An imbalance between excitatory and inhibitory neurotransmitters in amyotrophic lateral sclerosis revealed by use of 3-t proton magnetic resonance spectroscopy

JAMA Neurology

Volumn 70, Issue 8, 2013, Pages 1009-1016

  Foerster, Bradley R ^a,c,d   Pomper, Martin G ^d   Callaghan, Brian C ^a   Petrou, Myria ^d   Edden, Richard A E ^d,e   Mohamed, Mona A ^d,e   Welsh, Robert C ^b   Carlos, Ruth C ^a   Barker, Peter B ^d,e   Feldman, Eva L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLINE; CREATININE; GLUTAMIC ACID; GLUTAMINE; INOSITOL; N ACETYLASPARTIC ACID; RILUZOLE;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BRAIN REGION; CASE CONTROL STUDY; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; MALE; MOLECULAR PATHOLOGY; MOTOR CORTEX; NEUROTRANSMISSION; PONS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; WHITE MATTER;

EID: 84882447354     PISSN: 21686149     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamaneurol.2013.234     Document Type: Article

References (48)

1. Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009;8(1):94-109.
2. Kiernan MC, Vucic S, Cheah BC, et al. Amyotrophic lateral sclerosis. Lancet. 2011;377(9769):942-955.
3. Swash M. Why are upper motor neuron signs difficult to elicit in amyotrophic lateral sclerosis? J Neurol Neurosurg Psychiatry. 2012;83(6): 659-662.
4. Miller RG, Mitchell JD, Lyon M, Moore DH. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst Rev. 2007;(1):CD001447.
5. Lacomblez L, Bensimon G, Leigh PN, Guillet P, Meininger V; Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Lancet. 1996;347(9013):1425-1431.
6. Doble A. The pharmacology and mechanism of action of riluzole. Neurology. 1996;47(6)(suppl 4):S233-S241.
7. Turner MR, Modo M. Advances in the application of MRI to amyotrophic lateral sclerosis. Expert Opin Med Diagn. 2010;4(6):483-496.
8. Gujar SK, Maheshwari S, Bjorkman-Burtscher I, Sundgren PC.Magnetic resonance spectroscopy. J Neuroophthalmol. 2005;25(3):217-226.
9. Mescher M, Merkle H, Kirsch J, Garwood M, Gruetter R. Simultaneous in vivo spectral editing and water suppression. NMR Biomed. 1998;11(6):266-272.
10. Edden RA, Barker PB. Spatial effects in the detection of gamma-aminobutyric acid: improved sensitivity at high fields using inner volume saturation. Magn Reson Med. 2007;58(6):1276- 1282.
11. Turner MR, Kiernan MC. Does interneuronal dysfunction contribute to neurodegeneration in amyotrophic lateral sclerosis? Amyotroph Lateral Scler. 2012;13(3):245-250.
12. Agosta F, Chio A, CosottiniM, et al. The present and the future of neuroimaging in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. 2010;31(10):1769-1777.
13. Kalra S, Cashman NR, Genge A, Arnold DL. Recovery of N-acetylaspartate in corticomotor neurons of patients with ALS after riluzole therapy. Neuroreport. 1998;9(8):1757-1761.
14. Kalra S, Tai P, Genge A, Arnold DL. Rapid improvement in cortical neuronal integrity in amyotrophic lateral sclerosis detected by proton magnetic resonance spectroscopic imaging. J Neurol. 2006;253(8):1060-1063.
15. Foerster BR, Callaghan BC, PetrouM, Edden RA, Chenevert TL, Feldman EL. Decreased motor cortex γ-aminobutyric acid in amyotrophic lateral sclerosis. Neurology. 2012;78(20):1596-1600.
16. Brooks BR,Miller RG, Swash M, Munsat TL; World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1(5):293-299.
17. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206-207.
18. Turner MR, Cagnin A, Turkheimer FE, et al. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis. 2004;15(3):601-609.
19. Ellis CM, Simmons A, Jones DK, et al. Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology. 1999;53(5):1051-1058.
20. Smith RA, Berg JE, Pope LE, Thisted RA. Measuring pseudobulbar affect in ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 2004;5(suppl 1):99-102.
21. Provencher SW. Estimation ofmetabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med. 1993;30(6):672-679.
22. Stagg CJ, Best JG, Stephenson MC, et al. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J Neurosci. 2009;29(16):5202-5206.
23. Rothstein JD. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol. 2009;65(suppl 1):S3-S9.
24. Kiernan MC, Petri S. Hyperexcitability and amyotrophic lateral sclerosis. Neurology. 2012;78(20):1544-1545.
25. Douaud G, Filippini N, Knight S, Talbot K, Turner MR. Integration of structural and functional magnetic resonance imaging in amyotrophic lateral sclerosis. Brain. 2011;134(pt 12):3470-3479.
26. Nieto-Gonzalez JL, Moser J, Lauritzen M, Schmitt-John T, Jensen K. Reduced GABAergic inhibition explains cortical hyperexcitability in the wobbler mouse model of ALS. Cereb Cortex. 2011;21(3):625-635.
27. Petri S, Krampfl K, Hashemi F, et al. Distribution of GABAA receptor mRNA in the motor cortex of ALS patients. J Neuropathol Exp Neurol. 2003;62(10):1041-1051.
28. Turner MR, Osei-Lah AD, Hammers A, et al. Abnormal cortical excitability in sporadic but not homozygous D90A SOD1 ALS. J Neurol Neurosurg Psychiatry. 2005;76(9):1279-1285.
29. Puts NA, Edden RA. In vivomagnetic resonance spectroscopy of GABA: amethodological review. Prog Nucl Magn Reson Spectrosc. 2012;60:29-41.
30. Tkac I, Oz G, AdrianyG,Uǧurbil K, Gruetter R. In vivo 1H NMR spectroscopy of the human brain at high magnetic fields: metabolite quantification at 4T vs. 7T. Magn Reson Med. 2009;62(4):868-879.
31. Cheah BC, Vucic S, Krishnan AV, Kiernan MC. Riluzole, neuroprotection and amyotrophic lateral sclerosis. Curr Med Chem. 2010;17(18):1942-1959.
32. Cifra A, Mazzone GL, Nistri A. Riluzole: what it does to spinal and brainstem neurons and how it does it. Neuroscientist. 2013;19(2):137-144.
33. Lamanauskas N, Nistri A. Riluzole blocks persistent Na+ and Ca2+ currents and modulates release of glutamate via presynaptic NMDA receptors on neonatal rat hypoglossal motoneurons in vitro. Eur J Neurosci. 2008;27(10):2501-2514.
34. Albo F, Pieri M, Zona C. Modulation of AMPA receptors in spinal motor neurons by the neuroprotective agent riluzole. J Neurosci Res. 2004;78(2):200-207.
35. Fumagalli E, Funicello M, Rauen T, Gobbi M, Mennini T. Riluzole enhances the activity of glutamate transporters GLAST, GLT1 and EAAC1. Eur J Pharmacol. 2008;578(2-3):171-176.
36. He Y, Benz A, Fu T, et al. Neuroprotective agent riluzole potentiates postsynaptic GABA(A) receptor function. Neuropharmacology. 2002;42(2): 199-209.
37. Mantz J, Laudenbach V, Lecharny JB, Henzel D, Desmonts JM. Riluzole, a novel antiglutamate, blocks GABA uptake by striatal synaptosomes. Eur J Pharmacol. 1994;257(1-2):R7-R8.
38. Stefan K, Kunesch E, Benecke R, Classen J. Effects of riluzole on cortical excitability in patients with amyotrophic lateral sclerosis. Ann Neurol. 2001;49(4):536-539.
39. Schwenkreis P, Liepert J,Witscher K, et al. Riluzole suppresses motor cortex facilitation in correlation to its plasma level: a study using transcranial magnetic stimulation. Exp Brain Res. 2000;135(3):293-299.
40. Filippini N, Douaud G, Mackay CE, Knight S, Talbot K, Turner MR. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology. 2010;75(18):1645-1652.
41. Iwata NK, Kwan JY, Danielian LE, et al. White matter alterations differ in primary lateral sclerosis and amyotrophic lateral sclerosis. Brain. 2011;134(pt 9):2642-2655.
42. Storch A, Burkhardt K, Ludolph AC, Schwarz J. Protective effects of riluzole on dopamine neurons: involvement of oxidative stress and cellular energy metabolism. J Neurochem. 2000;75(6):2259-2269.
43. BlockW, Karitzky J, Traber F, et al. Proton magnetic resonance spectroscopy of the primary motor cortex in patients with motor neuron disease: subgroup analysis and follow-up measurements. Arch Neurol. 1998;55(7):931-936.
44. Bowen BC, Pattany PM, Bradley WG, et al. MR imaging and localized proton spectroscopy of the precentral gyrus in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. 2000;21(4):647-658.
45. Kalra S, Hanstock CC, Martin WR, Allen PS, JohnstonWS. Detection of cerebral degeneration in amyotrophic lateral sclerosis using high-field magnetic resonance spectroscopy. Arch Neurol. 2006;63(8):1144-1148.
46. Pioro EP, Majors AW, Mitsumoto H, Nelson DR, Ng TC. 1H-MRS evidence of neurodegeneration and excess glutamate + glutamine in ALS medulla. Neurology. 1999;53(1):71-79.
47. Han J, Ma L. Study of the features of proton MR spectroscopy ((1)H-MRS) on amyotrophic lateral sclerosis. J Magn Reson Imaging. 2010;31(2): 305-308.
48. BradleyWG, Bowen BC, Pattany PM, Rotta F. 1H-magnetic resonance spectroscopy in amyotrophic lateral sclerosis. J Neurol Sci. 1999;169(1-2):84-86.