Impact of family history of alcoholism on glutamine/glutamate ratio in anterior cingulate cortex in substance-naïve adolescents

Developmental Cognitive Neuroscience

Volumn 16, Issue , 2015, Pages 147-154

  Cohen Gilbert, Julia E ^a,b   Sneider, Jennifer T ^a,b   Crowley, David J ^a,b   Rosso, Isabelle M ^a,b   Jensen, J Eric ^a,b   Silveri, Marisa M ^a,b  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Adolescence; Alcoholism; Family history; Glutamate; Impulsivity; MRS

Indexed keywords

GLUTAMIC ACID; GLUTAMINE;

ADOLESCENT; ADULT; AGE; ALCOHOLISM; AMINO ACID BRAIN LEVEL; ANTERIOR CINGULATE; ARTICLE; CELL METABOLISM; CHILD; COMPARATIVE STUDY; CORRELATIONAL STUDY; FAMILY HISTORY; FEMALE; GENETIC RISK; HUMAN; HUMAN EXPERIMENT; IMPULSE CONTROL DISORDER; IMPULSIVENESS; MALE; METABOLIC RATE; METABOLITE; NEUROTRANSMISSION; NORMAL HUMAN; OCCIPITAL CORTEX; PARIETO OCCIPITAL CORTEX; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTON NUCLEAR MAGNETIC RESONANCE; SELF REPORT; AGING; BRAIN CHEMISTRY; CINGULATE GYRUS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; YOUNG ADULT;

ADOLESCENT; AGING; ALCOHOLISM; BRAIN CHEMISTRY; CHILD; FEMALE; GLUTAMIC ACID; GLUTAMINE; GYRUS CINGULI; HUMANS; IMPULSIVE BEHAVIOR; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; YOUNG ADULT;

EID: 84929774171     PISSN: 18789293     EISSN: 18789307     Source Type: Journal    
DOI: 10.1016/j.dcn.2015.04.005     Document Type: Article

References (53)

1. Alterman, A.I., Searles, J.S., Hall, J.G., Failure to find differences in drinking behavior as a function of familial risk for alcoholism: a replication. J. Abnorm. Psychol. 98:1 (1989), 50–53.
2. Behar, K.L., Rothman, D.L., In vivo nuclear magnetic resonance studies of glutamate-gamma-aminobutyric acid-glutamine cycling in rodent and human cortex: the central role of glutamine. J. Nutr. 131:9 Suppl. (2001), 2498S–2504S discussion 2523S–2494S.
3. Biederman, J., Faraone, S.V., Monuteaux, M.C., Feighner, J.A., Patterns of alcohol and drug use in adolescents can be predicted by parental substance use disorders. Pediatrics 106:4 (2000), 792–797.
4. Casey, B.J., Jones, R.M., Hare, T.A., The adolescent brain. Ann. N.Y. Acad. Sci. 1124:1 (2008), 111–126, 10.1196/annals.1440.010.
5. Choi, I.-Y., Lee, S.-P., Merkle, H., Shen, J., In vivo detection of gray and white matter differences in GABA concentration in the human brain. Neuroimage 33:1 (2006), 85–93, 10.1016/j.neuroimage.2006.06.016.
6. Cohen-Gilbert, J.E., Jensen, J.E., Silveri, M.M., Contributions of magnetic resonance spectroscopy to understanding development: potential applications in the study of adolescent alcohol use and abuse. Dev. Psychopathol. 26:02 (2014), 405–423, 10.1017/S0954579414000030.
7. Conway, K.P., Swendsen, J.D., Merikangas, K.R., Alcohol expectancies, alcohol consumption, and problem drinking: the moderating role of family history. Addict. Behav. 28:5 (2003), 823–836, 10.1016/S0306-4603(02)00265-4.
8. DeVito, E.E., Meda, S.A., Jiantonio, R., Potenza, M.N., Krystal, J.H., Pearlson, G.D., Neural correlates of impulsivity in healthy males and females with family histories of alcoholism. Neuropsychopharmacology 38:10 (2013), 1854–1863, 10.1038/npp.2013.92.
9. Finn, P.R., Justus, A., Mazas, C., Steinmetz, J.E., Working memory, executive processes and the effects of alcohol on Go/No-Go learning: testing a model of behavioral regulation and impulsivity. Psychopharmacology (Berl) 146:4 (1999), 465–472, 10.1007/PL00005492.
10. Fossati, A., Barratt, E.S., Acquarini, E., Di Ceglie, A., Psychometric properties of an adolescent version of the Barratt Impulsiveness Scale-11 for a sample of Italian high school students. Percept. Mot. Skills 95:2 (2002), 621–635, 10.2466/pms.2002.95.2.621.
11. Gass, J.T., Olive, M.F., Glutamatergic substrates of drug addiction and alcoholism. Biochem. Pharmacol. 75:1 (2008), 218–265, 10.1016/j.bcp.2007.06.039.
12. Gierski, F., Hubsch, B., Stefaniak, N., Benzerouk, F., Cuervo-Lombard, C., Bera-Potelle, C., Cohen, R., Kahn, J.P., Limosin, F., Executive functions in adult offspring of alcohol-dependent probands: toward a cognitive endophenotype?. Alcohol Clin. Exp. Res. 37:s1 (2013), E356–E363, 10.1111/j.1530-0277.2012.01903.x.
13. Gleich, T., Lorenz, R.C., Pöhland, L., Raufelder, D., Deserno, L., Beck, A., Heinz, A., Kühn, S., Gallinat, J., Frontal glutamate and reward processing in adolescence and adulthood. Brain Struct. Funct., 2014, 10.1007/s00429-014-0844-3.
14. Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., Nugent, T.F. 3rd, Herman, D.H., Clasen, L.S., Toga, A.W., Rapoport, J.L., Thompson, P.M., Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U. S. A. 101:21 (2004), 8174–8179, 10.1073/pnas.0402680101.
15. Grachev, I.D., Apkarian, A.V., Chemical heterogeneity of the living human brain: a proton MR spectroscopy study on the effects of sex, age, and brain region. Neuroimage 11:5 (2000), 554–563, 10.1006/nimg.2000.0557.
16. Hadel, S., Wirth, C., Rapp, M., Gallinat, J., Schubert, F., Effects of age and sex on the concentrations of glutamate and glutamine in the human brain. J. Magn. Reson. Imaging 38:6 (2013), 1480–1487, 10.1002/jmri.24123.
17. Hardee, J.E., Weiland, B.J., Nichols, T.E., Welsh, R.C., Soules, M.E., Steinberg, D.B., Zubieta, J.K., Zucker, R.A., Heitzeg, M.M., Development of impulse control circuitry in children of alcoholics. Biol. Psychiatry 76:9 (2014), 708–716, 10.1016/j.biopsych.2014.03.005.
18. Hermann, D., Weber-Fahr, W., Sartorius, A., Hoerst, M., Frischknecht, U., Tunc-Skarka, N., Perreau-Lenz, S., Hansson, A.C., Krumm, B., Kiefer, F., Spanagel, R., Mann, K., Ende, G., Sommer, W.H., Translational magnetic resonance spectroscopy reveals excessive central glutamate levels during alcohol withdrawal in humans and rats. Biol. Psychiatry 71:11 (2012), 1015–1021, 10.1016/j.biopsych.2011.07.034.
19. Hill, S.Y., Shen, S., Lowers, L., Locke, J., Factors predicting the onset of adolescent drinking in families at high risk for developing alcoholism. Biol. Psychiatry 48:4 (2000), 265–275, 10.1016/S0006-3223(00)00841-6.
20. Hoerst, M., Weber-Fahr, W., Tunc-Skarka, N., Ruf, M., Bohus, M., Schmahl, C., Ende, G., Correlation of glutamate levels in the anterior cingulate cortex with self-reported impulsivity in patients with borderline personality disorder and healthy controls. Arch. Gen. Psychiatry 67:9 (2010), 946–954.
21. Hu, J., Yang, S., Xuan, Y., Jiang, Q., Yang, Y., Haacke, E.M., Simultaneous detection of resolved glutamate, glutamine, and gamma-aminobutyric acid at 4T. J. Magn. Reson. 185:2 (2007), 204–213, 10.1016/j.jmr.2006.12.010.
22. Jamadar, S., DeVito, E.E., Jiantonio, R.E., Meda, S.A., Stevens, M.C., Potenza, M.N., Krystal, J.H., Pearlson, G.D., Memantine, an NMDA receptor antagonist, differentially influences Go/No-Go performance and fMRI activity in individuals with and without a family history of alcoholism. Psychopharmacology (Berl.) 222:1 (2012), 129–140, 10.1007/s00213-011-2628-2.
23. Jensen, J.E., Licata, S.C., Öngür, D., Friedman, S.D., Prescot, A.P., Henry, M.E., Renshaw, P.F., Quantification of J-resolved proton spectra in two-dimensions with LCModel using GAMMA-simulated basis sets at 4 Tesla. NMR Biomed. 22:7 (2009), 762–769, 10.1002/nbm.1390.
24. Kaiser, L.G., Schuff, N., Cashdollar, N., Weiner, M.W., Age-related glutamate and glutamine concentration changes in normal human brain: 1H MR spectroscopy study at 4T. Neurobiol. Aging 26:5 (2005), 665–672.
25. Krystal, J.H., Petrakis, I.L., Mason, G., Trevisan, L., D'Souza, D.C., N-methyl-D-aspartate glutamate receptors and alcoholism: reward, dependence, treatment, and vulnerability. Pharmacol. Ther. 99:1 (2003), 79–94, 10.1016/S0163-7258(03)00054-8.
26. Leland, D.S., Arce, E., Miller, D.A., Paulus, M.P., Anterior cingulate cortex and benefit of predictive cueing on response inhibition in stimulant dependent individuals. Biol. Psychiatry 63:2 (2008), 184–190, 10.1016/j.biopsych.2007.04.031.
27. Luna, B., Padmanabhan, A., O'Hearn, K., What has fMRI told us about the Development of Cognitive Control through Adolescence?. Brain Cogn. 72:1 (2010), 101–113.
28. Luna, B., Sweeney, J.A., The emergence of collaborative brain function: FMRI studies of the development of response inhibition. Ann. N. Y. Acad. Sci. 1021 (2004), 296–309, 10.1196/annals.1308.035.
29. Meyerhoff, D.J., Durazzo, T.C., Ende, G., Chronic alcohol consumption, abstinence and relapse: brain proton magnetic resonance spectroscopy studies in animals and humans. Behavioral Neurobiology of Alcohol Addiction, 2013, Springer, Berlin, 511–540.
30. Meyerhoff, D.J., Edith, V.S., Adolf, P., Brain proton magnetic resonance spectroscopy of alcohol use disorders. Handbook of Clinical Neurology, vol. 125, 2014, Elsevier, Amsterdam & New York, 313–337 (Chapter 19).
31. Mon, A., Durazzo, T.C., Meyerhoff, D.J., Glutamate GABA, and other cortical metabolite concentrations during early abstinence from alcohol and their associations with neurocognitive changes. Drug Alcohol Depend. 125:1–2 (2012), 27–36, 10.1016/j.drugalcdep.2012.03.012.
32. Moss, H.B., Talagala, S.L., Kirisci, L., Phosphorus-31 magnetic resonance brain spectroscopy of children at risk for a substance use disorder: preliminary results. Psychiatry Res. 76:2–3 (1997), 101–112, 10.1016/S0925-4927(97)00067-X.
33. Öngür, D., Jensen, J.E., Prescot, A.P., Stork, C., Lundy, M., Cohen, B.M., Renshaw, P.F., Abnormal glutamatergic neurotransmission and neuronal-glial interactions in acute mania. Biol. Psychiatry 64:8 (2008), 718–726, 10.1016/j.biopsych.2008.05.014.
34. Patel, A.B., de Graaf, R.A., Mason, G.F., Rothman, D.L., Shulman, R.G., Behar, K.L., The contribution of GABA to glutamate/glutamine cycling and energy metabolism in the rat cortex in vivo. Proc. Natl. Acad. Sci. U. S. A. 102:15 (2005), 5588–5593, 10.1073/pnas.0501703102.
35. Petrakis, I.L., Limoncelli, D., Gueorguieva, R., Jatlow, P., Boutros, N.N., Trevisan, L., Gelernter, J., Krystal, J.H., Altered NMDA glutamate receptor antagonist response in individuals with a family vulnerability to alcoholism. Am. J. Psychiatry 161:10 (2004), 1776–1782.
36. Poon, E., Ellis, D.A., Fitzgerald, H.E., Zucker, R.A., Intellectual, cognitive, and academic performance among sons of alcoholics, during the early school years: differences related to subtypes of familial alcoholism. Alcohol. Clin. Exp. Res. 24:7 (2000), 1020–1027, 10.1111/j.1530-0277.2000.tb04645.x.
37. Provencher, S.W., Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn. Reson. Med. 30:6 (1993), 672–679, 10.1002/mrm.1910300604.
38. Rosenberg, D.R., MacMaster, F.P., Mirza, Y., Smith, J.M., Easter, P.C., Banerjee, S.P., Bhandari, R., Boyd, C., Lynch, M., Rose, M., Ivey, J., Villafuerte, R.A., Moore, G.J., Renshaw, P., Reduced anterior cingulate glutamate in pediatric major depression: a magnetic resonance spectroscopy study. Biol. Psychiatry 58:9 (2005), 700–704, 10.1016/j.biopsych.2005.05.007.
39. Rosenberg, D.R., Mirza, Y., Russell, A., Tang, J., Smith, J.M., Banerjee, S.P., Bhandari, R., Rose, M., Ivey, J., Boyd, C., Moore, G.J., Reduced anterior cingulate glutamatergic concentrations in childhood OCD and major depression versus healthy controls. J. Am. Acad. Child Adolesc. Psychiatry 43:9 (2004), 1146–1153, 10.1097/01.chi.0000132812.44664.2d.
40. Rothman, D.L., Sibson, N.R., Hyder, F., Shen, J., Behar, K.L., Shulman, R.G., In vivo nuclear magnetic resonance spectroscopy studies of the relationship between the glutamate–glutamine neurotransmitter cycle and functional neuroenergetics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354:1387 (1999), 1165–1177, 10.1098/rstb.1999.0472.
41. Rubia, K., Smith, A.B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., Brammer, M., Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Hum. Brain Mapp. 27:12 (2006), 973–993, 10.1002/hbm.20237.
42. Sher, K.J., Martin, E.D., Wood, P.K., Rutledge, P.C., Alcohol use disorders and neuropsychological functioning in first-year undergraduates. Exp. Clin. Psychopharmacol. 5:3 (1997), 304–315, 10.1037/1064-1297.5.3.304.
43. Sibson, N.R., Dhankhar, A., Mason, G.F., Rothman, D.L., Behar, K.L., Shulman, R.G., Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity. Proc. Natl. Acad. Sci. U. S. A. 95:1 (1998), 316–321.
44. Silveri, M.M., GABAergic contributions to alcohol responsivity during adolescence: insights from preclinical and clinical studies. Pharmacol. Ther. 143:2 (2014), 197–216, 10.1016/j.pharmthera.2014.03.001.
45. Silveri, M.M., Rogowska, J., McCaffrey, A., Yurgelun-Todd, D.A., Adolescents at risk for alcohol abuse demonstrate altered frontal lobe activation during Stroop performance. Alcohol. Clin. Exp. Res. 35:2 (2011), 218–228, 10.1111/j.1530-0277.2010.01337.x.
46. Silveri, M.M., Sneider, J.T., Crowley, D.J., Covell, M.J., Acharya, D., Rosso, I.M., Jensen, J.E., Frontal lobe gamma-aminobutyric acid levels during adolescence: associations with impulsivity and response inhibition. Biol. Psychiatry 74:4 (2013), 296–304, 10.1016/j.biopsych.2013.01.033.
47. Smith, S., Levante, T., Meier, B.H., Ernst, R.R., Computer simulations in magnetic resonance. An object-oriented programming approach. J. Magn. Reson. A 106:1 (1994), 75–105, 10.1006/jmra.1994.1008.
48. Squeglia, L.M., Jacobus, J., Tapert, S.F., The influence of substance use on adolescent brain development. Clin. EEG Neurosci. 40:1 (2009), 31–38, 10.1177/155005940904000110.
49. Stoltenberg, S.F., Mudd, S.A., Blow, F.C., Hill, E.M., Evaluating measures of family history of alcoholism: density versus dichotomy. Addiction 93:10 (1998), 1511–1520, 10.1046/j.1360-0443.1998.931015117.x.
50. Sullivan, E., Pfefferbaum, A., Brain proton magnetic resonance spectroscopy of alcohol use disorders. Alcohol and the Nervous System: Handbook of Clinical Neurology, vol. 125, 2014, 313.
51. Tsai, G., Coyle, J.T., The role of glutamatergic neurotransmission in the pathophysiology of alcoholism. Annu. Rev. Med. 49 (1998), 173–184, 10.1146/annurev.med.49.1.173.
52. Ward, R.J., Lallemand, F., de Witte, P., Biochemical and neurotransmitter changes implicated in alcohol-induced brain damage in chronic or ‘binge drinking’ alcohol abuse. Alcohol Alcohol. 44:2 (2009), 128–135, 10.1093/alcalc/agn100.
53. Yüksel, C., Öngür, D., Magnetic resonance spectroscopy studies of glutamate-related abnormalities in mood disorders. Biol. Psychiatry 68:9 (2010), 785–794, 10.1016/j.biopsych.2010.06.016.