.D., Dhillo W.S., Stanley S.A., Ghatei M.A., Bloom S.R. Differential hypothalamic neuronal activation following peripheral injection of GLP-1 and oxyntomodulin in mice detected by manganese-enhanced magnetic resonance imaging. Biochem. Biophys. Res. Commun. 2006, 350:298-306.
3. Colman J.R., Nowocin K.J., Switzer R.C., Trusk T.C., Ramsdell J.S. Mapping and reconstruction of domoic acid induced neurodegeneration in the mouse brain. Neurotoxicol. Teratol. 2005, 27:753-767.
4. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 2001, 11:327-335.
5. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr. Opin. Neurobiol. 2006, 16:288-297.
6. de Tassigny X., Ackroyd K.J., Chatzidaki E.E., Colledge W.H. Kisspeptin signaling is required for peripheral but not central stimulation of gonadotrophin releasing hormone neurons by NMDA. J. Neurosci. 2010, 30:8581-8590.
7. Drapeau P., Nachshen D.A. Manganese fluxes and manganese-dependent neurotransmitter release in presynaptic nerve endings isolated from rat brain. J. Physiol. 1984, 348:493-510.
8. Eschenko O., Canals S., Simanova I., Beyerlein N., Murayama Y., Logothetis M.K. Mapping of functional brain activity in freely behaving rats during voluntary running using manganese-enhanced MRI: implication for longitudinal studies. NeuroImage 2010, 49:2544-2555.
9. Eyigor O., Centers A., Jennes L. Distribution of ionotropic glutamate receptor subunit mRNAs in the rat hypothalamus. J. Comp. Neurol. 2001, 434:101-124.
10. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotaxic Coordinates 1997, Academic Press.
11. Gill S.S., Pulido O.M. Glutamate receptors in peripheral tissues: current knowledge, future research, and implications for toxicology. Toxicol. Pathol. 2001, 29:208-223.
12. Gillard S.E., Tzaferis J., Tsui H.C., Kingston A.E. Expression of metabotropic glutamate receptors in rat meningeal and brain microvasculature and choroid plexus. J. Comp. Neurol. 2003, 461:317-332.
13. Gsell W., Burke M., Wiedermann D., Bonvento G., Silva A.C., Dauphin F., Buhrle C., Hoehn M., Schwindt W. Differential effects of NMDA and AMPA glutamate receptors on functional magnetic resonance imaging signals and evoked neuronal activity during forepaw stimulation of the rat. J. Neurosci. 2006, 26:8409-8416.
14. Hankir M.K., Parkinson J.P., Minnion J.S., Addsion A.L., Bloom S.R., Bell J.D. PYY3-36 and pancreatic polypeptide differentially regulate mouse hypothalamic neuronal activity in vivo as determined by manganese enhanced magnetic resonance imaging. J. Neuroendocrinol. 2011, 23:371-380.
15. Hawkins R.A. The blood-brain barrier and glutamate. Am. J. Clin. Nutr. 2009.
16. Itoh K., Sakata M., Watanabe M., Aikawa Y., Fujii H. The entry of manganese ions into the brain is accelerated by the activation of N-methyl-D-aspartate receptors. Neuroscience 2008, 154:732-740.
17. Kia H.K., Yen G., Krebs C.J., Pfaff D.W. Colocalization of estrogen receptor alpha and NMDA-2D mRNAs in amygdaloid and hypothalamic nuclei of the mouse brain. Brain Res. Mol. Brain Res. 2002, 104:47-54.
18. Kuo Y.T., Herlihy A.H., So P.W., Bhakoo K.K., Bell J.D. In vivo measurements of T1 relaxation times in mouse brain associated with different modes of systemic administration of manganese chloride. J. Magn. Reson. Imaging 2005, 21:334-339.
19. Kuo Y.T., Herlihy A.H., So P.W., Bell J.D. Manganese-enhanced magnetic resonance imaging (MEMRI) without compromise of the blood-brain barrier detects hypothalamic neuronal activity in vivo. NMR Biomed. 2006, 19:1028-1034.
20. Kuo Y.T., Parkinson J.R., Chaudhri O.B., Herlihy A.H., So P.W., Dhillo W.S., Small C.J., Bloom S.R., Bell J.D. The temporal sequence of gut peptide CNS interactions tracked in vivo by magnetic resonance imaging. J. Neurosci. 2007, 27:12341-12348.
21. 2: dose-dependent and temporal evolution of T1 contrast. Magn. Reson. Med. 2005, 53:640-648.
22. Lehmann A., Jonsson T. MK-801 selectively protects mouse arcuate neurons in vivo against glutamate toxicity. NeuroReport 1992, 3:421-424.
23. Lin Y.J., Koretsky A.P. Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn. Reson. Med. 1997, 38:378-388.
24. Lu H., Xi Z.X., Gitajn L., Rea W., Yang Y., Stein E.A. Cocaine-induced brain activation detected by dynamic manganese-enhanced magnetic resonance imaging (MEMRI). Proc. Natl. Acad. Sci. U. S. A 2007, 104:2489-2494.
25. London R.E., Toney G., Gabel S.A., Funk A. Magnetic resonance imaging studies of the brains of anesthetized rats treated with manganese choride. Brain Res. Bull. 1989, 23:229-235.
26. Mayer M.L., Westbrook G.L. Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J. Physiol. 1987, 394:501-527.
27. Meng W., Tobin J.R., Busija D.W. Glutamate-induced cerebral vasodilation is mediated by nitric oxide through N-methyl-D-aspartate receptors. Stroke 1995, 26:857-862.
28. Mintz E.M., Marvel C.L., Gillespie C.F., Price K.M., Albers H.E. Activation of NMDA receptors in the suprachiasmatic nucleus produces light-like phase shifts of the circadian clock in vivo. J. Neurosci. 1999, 19:5124-5130.
29. Morita H., Ogino T., Seo Y., Fujiki N., Tanaka K., Takamata A., Nakamura S., Murakami M. Detection of hypothalamic activation by manganese ion contrasted T(1)-weighted magnetic resonance imaging in rats. Neurosci. Lett. 2002, 326:101-104.
30. Neves G., Cooke S.F., Bliss T.V. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 2008, 9:65-75.
31. O'Hara B.F., Andretic R., Heller H.C., Carter D.B., Kilduff T.S. GABAA, GABAC, and NMDA receptor subunit expression in the suprachiasmatic nucleus and other brain regions. Brain Res. Mol. Brain Res. 1995, 28:239-250.
32. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 1969, 164:719-721.
33. Pardridge W.M. CNS drug design based on principles of blood-brain barrier transport. J. Neurochem. 1998, 70:1781-1792.
34. Parker S.L., Crowley W.R. Stimulation of oxytocin release in the lactating rat by central excitatory amino acid mechanisms: evidence for specific involvement of R, S-alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid-sensitive glutamate receptors. Endocrinology 1993, 133:2847-2854.
35. Parkinson J.R., Chaudhri O.B., Bell J.D. Imaging appetite-regulating pathways in the central nervous system using manganese-enhanced magnetic resonance imaging. Neuroendocrinology 2009, 89:121-130.
36. Parkinson J.R., Chaudhri O.B., Kuo Y.T., Field B.C., Herlihy A.H., Dhillo W.S., Ghatei M.A., Bloom S.R., Bell J.D. Differential patterns of neuronal activation in the brainstem and hypothalamus following peripheral injection of GLP-1, oxyntomodulin and lithium chloride in mice detected by manganese-enhanced magnetic resonance imaging (MEMRI). NeuroImage 2009, 44:1022-1031.
37. Rabin O., Hegedus L., Bourre J.M., Smith Q.R. Rapid brain uptake of manganese(II) across the blood-brain barrier. J. Neurochem. 1993, 61:509-517.
38. Sagar S.M., Sharp F.R., Curan T. Expression of c fos in the brain: metabolic mapping at the cellular level. Science 1988, 240:1328-1331.
39. Schmitt C., Strazielle N., Richaud P., Bouron A., Ghersi Egei E.F. Active transport at the blood-CSF barrier contributes to manganese influx into the brain. J. Neurochem. 2011, 117:747-756.
40. Shin S.W., Park J.W., Suh M.H., Suh S.I., Choe B.K. Persistent expression of Fas/FasL mRNA in the mouse hippocampus after a singleNMDA injection. J. Neurochem. 1998, 71:1773-1776.
41. Smyth C.E., Natarajan M., Wilkinson M. Neonatal hypothalamic c-fos expression in an excitotoxicity-induced model of precocious puberty. Brain Res. Dev. Brain Res. 1997, 104:153-162.
42. van den Pol A.N., Wuarin J.P., Dudek F.E. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 1990, 250:1276-1278.
43. van den Pol A.N., Hermans-Borgmeyer I., Hofer M., Ghosh P., Heinemann S. Ionotropic glutamate-receptor gene expression in hypothalamus: localization of AMPA, kainate, and NMDA receptor RNA with in situ hybridization. J. Comp. Neurol. 1994, 343:428-444.
44. Walker R., Lupien J.R. The safety evaluation of monosodium glutamate. J. Nutr. 2000, 130:1049S-1052S.
45. Watkins J.C., Jane D.E. The glutamate story. Br. J. Pharmacol. 2006, 147(Suppl. 1):S100-S108.
46. Xu Z., Herbert J. Effects of intracerebroventricular dizocilpine (MK801) on dehydration-induced dipsogenic responses, plasma vasopressin and c-fos expression in the rat forebrain. Brain Res. 1998, 784:91-99.