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Altered cerebral blood flow and neurocognitive correlates in adolescent cannabis users

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Abstract

Rationale

The effects of adolescent marijuana use on the developing brain remain unclear, despite its prevalence. Arterial spin labeling (ASL) is a noninvasive imaging technique that characterizes neurovascular status and cerebral blood flow (CBF), potentially revealing contributors to neuropathological alterations. No studies to date have looked at CBF in adolescent marijuana users.

Objectives

This study examined CBF in adolescent marijuana users and matched healthy controls at baseline and after 4 weeks of monitored abstinence.

Methods

Heavy adolescent marijuana users (n = 23, >200 lifetime marijuana use days) and demographically matched controls (n = 23) with limited substance exposure underwent an ASL brain scan at an initial session and after 4 weeks of sequential urine toxicology to confirm abstinence.

Results

Marijuana users showed reduced CBF in four cortical regions including the left superior and middle temporal gyri, left insula, left and right medial frontal gyrus, and left supramarginal gyrus at baseline; users showed increased CBF in the right precuneus at baseline, as compared to controls (corrected p values < 0.05). No between group differences were found at follow-up.

Conclusions

Marijuana use may influence CBF in otherwise healthy adolescents acutely; however, group differences were not observed after several weeks of abstinence. Neurovascular alterations may contribute to or underlie changes in brain activation, neuropsychological performance, and mood observed in young cannabis users with less than a month of abstinence.

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References

  • Abdullaev Y, Posner MI, Nunnally R, Dishion TJ (2010) Functional MRI evidence for inefficient attentional control in adolescent chronic cannabis use. Behav Brain Res 215:45–57

    Article  PubMed  Google Scholar 

  • Ashtari M, Cervellione K, Cottone J, Ardekani BA, Sevy S, Kumra S (2009) Diffusion abnormalities in adolescents and young adults with a history of heavy cannabis use. J Psychiatr Res 43:189–204

    Article  PubMed  Google Scholar 

  • Bava S, Jacobus J, Mahmood O, Yang TT, Tapert SF (2010) Neurocognitive correlates of white matter quality in adolescent substance users. Brain Cogn 72:347–354

    Article  PubMed  Google Scholar 

  • Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571

    Google Scholar 

  • Becker B, Wagner D, Gouzoulis-Mayfrank E, Spuentrup E, Daumman J (2010) The impact of early-onset cannabis use on functional brain correlates of working memory. Prog Neuropsychopharmacol Biol Psychiatry 34:837–845

    Article  PubMed  CAS  Google Scholar 

  • Block RI, O’Leary DS, Hichwa RD, Augustinack JC, Ponto LL, Ghoneim MM, Arndt S, Erhardt JC, Hurtig RR, Watkins GL, Hall JA, Nathan PE, Andreasen NC (2000) Cerebellar hypoactivity in frequent marijuana users. NeuroReport 11:749–753

    Article  PubMed  CAS  Google Scholar 

  • Block RI, O’Leary DS, Hichwa RD, Augustinack JC, Boles PLL, Ghoneim MM, Arndt S, Hurtig RR, Watkins GL, Hall JA, Nathan PE, Andreasen NC (2002) Effects of frequent marijuana use on memory-related regional cerebral blood flow. Pharmacol Biochem Behav 72:237–250

    Article  PubMed  CAS  Google Scholar 

  • Bolla KI, Eldreth DA, Matochik JA, Cadet JL (2005) Neural substrates of faulty decision-making in abstinent marijuana users. NeuroImage 26:480–492

    Article  PubMed  Google Scholar 

  • Brown SA, Myers MG, Lippke L, Tapert SF, Stewart DG, Vik PW (1998) Psychometric evaluation of the customary drinking and drug use record (CDDR): a measure of adolescent alcohol and drug involvement. J Stud Alcohol 59:427–438

    PubMed  CAS  Google Scholar 

  • Buxton RB (2009) Introduction to functional magnetic resonance imaging: principles and techniques. University Press, Cambridge

    Book  Google Scholar 

  • Chalela JA, Alsop DC, Gonzalez-Atavales JB, Maldjian JA, Kasner SE, Detre JA (2000) Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. Stroke 31:680–687

    Article  PubMed  CAS  Google Scholar 

  • Cox R (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):172–173

    Article  Google Scholar 

  • Delis DC, Kramer JH, Kaplan E, Ober BA (2001) California verbal learning test, 2nd edn. The Psychological Corporation, San Antonio

    Google Scholar 

  • Delisi LE, Bertisch HC, Szulc KU, Majcher M, Brown K, Bappal A, Ardekani BA (2006) A preliminary DTI study showing no brain structural change associated with adolescent cannabis use. Harm Reduct J 3:17

    Article  PubMed  Google Scholar 

  • Demir B, Ulug B, Lay Ergun E, Erbas B (2002) Regional cerebral blood flow and neuropsychological functioning in early and late onset alcoholism. Psychiatry Res 115:115–125

    Article  PubMed  Google Scholar 

  • Domino EF, Minoshima S, Guthrie S, Ohl L, Ni L, Koeppe RA, Zubieta J (2000) Nicotine effects on regional cerebral blood flow in awake resting tobacco smokers. Synapse 38:313–321

    Article  PubMed  CAS  Google Scholar 

  • Eldreth DA, Matochik JA, Cadet JL, Bolla KI (2004) Abnormal brain activity in prefrontalbrain regions in abstinent marijuana users. NeuroImage 23:914–920

    Article  PubMed  Google Scholar 

  • Filbey FM, Schacht JP, Myers US, Chavez RS, Hutchinson KE (2009) Marijuana craving in the brain. Proc Natl Acad Sci USA 106:13016–13021

    Article  PubMed  CAS  Google Scholar 

  • Hanson KL, Winward JL, Schweinsburg AD, Medina KL, Brown SA, Tapert SF (2010) Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addict Behav 35:970–976

    Article  PubMed  Google Scholar 

  • Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87:1932–1936

    Article  PubMed  CAS  Google Scholar 

  • Herning RI, Better WE, Tate K, Cadet JL (2005) Cerebrovascular perfusion in marijuana users during a month of monitored abstinence. Neurology 64:488–493

    Article  PubMed  Google Scholar 

  • Jacobus J, McQueeny T, Bava S, Schweinsburg BC, Frank LR, Yang TT, Tapert SF (2009a) White matter integrity in adolescents with histories of marijuana use and binge drinking. Neurotoxicol Teratol 31:349–355

    Article  PubMed  CAS  Google Scholar 

  • Jacobus J, Bava S, Cohen-Zion M, Mahmood O, Tapert SF (2009b) Functional consequences of marijuana use in adolescents. Pharmacol Biochem Behav 92:559–565

    Article  PubMed  CAS  Google Scholar 

  • Jager G, Block RI, Luijten M, Ramsey NF (2010) Cannabis use and memory function in adolescent boys: a cross-sectional multicenter functional magnetic resonance imaging study. J Am Acad Child Adolesc Psychiatry 49:561–572

    PubMed  Google Scholar 

  • Johnston LD, O’Malley PM, Bachman JG, Schulenberg JE (2010) Monitoring the Future national survey results on drug use, 1975–2009: Vol I. Secondary school students (NIH publication no. 107584). National Institute on Drug Abuse, Bethesda, MD

    Google Scholar 

  • Jones RT (2002) Cardiovascular system effects of marijuana. J Clin Pharmacol 42:58S–63S

    PubMed  CAS  Google Scholar 

  • Kim SG (1995) Quantification of regional cerebral blood flow change by flow sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 34:293–301

    Article  PubMed  CAS  Google Scholar 

  • Kunos G, Jarai Z, Batkai S, Goparaju SK, Ishac EJN, Liu J, Wang L, Wagner JA (2000) Endocannabinoids as cardiovascular modulators. Chem Phys Lipids 108:159–168

    Article  PubMed  CAS  Google Scholar 

  • Liu TT, Wong EC (2005) A signal processing model for arterial spin labeling functional MRI. NeuroImage 24:207–215

    Article  PubMed  Google Scholar 

  • Lundqvist T, Jonsson S, Warkentin S (2001) Frontal lobe dysfunction in long-term cannabis users. Neurotoxicol Teratol 23:437–443

    Article  PubMed  CAS  Google Scholar 

  • Mathew RJ, Wilson WH (1993) Acute changes in cerebral blood flow after smoking marijuana. Life Sci 52:757–767

    Article  PubMed  CAS  Google Scholar 

  • Mathew RJ, Wilson WH, Tant SR (1989) Acute changes in cerebral blood flow associated with marijuana smoking. Acta Psychiatr Scand 79:118–129

    Article  PubMed  CAS  Google Scholar 

  • Mathew RJ, Wilson WH, Humphreys DF, Lowe JV, Wiethe KE (1992) Regional cerebral blood flow after marijuana smoking. J Cereb Blood Flow Metab 12:750–758

    Article  PubMed  CAS  Google Scholar 

  • Mathew RJ, Wilson WH, Coleman RE, Turkington TG, DeGrado TR (1997) Marijuana intoxication and brain activation in marijuana smokers. Life Sci 60:2075–2089

    Article  PubMed  CAS  Google Scholar 

  • Mathew RJ, Wilson WH, Turkington TG, Hawk TC, Coleman RE, DeGrado TR, Provenzale J (2002) Time course of tetrahydrocannabinol-induced changes in regional cerebral blood flow measured with positron emission tomography. Psychiatry Res 116:173–185

    Article  PubMed  CAS  Google Scholar 

  • Martin-Santos R, Fagundo AB, Crippa JA, Atakan Z, Bhattacharyya S, Allen P, Fusar-Poli P, Borgwardt S, Seal M, Busatto GF, McGuire P (2010) Neuroimaging in cannabis use: a systematic review of the literature. Psychol Med 40:383–398

    Article  PubMed  CAS  Google Scholar 

  • Murphy K, Dixon V, LaGrave K, Kaufman J, Risinger R, Bloom A, Garavan H (2006) A validation of event-related fMRI comparisons between users of cocaine, nicotine, or cannabis and control subjects. Am J Psychiatry 163:1245–1251

    Article  PubMed  Google Scholar 

  • O’Leary DS, Block RI, Koeppel JA, Flaum M, Schultz SK, Andreasen NC, Ponto LB, Watkins GL, Hurtig RR, Hichwa RD (2002) Effects of smoking marijuana on brain perfusion and cognition. Neuropsychopharmacology 26:802–816

    Article  PubMed  Google Scholar 

  • Pope HG Jr, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D (2001) Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58:909–915

    Article  PubMed  Google Scholar 

  • Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P (1999) SENSE: sensitivity encoding for fast MRI. Magn Reson Med 42:952–962

    Article  PubMed  CAS  Google Scholar 

  • Randall MD, Kendall DA, O’Sullivan S (2004) The complexities of the cardiovascular actions of cannabinoids. Br J Pharmacol 142:20–26

    Article  PubMed  CAS  Google Scholar 

  • Rice JP, Reich T, Bucholz KK, Neuman RJ, Fishman R, Rochberg N, Hesselbrock VM, Nurnberger JI Jr, Schuckit MA, Begleiter H (1995) Comparison of direct interview and family history diagnoses of alcohol dependence. Alcohol Clin Exp Res 19:1018–1023

    Article  PubMed  CAS  Google Scholar 

  • Schweinsburg AD, Schweinburg BC, Nagel BJ, Eyler LT, Tapert SF (2011) Neural correlates of verbal learning in adolescent alcohol and marijuana users. Addiction 106:564–573

    Article  PubMed  Google Scholar 

  • Sevy S, Smith GS, Ma Y, Dhawan V, Chaly T, Kingsley PB, Kumra S, Abdelmessih S, Eidelberg D (2008) Cerebral glucose metabolism and D2/D3 receptor availability in young adults with cannabis dependence measured with positron emission tomography. Psychopharmacology (Berl) 197:549–556

    Article  CAS  Google Scholar 

  • Smith SM, Jenkinson M, Wollrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DR, Niazy RK, Saunders J, Bickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23:208–219

    Article  Google Scholar 

  • Smith ML, Barnes AJ, Huestis MA (2009) Identifying new cannabis use with urine creatinine-normalized THCCOOH concentrations and time intervals between specimen collections. J Anal Toxicol 33:185–189

    PubMed  CAS  Google Scholar 

  • Sneider JT, Pope HG, Silveri MM, Simpson NS, Gruber SA, Yurgelun-Todd DA (2008) Differences in regional blood volume during a 28-day period of abstinence in chronic cannabis smokers. Neuropsychopharmacology 18:612–619

    Article  CAS  Google Scholar 

  • Sobell LC, Sobell MB (1992) Timeline follow back. A technique for assessing self-reported alcohol consumption. Humana Press, Totowa, NJ

    Google Scholar 

  • Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the state-trait anxiety inventory (self-evaluation questionnaire). Consulting Psychologists, Palo Alto, CA

    Google Scholar 

  • Takahashi T, Shirane R, Sato S, Yoshimoto T (1999) Developmental changes of cerebral blood flow and oxygen metabolism in children. AJNR 20:917–922

    PubMed  CAS  Google Scholar 

  • Tapert SF, Schweinsburg AD, Drummond SP, Paulus MP, Brown SA, Yang TT, Frank LR. (2007) Functional MRI of inhibitory processing in abstinent adolescent marijuana users. Psychopharmacology (Berl) 194:173–183

    Google Scholar 

  • Tunving K, Thulin SO, Risberg J, Warkentin S (1986) Regional cerebral blood flow in long-term heavy cannabis use. Psychiatry Res 17:15–21

    Article  PubMed  CAS  Google Scholar 

  • van Hell H, Bossong MG, Jager G, Kristo G, van Osch MJP, Zelaya F, Kahn RS, Ramsey NF (2011) Evidence for involvement of the insula in the psychotropic effects of THC in humans: a double-blind, randomized pharmacological MRI study. Int J Neuropsychopharmacol 14:1377–1388

    Article  PubMed  Google Scholar 

  • Volkow ND, Gillespie H, Mullani N, Tancredi L, Grant C, Valentine A, Hollister L (1996) Brain glucose metabolism in chronic marijuana users at baseline and during marijuana intoxication. Psychiatry Res 67:29–38

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Qiu M, Constable RT (2005) In vivo method for correcting transmit/receive nonuniformities with phased array coils. Magn Reson Med 53:666–674

    Article  PubMed  Google Scholar 

  • Wechsler D (1997) WAIS-III manual. Psychological Corporation, New York, NY

    Google Scholar 

  • Wechsler D (1999) Wechsler abbreviated scale of intelligence-administration and scoring manual. Psychological Corporation, London, UK

    Google Scholar 

  • Wilkinson GD (1993) WRAT-3 Wide range achievement test administration manual, 3rd edn. Western Psychological Services, Wilmington, DE

    Google Scholar 

  • Wong EC, Buston RB, Frank LR (1998) Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magn Reson Med 39:702–708

    Article  PubMed  CAS  Google Scholar 

  • Zubieta J, Lombardi U, Minoshima S, Guthrie S, Ni L, Ohl LE, Koeppe RA, Domino EF (2001) Regional cerebral blood flow effects of nicotine in overnight abstinent smokers. Biol Psychiatry 49:906–913

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We extend our appreciation to Anthony Scarlett and Rachel Thayer for their assistance with data collection and to participating families and schools. This research was made possible by funding from the National Institute on Drug Abuse (P20 DA024194, R01 DA021182, F31 DA026263), the National Institute on Alcohol Abuse and Alcoholism (7R01 AA13419), and the National Institute of Mental Health (R01 MH084796).

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Correspondence to Susan F. Tapert.

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Jacobus, J., Goldenberg, D., Wierenga, C.E. et al. Altered cerebral blood flow and neurocognitive correlates in adolescent cannabis users. Psychopharmacology 222, 675–684 (2012). https://doi.org/10.1007/s00213-012-2674-4

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  • DOI: https://doi.org/10.1007/s00213-012-2674-4

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