Abnormal striatal circuitry and intensified novelty seeking among adolescents who abuse methamphetamine and cannabis

Developmental Neuroscience

Volumn 34, Issue 4, 2012, Pages 310-317

  Churchwell, John C ^a,b   Carey, Paul D ^c   Ferrett, Helen L ^c   Stein, Dan J ^c   Yurgelun Todd, Deborah A ^a,b  

^a UNIVERSITY OF UTAH   (United States)

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

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Adolescence; Cannabis; Magnetic resonance imaging; Methamphetamine; Novelty seeking; Striatum

Indexed keywords

CANNABIS; DOPAMINE; METHAMPHETAMINE;

ADULT; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN SIZE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; HUMAN; INTENSIFIED NOVELTY SEEKING; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PERSONALITY; PRIORITY JOURNAL; SUBSTANCE ABUSE;

ADOLESCENT; ADOLESCENT PSYCHOLOGY; ALCOHOL DRINKING; AMPHETAMINE-RELATED DISORDERS; CAUDATE NUCLEUS; CHILD; CORPUS STRIATUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MALE; MARIJUANA ABUSE; METHAMPHETAMINE; NUCLEUS ACCUMBENS; ORGAN SIZE; PERSONALITY INVENTORY; PUTAMEN; REWARD; SMOKING;

EID: 84867989217     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000337724     Document Type: Article

References (60)

1. United Nations Office on Drugs and Crime: World Drug Report 2010. United Nations Publications, 2010.
2. Chen CY, Storr CL, Anthony JC: Early-onset drug use and risk for drug dependence problems. Addict Behav 2009; 34: 319-322.
3. Schramm-Sapyta NL, Walker QD, Caster JM, Levin ED, Kuhn CM: Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacology 2009; 206: 1-21.
4. Lynskey MT, Heath AC, Bucholz KK, Slutske WS, Madden PA, Nelson EC, Statham DJ, Martin NG: Escalation of drug use in earlyonset cannabis users versus co-twin controls. JAMA 2003; 289: 427-433. (Pubitemid 36119962)
5. Rodriguez de Fonseca F, Ramos JA, Bonnin A, Fernandez-Ruiz JJ: Presence of cannabinoid binding sites in the brain from early postnatal ages. Neuroreport 1993; 4: 135-138. (Pubitemid 23080859)
6. Tarazi FI, Baldessarini RJ: Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 2000; 18: 29-37. (Pubitemid 30116706)
7. Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley JW, Robbins TW: Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci 2008; 363: 3125-3135.
8. Zuckerman M: Behavioral Expressions and Biosocial Bases of Sensation Seeking. New York, Cambridge University Press, 1994.
9. Steinberg L: A social neuroscience perspective on adolescent risk-taking. Dev Rev 2008; 28: 78-106.
10. Churchwell JC, Yurgelun-Todd DA: Neuroimaging, adolescence and risky behavior; in Bardo MT, Fishbein DH, Milich R(eds): Inhibitory Control and Drug Abuse Prevention. From Research to Translation. New York, Springer, 2011, vol 1.
11. Bardo MT, Donohew RL, Harrington NG: Psychobiology of novelty seeking and drug seeking behavior. Behav Brain Res 1996; 77: 23-43. (Pubitemid 26166299)
12. Huang HY, Lee IH, Chen KC, Yeh TL, Chen PS, Yang YK, Chiu NT, Yao WJ, Chen CC: Association of novelty seeking scores and striatal dopamine D 2/D 3 receptor availability of healthy volunteers: single photon emission computed tomography with 123 I-iodobenzamide. J Formos Med Assoc 2010; 109: 736-739.
13. Van Laere K, Goffin K, Bormans G, Casteels C, Mortelmans L, de Hoon J, Grachev I, Vandenbulcke M, Pieters G: Relationship of type cannabinoid receptor availability in the human brain to novelty-seeking temperament. Arch Gen Psychiatry 2009; 66: 196-204.
14. Bossong MG, van Berckel BN, Boellaard R, Zuurman L, Schuit RC, Windhorst AD, van Gerven JM, Ramsey NF, Lammertsma AA, Kahn RS: Delta 9- tetrahydrocannabinol induces dopamine release in the human striatum. Neuropsychopharmacology 2009; 34: 759-766.
15. Drevets WC, Price JC, Kupfer DJ, Kinahan PE, Lopresti B, Holt D, Mathis C: PET measures of amphetamine-induced dopamine release in ventral versus dorsal striatum. Neuropsychopharmacology 1999; 21: 694-709.
16. Crawford AM, Pentz MA, Chou CP, Li C, Dwyer JH: Parallel developmental trajectories of sensation seeking and regular substance use in adolescents. Psychology of addictive behaviors. Psychol Addict Behav 2003; 17: 179-192. (Pubitemid 37153092)
17. Piazza PV, Deminiere JM, Le Moal M, Simon H: Factors that predict individual vulnerability to amphetamine self-administration. Science 1989; 245: 1511-1513. (Pubitemid 19243245)
18. Martin-Santos R, Fagundo AB, Crippa JA, Atakan Z, Bhattacharyya S, Allen P, Fusar-Poli P, Borgwardt S, Seal M, Busatto GF, Mc-Guire P: Neuroimaging in cannabis use: a systematic review of the literature. Psychol Med 2010; 40: 383-398.
19. Chang L, Alicata D, Ernst T, Volkow N: Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 2007; 102(suppl 1):16-32. (Pubitemid 46328220)
20. Sevy S, Smith GS, Ma Y, Dhawan V, Chaly T, Kingsley PB, Kumra S, Abdelmessih S, Eidelberg D: Cerebral glucose metabolism and D2/D3 receptor availability in young adults with cannabis dependence measured with positron emission tomography. Psychopharmacology 2008; 197: 549-556.
21. Nestor L, Hester R, Garavan H: Increased ventral striatal BOLD activity during nondrug reward anticipation in cannabis users. Neuroimage 2010; 49: 1133-1143.
22. van Hell HH, Vink M, Ossewaarde L, Jager G, Kahn RS, Ramsey NF: Chronic effects of cannabis use on the human reward system: an fMRI study. Eur Neuropsychopharmacol 2010; 20: 153-163.
23. Salo R, Fassbender C: Structural, functional and spectroscopic MRI studies of methamphetamine addiction. Curr Top Behav Neurosci 2011; 11: 321-364.
24. Johanson CE, Frey KA, Lundahl LH, Keenan P, Lockhart N, Roll J, Galloway GP, Koeppe RA, Kilbourn MR, Robbins T, Schuster CR: Cognitive function and nigrostriatal markers in abstinent methamphetamine abusers. Psychopharmacology (Berl) 2006.
25. McCann UD, Wong DF, Yokoi F, Villemagne V, Dannals RF, Ricaurte GA: Reduced striatal dopamine transporter density in abstinent methamphetamine and methcathinone users: evidence from positron emission tomography studies with [ 11 C]WIN-35,428. J Neurosci 1998; 18: 8417-8422. (Pubitemid 28465016)
26. Volkow ND, Chang L, Wang GJ, Fowler JS, Leonido-Yee M, Franceschi D, Sedler MJ, Gatley SJ, Hitzemann R, Ding YS, Logan J, Wong C, Miller EN: Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. Am J Psychiatry 2001; 158: 377-382. (Pubitemid 32205193)
27. Lee B, London ED, Poldrack RA, Farahi J, Nacca A, Monterosso JR, Mumford JA, Bokarius AV, Dahlbom M, Mukherjee J, Bilder RM, Brody AL, Mandelkern MA: Striatal dopamine d2/d3 receptor availability is reduced in methamphetamine dependence and is linked to impulsivity. J Neurosci 2009; 29: 14734-14740.
28. Hoffman WF, Schwartz DL, Huckans MS, McFarland BH, Meiri G, Stevens AA, Mitchell SH: Cortical activation during delay discounting in abstinent methamphetamine dependent individuals. Psychopharmacology (Berl) 2008; 201: 183-193.
29. Chang L, Cloak C, Patterson K, Grob C, Miller EN, Ernst T: Enlarged striatum in abstinent methamphetamine abusers: a possible compensatory response. Biol Psychiatry 2005; 57: 967-974. (Pubitemid 40603079)
30. Jernigan TL, Gamst AC, Archibald SL, Fennema-Notestine C, Mindt MR, Marcotte TD, Heaton RK, Ellis RJ, Grant I: Effects of methamphetamine dependence and HIV infection on cerebral morphology. Am J Psychiatry 2005; 162: 1461-1472. (Pubitemid 41105560)
31. Tulloch IK, Afanador L, Zhu J, Angulo JA: Methamphetamine induces striatal cell death followed by the generation of new cells and a second round of cell death in mice. Curr Neuropharmacol 2011; 9: 79-83.
32. Voytek B, Berman SM, Hassid BD, Simon SL, Mandelkern MA, Brody AL, Monterosso J, Ling W, London ED: Differences in regional brain metabolism associated with marijuana abuse in methamphetamine abusers. Synapse 2005; 57: 113-115. (Pubitemid 40911526)
33. Cloninger CR: A systematic method for clinical description and classification of personality variants. A proposal. Arch Gen Psychiatry 1987; 44: 573-588. (Pubitemid 17082099)
34. Kaufman J, Birmaher B, Brent D, Rao U, Ryan N: The Schedule for Affective Disorders and Schizophrenia for School Aged Children (6-18 years) Lifetime Version, 1996.
35. First MB, Spitzer RL, Gibbon M, Williams JB: Structured Clinical Interview for DSMIV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P). New York, Biometrics Research, New York State Psychiatric Institute, 2002.
36. Dale AM, Fischl B, Sereno MI: Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999; 9: 179-194. (Pubitemid 29369874)
37. Sled JG, Zijdenbos AP, Evans AC: A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 1998; 17: 87-97. (Pubitemid 128742012)
38. Fischl B, Liu A, Dale AM: Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 2001; 20: 70-80. (Pubitemid 32293421)
39. Fischl B, Dale AM: Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 2000; 97: 11050-11055.
40. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ: An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006; 31: 968-980. (Pubitemid 44183792)
41. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM: Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002; 33: 341-355. (Pubitemid 34162530)
42. Leland DS, Arce E, Feinstein JS, Paulus MP: Young adult stimulant users' increased striatal activation during uncertainty is related to impulsivity. Neuroimage 2006; 33: 725-731. (Pubitemid 44485567)
43. Sakurai-Yamashita Y, Kataoka Y, Fujiwara M, Mine K, Ueki S: Delta 9-tetrahydrocannabinol facilitates striatal dopaminergic transmission. Pharmacol Biochem Behav 1989; 33: 397-400. (Pubitemid 19245527)
44. Simon SL, Richardson K, Dacey J, Glynn S, Domier CP, Rawson RA, Ling W: A comparison of patterns of methamphetamine and cocaine use. J Addict Dis 2002; 21: 35-44. (Pubitemid 35203852)
45. Miura H, Fujiki M, Shibata A, Ishikawa K: Prevalence and profile of methamphetamine users in adolescents at a juvenile classification home. Psychiatry Clin Neurosci 2006; 60: 352-357. (Pubitemid 43736401)
46. Lynskey MT, Vink JM, Boomsma DI: Early onset cannabis use and progression to other drug use in a sample of Dutch twins. Behav Genet 2006; 36: 195-200. (Pubitemid 43673562)
47. Kandel DB: Does marijuana use cause the use of other drugs? JAMA 2003; 289: 482-483. (Pubitemid 36119970)
48. Lamarque S, Taghzouti K, Simon H: Chronic treatment with Delta(9)-tetrahydrocannabinol enhances the locomotor response to amphetamine and heroin. Implications for vulnerability to drug addiction. Neuropharmacology 2001; 41: 118-129. (Pubitemid 32607651)
49. Pistis M, Perra S, Pillolla G, Melis M, Muntoni AL, Gessa GL: Adolescent exposure to cannabinoids induces long-lasting changes in the response to drugs of abuse of rat midbrain dopamine neurons. Biol Psychiatry 2004; 56: 86-94. (Pubitemid 38849412)
50. Steinberg L: Risk taking in adolescence: what changes, and why? Ann NY Acad Sci 2004; 1021: 51-58. (Pubitemid 38879609)
51. Kelley AE, Schochet T, Landry CF: Risk taking and novelty seeking in adolescence: introduction to part I. Ann NY Acad Sci 2004; 1021: 27-32. (Pubitemid 38879607)
52. Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DW: Incentiveelicited brain activation in adolescents: similarities and differences from young adults. J Neurosci 2004; 24: 1793-1802. (Pubitemid 38292790)
53. Laviola G, Pascucci T, Pieretti S: Striatal dopamine sensitization to D-amphetamine in periadolescent but not in adult rats. Pharmacol Biochem Behav 2001; 68: 115-124. (Pubitemid 32239447)
54. Laviola G, Adriani W, Terranova ML, Gerra G: Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 1999; 23: 993-1010. (Pubitemid 29502404)
55. Eisenman R, Grossman JC, Goldstein R: Undergraduate marijuana use as related to internal sensation novelty seeking and openness to experience. J Clin Psychol 1980; 36: 1013-1019. (Pubitemid 11241555)
56. Teicher MH, Andersen SL, Hostetter JC Jr: Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Brain Res Dev Brain Res 1995; 89: 167-172.
57. Robinson TE, Kolb B: Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine. J Neurosci 1997; 17: 8491-8497. (Pubitemid 27461070)
58. Kolb B, Gorny G, Limebeer CL, Parker LA: Chronic treatment with Delta-9-tetrahydrocannabinol alters the structure of neurons in the nucleus accumbens shell and medial prefrontal cortex of rats. Synapse 2006; 60: 429-436. (Pubitemid 44380153)
59. Sekine Y, Ouchi Y, Sugihara G, Takei N, Yoshikawa E, Nakamura K, Iwata Y, Tsuchiya KJ, Suda S, Suzuki K, Kawai M, Takebayashi K, Yamamoto S, Matsuzaki H, Ueki T, Mori N, Gold MS, Cadet JL: Methamphetamine causes microglial activation in the brains of human abusers. J Neurosci 2008; 28: 5756-5761.
60. Tost H, Braus DF, Hakimi S, Ruf M, Vollmert C, Hohn F, Meyer-Lindenberg A: Acute D2 receptor blockade induces rapid, reversible remodeling in human cortical-striatal circuits. Nat Neurosci 2010; 13: 920-922.