Neonatal alcohol-induced region-dependent changes in rat brain neurochemistry measured by high-resolution magnetic resonance spectroscopy

Alcoholism: Clinical and Experimental Research

Volumn 32, Issue 10, 2008, Pages 1697-1707

  O'Leary Moore, Shonagh K ^a,b   McMechan, Andrew P ^b   Galloway, Matthew P ^b   Hannigan, John H ^b,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal model (rat); Fetal alcohol syndrome; Glutamate; N acetyl aspartate

Indexed keywords

4 AMINOBUTYRIC ACID; ALCOHOL; CHOLINE; CREATININE; GLUTAMIC ACID; GLUTAMINE; INOSITOL; N ACETYLASPARTIC ACID; TAURINE;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; CORPUS STRIATUM; EX VIVO STUDY; FEMALE; FETAL ALCOHOL SYNDROME; FRONTAL CORTEX; HIPPOCAMPUS; LONG TERM EXPOSURE; MALE; NEUROCHEMISTRY; NEUROIMAGING; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT;

AMINO ACIDS; ANIMALS; ANIMALS, NEWBORN; ASPARTIC ACID; BODY WEIGHT; CEREBELLUM; CEREBRUM; CHOLINE; ETHANOL; FEMALE; MALE; PREGNANCY; RATS; TAURINE;

ANIMALIA; RATTUS;

EID: 52149116725     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2008.00747.x     Document Type: Article

References (79)

1. Abel EL, Hannigan JH (1995) Maternal risk factors in fetal alcohol syndrome: provocative and permissive influences. Neurotoxicol Teratol 17 : 448 462.
2. Abel EL, Sokol RJ (1991) A revised conservative estimate of the incidence of FAS and its economic impact. Alcohol Clin Exp Res 15 : 514 524.
3. Aerts L, Van Assche FA (2002) Taurine and taurine deficiency in the perinatal period. J Perinat Med 30 : 281 286.
4. Archibald SL, Fennema-Notestine C, Gamst A, Riley EP, Mattson SN, Jernigan TL (2001) Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol 43 : 148 154. [Erratum appears in Dev Med Child Neurol (2001) 43, 504].
5. Astley SJ, Weinberger E, Shaw DWW, Richards TL, Clarren SK (1995) Magnetic resonance imaging and spectroscopy in fetal ethanol exposed macaca nemestrina. Neurotoxicol Teratol 17 : 523 530.
6. Bertrand J, Floyd LL, Weber MK, the Fetal Alcohol Syndrome Prevention Team, Division of Birth Defects and Developmental Disabilities, National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention (CDC) (2005) Guidelines for identifying and referring persons with fetal alcohol syndrome. MMRW 54 : 1 14.
7. Bonavita S, Di Salle F, Tedeschi G (1999) Proton MRS in neurological disorders. Eur J Radiol 30 : 125 131.
8. Burd L, Cotsonas-Hassler TM, Martsoff JT, Kerbeshian J (2003) Recognition and management of fetal alcohol syndrome. Neurotoxicol Teratol 25 : 681 688.
9. Bustillo J, Barrow R, Paz R, Tang J, Seraji-Bozorgzad N, Moore GJ, Bolognani F, Lauriello J, Perrone-Bizzozero N, Galloway MP (2006) Long-term treatment of rats with haloperidol: lack of an effect on brain N-acetyl aspartate levels. Neuropsychopharmacology 31 : 751 756.
10. Cavassila S, Deval S, Huegen C, van Ormondt D, Graveron-Demilly D (2001) Cramér-Rao bounds: an evaluation tool for quantitation. NMR Biomed 14 : 278 283.
11. Ceccanti M, Alessandra Spagnolo P, Tarani L, Luisa Attilia M, Chessa L, Mancinelli R, Stegagno M, Francesco Sasso G, Romeo M, Jones KL, Robinson LK, Del Campo M, Gossage JP, May PA, Hoyme HE (2007) Clinical delineation of fetal alcohol spectrum disorders (FASD) in Italian children: comparison and contrast with other racial/ethnic groups and implications for diagnosis and prevention. Neurosci Biobehav Rev 31 : 270 277.
12. Center for Disease Control (2004) Alcohol consumption among women who are pregnant or might become pregnant - United States, 2000. MMWR 53 : 1178 1181.
13. Cheng LL, Ma MJ, Becerra L, Ptak T, Tracey I, Lackner A, Gonzales RG (1997) Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy. Proc Natl Acad Sci U S A 94 : 6408 6413.
14. Cohen-Kerem R, Koren G (2003) Antioxidants and fetal protection against alcohol teratogenicity 1: review of the experimental data and implications to humans. Neurotoxicol Teratol 25 : 1 9.
15. Cortese BM, Moore GJ, Bailey BA, Jacobson SW, Delaney-Black V, Hannigan JH (2006) Magnetic resonance spectroscopic imaging in prenatal alcohol-exposed children: Preliminary findings in the caudate nucleus. Neurotoxicol Teratol 28 : 597 606.
16. Danielsen ER, Ross B (1999) Magnetic Resonance Spectroscopy Diagnosis of Neurological Diseases. Marcel Dekker, New York.
17. Espina N, Hannigan JH, Martin DL (1989) Neuroactive amino acid levels following prenatal exposure to ethanol. Alcohol Clin Exp Res 13 : 319.
18. Fagerlund A, Heikkinen S, Autti-Ramo I, Korkman M, Timonen M, Kuusi T, Riley EP, Lundbom N (2006) Brain metabolic alterations in adolescents and young adults with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 30 : 2097 2104.
19. 3H-glutamate binding in 45 day old rats. Alcohol 5 : 125 133.
20. Goodlett CR, Horn KM (2001) Mechanisms of alcohol-induced damage to the developing nervous system. Alcohol Res Health 25 : 175 184.
21. Goodlett CR, Johnson TB (1997) Neonatal binge ethanol exposure using intubation: timing and dose effects on place learning. Neurotoxicol Teratol 19 : 435 466.
22. Goodlett CR, Lundhal KR (1996) Temporal determinants of neonatal alcohol-induced cerebellar damage and motor performance deficits. Pharmacol Biochem Behav 55 : 531 540.
23. Goodlett CR, Pearlman AD, Lundahl KR (1998) Binge neonatal alcohol intubations induce dose-dependent loss of Purkinje cells. Neurotoxicol Teratol 20 : 285 292.
24. Goodlett CR, Peterson SD (1995) Sex differences in vulnerability to developmental spatial learning deficits induced by limited binge alcohol exposure in neonatal rats. Neurobiol Learn Mem 64 : 265 275.
25. Green JT, Johnson TB, Goodlett CR, Steinmetz JE (2002) Eyeblink classical conditioning and interpositus nucleus activity are disrupted in adult rats exposed to ethanol as neonates. Learn Mem 9 : 304 320.
26. Green JT, Tran T, Steinmetz JE, Goodlett CR (2000) Neonatal ethanol produces cerebellar deep nuclear cell loss and correlated disruption of eyeblink conditioning in adult rats. Brain Res 956 : 302 311.
27. Griezerstein HB, Aldrich LK (1983) Ethanol and diazepam effects on intrauterine growth of the rat. Dev Pharmacol Ther 6 : 409 418.
28. Griffin JL, Bollard M, Nicholson JK, Bhakoo K (2002) Spectral profiles of cultured neuronal and glial cells derived from HRMAS (1)H NMR spectroscopy. NMR Biomed 15 : 375 384.
29. 1H nuclear magnetic resonance spectroscopic imaging of neuronal loss in the rat brain. Neuroscience 69 : 1095 1101.
30. Hamilton DA, Petropoulos H, Kodituwakku P, Tesche CD, Sutherland RJ, Savage DD (2003) Functional, morphological, and spectroscopic measurement of the hippocampus in fetal alcohol syndrome. Alcohol Clin Exp Res 27 : Abstract #217.
31. Hannigan JH (1996) What research with animals is telling us about alcohol-related neurodevelopmental disorders. Pharmacol Biochem Behav 55 : 489 500.
32. Hannigan JH, O'Leary-Moore SK, Berman RF (2007) Postnatal environmental or experiential amelioration of neurobehavioral effects of perinatal alcohol exposure in rats. Neurosci Biobehav Rev 31 : 202 211.
33. 1H-NMR spectroscopy. J Neurochem 68 : 305 312.
34. Heaton MB, Mitchell JJ, Paiva M (2000) Amelioration of ethanol-induced neurotoxicity in the neonatal rat central nervous system by antioxidant therapy. Alcohol Clin Exp Res 24 : 512 518.
35. Hoehn M, Nicolay K, Franke C, van der Sanden B (2001) Application of magnetic resonance to animal models of cerebral ischemia. J Magn Reson Imaging 14 : 491 509.
36. Horska A, Kaufmann WE, Brant LJ, Naidu S, Harris JC, Barker PB (2002) In vivo quantitative proton MRSI study of brain development from childhood to adolescence. J Magn Reson Imaging 15 : 137 143.
37. Hoyme HE, May PA, Kalberg WO, Kodituwakku P, Gossage JP, Trujillo PM, Buckley DG, Miller JH, Aragon AS, Khaole N, Viljoen DL, Jones KL, Robinson LK (2005) A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 115 : 39 47.
38. Huppi PS, Inder TE (2001) Magnetic resonance techniques in the evaluation of the perinatal brain: recent advances and future direction. Semin Neonatol 6 : 195 210.
39. Jansen JF, Backes WH, Nicolay K, Kooi ME (2006) 1H MR spectroscopy of the brain: absolute quantification of metabolites. Radiology 240 : 318 332.
40. Jones K, Smith D (1973) Recognition of the fetal alcohol syndrome in early infancy. The Lancet 2 : 999 1001.
41. Kahne D, Tudorica A, Borella A, Shapiro L, Johnstone F, Huang W, Whitaker-Azmitia PM (2002) Behavioral and magnetic resonance spectroscopic studies in the rat hyperserotonemic model of autism. Physiol Behav 75 : 403 410.
42. Kelly GM, Druse MJ, Tonetti DA, Oden BG (1986) Maternal ethanol consumption: binding of L-glutamate to synaptic membranes from whole brain, cortices, and cerebella of offspring. Exp Neurol 91 : 219 228.
43. Li BSY, Wang H, Gonen O (2003) Metabolic ratios to assumed stable creatine level may confound quantification of proton brain MR spectroscopy. Magn Reson Imaging 21 : 923 928.
44. Light KE, Kane CJM, Pierce DR, Jenkins D, Ge Y, Brown G, Yang H, Nyamweya N (1998) Intragastric intubation: important aspects of the model for administration of ethanol to rat pups during the postnatal period. Alcohol Clin Exp Res 22 : 1600 1606.
45. Maier SE, Chen WJ, West JR (1996) Prenatal binge-like alcohol exposure alters neurochemical profiles in the fetal rat brain. Pharmacol Biochem Behav 55 : 521 529.
46. Maier SE, Miller JA, Blackwell JM, West JR (1999) Fetal alcohol exposure and temporal vulnerability: regional differences in cell loss as a function of the timing of binge-like alcohol exposure during brain development. Alcohol Clin Exp Res 23 : 726 734.
47. Maier SE, West JR (2001) Regional differences in cell loss associated with binge-like alcohol exposure during the first two trimesters equivalent in rats. Alcohol 23 : 49 57.
48. Malisza KL, Kozlowski P, Ning G, Bascaramurty S, Tour UI (1999) Metabolite changes in neonatal rat brain during and after cerebral hypoxia-ischemia: a magnetic resonance spectroscopic imaging study. NMR Biomed 12 : 31 38.
49. Mattson SN, Riley EP, Sowell ER, Jernigan TL, Sobel DF, Jones KL (1996) A decrease in the size of the basal ganglia in children with fetal alcohol syndrome. Alcohol Clin Exp Res 20 : 1088 1093.
50. May PA, Gossage JP (2001) Estimating the prevalence of fetal alcohol syndrome. A summary. Alcohol Res Health 25 : 159 167.
51. Mena MA, Salinas M, Del Rio R, Herrara E (1982) Effects of maternal ethanol ingestion on cerebral neurotransmitters and cyclic-amp in rat offspring. Gen Pharm 13 : 241 248.
52. Michaelis EK (1990) Fetal alcohol exposure: cellular toxicity and molecular events involved in toxicity. Alcohol Clin Exp Res 14 : 819 826.
53. Moffett JR, Ross B, Arun P, Madhavarao CN, Namboodiri AMA (2007) N-acetyl-aspartate in the CNS: from neurodiagnostics to neurobiology. Prog Neurobiol 81 : 89 131.
54. Moloney B, Leonard BE (1984) Pre-natal and post-natal effects of alcohol in the rat II: changes in gamma-aminobutyric acid concentration and adenosine triphosphatase activity in the brain. Alcohol Alcohol 19 : 137 140.
55. Moore GJ (1998) Proton magnetic resonance spectroscopy in pediatric patients. Pediatr Radiol 28 : 805 814.
56. Moore GJ, Galloway MP (2002) Magnetic resonance spectroscopy: neurochemistry and treatment effects in affective disorders. Psychopharmacol Bull 36 : 1 23.
57. O'Leary-Moore SK, Galloway MP, McMechan AP, Hannigan JH, Bowen SE (2007) Region-dependent alterations in glutamate and GABA measured by high-resolution magnetic resonance spectroscopy following acute binge inhalation of toluene in juvenile rats. Neurotoxicol Teratol 29 : 466 475.
58. O'Leary-Moore SK, McMechan AP, Mathison SN, Berman RF, Hannigan JH (2006) Reversal learning deficits following fetal alcohol exposure: period of exposure and age at testing effects. Alcohol 38 : 99 110.
59. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates, 4th ed. Academic Press, San Diego, CA.
60. 1H MRS are reduced in adult male rats subjected to perinatal stress: preliminary observations and hypothetical implications for neurodevelopmental disorders. J Psychiatr Res 33 : 41 51.
61. Provencher SW (2001) Automatic quantification of localized in vivo 1H spectra with LCModel. NMR Biomed 14 : 260 264.
62. Raman L, Tkac I, Ennis K, Georgieff MK, Gruetter R, Rao R (2005) In vivo effect of chronic hypoxia on the neurochemical profile of the developing rat hippocampus. Dev Brain Res 156 : 202 209.
63. Rawat AK (1977) Developmental changes in the rat brain levels of neurotransmitters as influenced by maternal ethanol consumption in the rat. J Neurochem 28 : 1175 1182.
64. Riley EP, McGee CL (2005) Fetal alcohol spectrum disorders: an overview with emphasis on changes in brain and behavior. Exp Biol Med 230 : 357 365.
65. Riley EP, McGee CL, Sowell ER (2004) Teratogenic effects of alcohol: a decade of brain imaging. Am J Med Genet Part C, Semin Med Genet 127 : 35 41.
66. Roebuck TM, Mattson SN, Riley EP (1998) A review of the neuroanatomical findings in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 22 : 339 344.
67. Sampson PD, Streissguth AP, Bookstein FL, Little RE, Clarren SK, Dehaene P, Hanson JW, Graham JM Jr (1997) Incidence of fetal alcohol syndrome and prevalence of alcohol-related neurodevelopmental disorder. Teratology 56 : 317 326.
68. Smith AM, Zeve DR, Grisel JJ, Chen WJ (2005) Neonatal alcohol exposure increases malondialdehyde (MDA) and glutathione (GSH) levels in the developing cerebellum. Brain Res Dev Brain Res 160 : 231 238.
69. Sowell ER, Jernigan TL, Mattson SN, Riley EP, Sobel DF, Jones KL (1996) Abnormal development of the cerebellar vermis in children prenatally exposed to alcohol: size reduction in lobules I-V. Alcohol Clin Exp Res 20 : 31 34.
70. Spadoni AD, McGee CL, Fryer SL, Riley EP (2007) Neuroimaging and fetal alcohol spectrum disorders. Neurosci Biobehav Rev 31 : 239 245.
71. Stanley JA, Pettigrew JW, Keshevan MS (2000) Magnetic resonance spectroscopy in schizophrenia: methodological issues and findings-part I. Biol Psychiatry 48 : 357 368.
72. Stanton ME, Goodlett CR (1998) Neonatal ethanol exposure impairs eyeblink conditioning in weanling rats. Alcohol Clin Exp Res 22 : 270 275.
73. Thomas JD, Biane JS, O'Bryan KA, O'Neill TM, Dominguez HD (2007) Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav Neurosci 121 : 120 130.
74. Thomas JD, Garrison M, O'Neill TM (2004) Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 26 : 35 45.
75. 1H NMR spectroscopy. Magn Reson Med 50 : 24 32.
76. 1H nuclear magnetic resonance spectroscopy. Magn Reson Med 53 : 1018 1024.
77. Viljoen DL, Gossage JP, Brooke L, Adnams CM, Jones KL, Robinson LK, Hoyme HE, Snell C, Khaole NC, Kodituwakku P, Asante KO, Findlay R, Quinton B, Marais AS, Kalberg WO, May PA (2005) Fetal alcohol syndrome epidemiology in a South African community: a second study of a very high prevalence area. J Stud Alcohol 66 : 593 604.
78. Wilken B, Dechent P, Herms J, Maxton C, Markakis E, Hanefeld F, Frahm J (2000) Quantitative proton magnetic resonance spectroscopy of focal brain lesions. Pediatr Neurol 3 : 22 31.
79. Yao FS, Caserta MT, Wyrwicz AM (1999) In vitro proton and phosphorus NMR spectroscopic analysis of murine (C57Bl/6J) brain development. NMR Biomed 12 : 463 470.