γ-Amino butyric acid and glutamate abnormalities in adolescent chronic marijuana smokers

Drug and Alcohol Dependence

Volumn 129, Issue 3, 2013, Pages 232-239

  Prescot, Andrew P ^a   Renshaw, Perry F ^a   Yurgelun Todd, Deborah A ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Amino butyric acid (GABA); Adolescent; Anterior cingulate cortex (ACC); Cannabis; Glutamate; Marijuana; Proton magnetic resonance spectroscopy

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID;

ADOLESCENT; ADOLESCENT HEALTH; ADULT; ARTICLE; BRAIN DYSFUNCTION; CANNABIS ADDICTION; CANNABIS SMOKING; CEREBROSPINAL FLUID; CHILD BEHAVIOR; CINGULATE GYRUS; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; FUNCTIONAL NEUROIMAGING; GRAY MATTER; HUMAN; MALE; METABOLITE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SEX DIFFERENCE; SMOKING HABIT;

ADOLESCENT; BIOLOGICAL MARKERS; COHORT STUDIES; CROSS-SECTIONAL STUDIES; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MARIJUANA SMOKING; TIME FACTORS; YOUNG ADULT;

CANNABIS; CANNABIS SATIVA;

EID: 84876087700     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2013.02.028     Document Type: Article

References (63)

1. Batra N.A., Seres-Mailo J., Hanstock C., Seres P., Khudabux J., Bellavance F., Baker G., Allen P., Tibbo P., Hui E., Le Melledo J.M. Proton magnetic resonance spectroscopy measurement of brain Glu levels in premenstrual dysphoric disorder. Biol. Psychiatry 2008, 63:1178-1184.
2. Bhagwagar Z., Wylezinska M., Taylor M., Jezzard P., Matthews P.M., Cowen P.J. Increased brain GABA concentrations following acute administration of a selective serotonin reuptake inhibitor. Am. J. Psychiatry 2004, 161:368-370.
3. Boy F., Evans C.J., Edden R.A., Singh K.D., Husain M., Sumner P. Individual differences in subconscious motor control predicted by GABA concentration in SMA. Curr. Biol. 2010, 20:1779-1785.
4. Cai K., Nanga R.P., Lamprou L., Schinstine C., Elliott M., Hariharan H., Reddy R., Epperson C.N. The impact of gabapentin administration on brain GABA and glutamate concentrations: a 7T (1)H MRS study. Neuropsychopharmacology 2012, 37:2764-2771.
5. Chang L., Cloak C., Yakupov R., Ernst T. Combined and independent effects of chronic marijuana use and HIV on brain metabolites. J. Neuroimmune Pharmacol. 2006, 1:65-76.
6. Chang L., Jiang C.S., Ernst T. Effects of age and sex on brain Glu and other metabolites. Magn. Reson. Imaging 2009, 27:142-145.
7. Churchwell J.C., Lopez-Larson M., Yurgelun-Todd D.A. Altered frontal cortical volume and decision making in adolescent cannabis users. Front. Psychol. 2010, 1:225.
8. Cohen-Cory S. The developing synapse: construction and modulation of synaptic structures and circuits. Science 2002, 298:770-776.
9. Crews F., He J., Hodge C. Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol. Biochem. Behav. 2007, 86:189-199.
10. Dalton V.S., Zavitsanou K. Cannabinoid effects on CB1 receptor density in the adolescent brain: an autoradiographic study using the synthetic cannabinoid HU210. Synapse 2010, 64:845-854.
11. de Graaf R.A., Rothman D.L., Behar K.L. State of the art direct 13C and indirect 1H-[13C] NMR spectroscopy in vivo. A practical guide. NMR Biomed. 2011, 24:958-972.
12. Devane W.A., Dysarz F.A., Johnson M.R., Melvin L.S., Howlett A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 1988, 34:605-613.
13. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258:1946-1949.
14. Ehrenreich H., Rinn T., Kunert H.J., Moeller M.R., Poser W., Schilling L., Gigerenzer G., Hoehe M.R. Specific attentional dysfunction in adults following early start of cannabis use. Psychopharmacology (Berl.) 1999, 142:295-301.
15. Epperson C.N., Haga K., Mason G.F., Sellers E., Gueorguieva R., Zhang W., Weiss E., Rothman D.L., Krystal J.H. Cortical gamma-aminobutyric acid levels across the menstrual cycle in healthy women and those with premenstrual dysphoric disorder: a proton magnetic resonance spectroscopy study. Arch. Gen. Psychiatry 2002, 59:851-858.
16. Gabbay V., Mao X., Klein R.G., Ely B.A., Babb J.S., Panzer A.M., Alonso C.M., Shungu D.C. Anterior cingulate cortex gamma-aminobutyric acid in depressed adolescents: relationship to anhedonia. Arch. Gen. Psychiatry 2012, 69:139-149.
17. Geramita M., van der Veen J.W., Barnett A.S., Savostyanova A.A., Shen J., Weinberger D.R., Marenco S. Reproducibility of prefrontal gamma-aminobutyric acid measurements with J-edited spectroscopy. NMR Biomed. 2011, 24:1089-1098.
18. Glass M., Dragunow M., Faull R.L. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1997, 77:299-318.
19. Gruber S.A., Yurgelun-Todd D.A. Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Brain Res. Cogn. Brain Res. 2005, 23:107-118.
20. Gruber S.A., Rogowska J., Yurgelun-Todd D.A. Altered affective response in marijuana smokers: an FMRI study. Drug Alcohol Depend. 2009, 105:139-153.
21. Guillem E., Pelissolo A., Vorspan F., Bouchez-Arbabzadeh S., Lepine J.P. Sociodemographic profiles, addictive and mental comorbidity in cannabis users in an outpatient specific setting. Encephale 2009, 35:226-233.
22. Hajos N., Freund T.F. Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 2002, 43:503-510.
23. Herkenham M., Lynn A.B., Johnson M.R., Melvin L.S., de Costa B.R., Rice K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 1991, 11:563-583.
24. Hermann D., Sartorius H., Welzel H., Walter S., Skopp G., Ende G., Mann K. Dorsolateral prefrontal cortex N-acetylaspartate/total creatine (NAA/tCr) loss in male recreational cannabis users. Biol. Psychiatry 2007, 61:1281-1289.
25. Hester R., Nestor L., Garavan H. Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 2009, 34:2450-2458.
26. Hoffman A.F., Oz M., Yang R., Lichtman A.H., Lupica C.R. Opposing actions of chronic Delta9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation. Learn. Mem. 2007, 14:63-74.
27. Huttenlocher P.R. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res. 1979, 163:195-205.
28. Jager G., Block R.I., Luijten M., Ramsey N.F. Cannabis use and memory brain function in adolescent boys: a cross-sectional multicenter functional magnetic resonance imaging study. J. Am. Acad. Child Adolesc. Psychiatry 2010, 49:561-572.
29. Jensen J.E., Frederick Bde B., Renshaw P.F. Grey and white matter GABA level differences in the human brain using two-dimensional, J-resolved spectroscopic imaging. NMR Biomed. 2005, 18:570-576.
30. Johnston L., O'Malley P., Bachman J., Schulenberg J. Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2008 2009, National Institute on Drug Abuse, Bethesda, MD, (NIH Publicaiton No. 09-7401).
31. Kaiser L.G., Young K., Matson G.B. Elimination of spatial interference in PRESS-localized editing spectroscopy. Magn. Reson. Med. 2007, 58:813-818.
32. Kaufman J., Birmaher B., Brent D., Rao U., Flynn C., Moreci P., Williamson D., Ryan N. Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. J. Am. Acad. Child Adolesc. Psychiatry 1997, 36:980-988.
33. Klose U. In vivo proton spectroscopy in presence of eddy currents. Magn. Reson. Med. 1990, 14:26-30.
34. Laaris N., Good C.H., Lupica C.R. Delta9-tetrahydrocannabinol is a full agonist at CB1 receptors on GABA neuron axon terminals in the hippocampus. Neuropharmacology 2010, 59:121-127.
35. Lubman D.I., Allen N.B., Rogers N., Cementon E., Bonomo Y. The impact of co-occurring mood and anxiety disorders among substance-abusing youth. J. Affect. Disord. 2007, 103:105-112.
36. Marshall I., Higinbotham J., Bruce S., Freise A. Use of Voigt lineshape for quantification of in vivo 1H spectra. Magn. Reson. Med. 1997, 37:651-657.
37. Mason G.F., Krystal J.H. MR spectroscopy: its potential role for drug development for the treatment of psychiatric diseases. NMR Biomed. 2006, 19:690-701.
38. Mason B.J., Crean R., Goodell V., Light J.M., Quello S., Shadan F., Buffkins K., Kyle M., Adusumalli M., Begovic A., Rao A proof-of-concept randomized controlled study of gabapentin: effects on cannabis use, withdrawal and executive function deficits in cannabis-dependent adults. Neuropsychopharmacology 2012, 37:1689-1698.
39. Mechoulam R., Gaoni Y. A total synthesis of Dl-Delta-1-tetrahydrocannabinol, the active constituent of hashish. J. Am. Chem. Soc. 1965, 87:3273-3275.
40. Mescher M., Merkle H., Kirsch J., Garwood M., Gruetter R. Simultaneous in vivo spectral editing and water suppression. NMR Biomed. 1998, 11:266-272.
41. Natt O., Bezkorovaynyy V., Michaelis T., Frahm J. Use of phased array coils for a determination of absolute metabolite concentrations. Magn. Reson. Med. 2005, 53:3-8.
42. Northoff G., Walter M., Schulte R.F., Beck J., Dydak U., Henning A., Boeker H., Grimm S., Boesiger P. GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nat. Neurosci. 2007, 10:1515-1517.
43. Ogg R.J., Kingsley P.B., Taylor J.S. WET, a T1- and B1-insensitive water-suppression method for in vivo localized 1H NMR spectroscopy. J. Magn. Reson. B 1994, 104:1-10.
44. O'Shea M., Singh M.E., McGregor I.S., Mallet P.E. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J. Psychopharmacol. 2004, 18:502-508.
45. Pope H.G., Gruber A.J., Hudson J.I., Cohane G., Huestis M.A., Yurgelun-Todd D. Early-onset cannabis use and cognitive deficits: what is the nature of the association?. Drug Alcohol Depend. 2003, 69:303-310.
46. Prescot A.P., Locatelli A.E., Renshaw P.F., Yurgelun-Todd D.A. Neurochemical alterations in adolescent chronic marijuana smokers: a proton MRS study. Neuroimage 2011, 57:69-75.
47. Realini N., Rubino T., Parolaro D. Neurobiological alterations at adult age triggered by adolescent exposure to cannabinoids. Pharmacol. Res. 2009, 60:132-138.
48. Rubino T., Parolaro D. Long lasting consequences of cannabis exposure in adolescence. Mol. Cell. Endocrinol. 2008, 286:S108-S113.
49. Sailasuta N., Ernst T., Chang L. Regional variations and the effects of age and gender on Glu concentrations in the human brain. Magn. Reson. Imaging 2008, 26:667-675.
50. Sanacora G., Mason G.F., Rothman D.L., Krystal J.H. Increased occipital cortex GABA concentrations in depressed patients after therapy with selective serotonin reuptake inhibitors. Am. J. Psychiatry 2002, 159:663-665.
51. Schlicker E., Kathmann M. Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol. Sci. 2001, 22:565-572.
52. Schneider M., Koch M. Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 2003, 28:1760-1769.
53. Schulte R.F., Boesiger P. ProFit: two-dimensional prior-knowledge fitting of J-resolved spectra. NMR Biomed. 2006, 19:255-263.
54. Schweinsburg A.D., Brown S.A., Tapert S.F. The influence of marijuana use on neurocognitive functioning in adolescents. Curr. Drug Abuse Rev. 2008, 1:99-111.
55. Slotkin T.A. Nicotine and the adolescent brain: insights from an animal model. Neurotoxicol. Teratol. 2002, 24:369-384.
56. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
57. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl. 1):S208-S219.
58. Spear L.P. Assessment of adolescent neurotoxicity: rationale and methodological considerations. Neurotoxicol. Teratol. 2007, 29:1-9.
59. Sugiura T., Kondo S., Sukagawa A., Nakane S., Shinoda A., Itoh K., Yamashita A., Waku K. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 1995, 215:89-97.
60. Stiglick A., Kalant H. Residual effects of chronic cannabis treatment on behavior in mature rats. Psychopharmacology (Berl.) 1985, 85:436-439.
61. Taylor M.J., Norbury R., Murphy S., Rudebeck S., Jezzard P., Cowen P.J. Lack of effect of citalopram on magnetic resonance spectroscopy measures of Glu and glutamine in frontal cortex of healthy volunteers. J. Psychopharmacol. 2010, 24:1217-1221.
62. Wilson R.I., Nicoll R.A. Endocannabinoid signaling in the brain. Science 2002, 296:678-682.
63. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imag. 2001, 20:45-57.