Cortical thickness in adolescent marijuana and alcohol users: A three-year prospective study from adolescence to young adulthood

Developmental Cognitive Neuroscience

Volumn 16, Issue , 2015, Pages 101-109

  Jacobus, Joanna ^a,b   Squeglia, Lindsay M ^c   Meruelo, Alejandro D ^b   Castro, Norma ^b   Brumback, Ty ^b   Giedd, Jay N ^b   Tapert, Susan F ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Adolescence; Alcohol; Brain; Cortical thickness; Imaging; Marijuana

Indexed keywords

CANNABIS;

ADOLESCENT; ADULT; ALCOHOLISM; ARTICLE; CANNABIS ADDICTION; CANNABIS USE; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DISEASE ASSOCIATION; FEMALE; FOLLOW UP; FRONTAL CORTEX; HEALTH STATUS; HUMAN; MALE; NERVE GROWTH; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; ONSET AGE; PARIETAL CORTEX; PRIORITY JOURNAL; PROSPECTIVE STUDY; TEMPORAL CORTEX; TIME FACTOR; UNDERAGE DRINKING; YOUNG ADULT; BRAIN CORTEX; CONVALESCENCE; FRONTAL LOBE; MENTAL HEALTH; PARIETAL LOBE; PATHOLOGY; SOCIOECONOMICS;

ADOLESCENT; AGE OF ONSET; ALCOHOLISM; CEREBRAL CORTEX; FEMALE; FRONTAL LOBE; HEALTH STATUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MARIJUANA ABUSE; MENTAL HEALTH; PARIETAL LOBE; PROSPECTIVE STUDIES; RECOVERY OF FUNCTION; SOCIOECONOMIC FACTORS; YOUNG ADULT;

EID: 84928810070     PISSN: 18789293     EISSN: 18789307     Source Type: Journal    
DOI: 10.1016/j.dcn.2015.04.006     Document Type: Article

References (78)

1. Agosti, V., Nunes, E., Levin, F., Rates of psychiatric comorbidity among U.S. residents with lifetime cannabis dependence. Am. J. Drug Alcohol Abuse 28:4 (2002), 643–652.
2. Ashtari, M., Avants, B., Cyckowski, L., Cervellione, K.L., Roofeh, D., Cook, P., Kumra, S., Medial temporal structures and memory functions in adolescents with heavy cannabis use. J. Psychiatr. Res. 45:8 (2011), 1055–1066, 10.1016/j.jpsychires.2011.01.004.
3. Batalla, A., Bhattacharyya, S., Yucel, M., Fusar-Poli, P., Crippa, J.A., Nogue, S., Martin-Santos, R., Structural and functional imaging studies in chronic cannabis users: a systematic review of adolescent and adult findings. PLoS ONE, 8(2), 2013, e55821, 10.1371/journal.pone.0055821.
4. Battistella, G., Fornari, E., Annoni, J.M., Chtioui, H., Dao, K., Fabritius, M., Giroud, C., Long-term effects of cannabis on brain structure. Neuropsychopharmacology 39:9 (2014), 2041–2048, 10.1038/npp.2014.67.
5. Bava, S., Frank, L.R., McQueeny, T., Schweinsburg, B.C., Schweinsburg, A.D., Tapert, S.F., Altered white matter microstructure in adolescent substance users. Psychiatry Res. 173:3 (2009), 228–237, 10.1016/j.pscychresns.2009.04.005.
6. Bava, S., Jacobus, J., Mahmood, O., Yang, T.T., Tapert, S.F., Neurocognitive correlates of white matter quality in adolescent substance users. Brain Cogn. 72:3 (2010), 347–354, 10.1016/j.bandc.2009.10.012.
7. Beck, A., Beck Depression Inventory (BDI). 1978, Psychological Corporation, San Antonio, TX.
8. Berghuis, P., Rajnicek, A.M., Morozov, Y.M., Ross, R.A., Mulder, J., Urban, G.M., Harkany, T., Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316:5828 (2007), 1212–1216, 10.1126/science.1137406.
9. Brown, S.A., McGue, M., Maggs, J., Schulenberg, J., Hingson, R., Swartzwelder, S., Murphy, S., A developmental perspective on alcohol and youths 16 to 20 years of age. Pediatrics 121:Suppl. 4 (2008), S290–S310, 10.1542/peds.2007-2243D.
10. Brown, S.A., Myers, M.G., Lippke, L., Tapert, S.F., Stewart, D.G., Vik, P.W., Psychometric evaluation of the Customary Drinking and Drug Use Record (CDDR): a measure of adolescent alcohol and drug involvement. J. Stud. Alcohol 59:4 (1998), 427–438.
11. Brown, S.A., Tapert, S.F., Granholm, E., Delis, D.C., Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol. Clin. Exp. Res. 24:2 (2000), 164–171.
12. Casey, B.J., Jones, R.M., Hare, T.A., The adolescent brain. Ann. N. Y. Acad. Sci. 1124 (2008), 111–126, 10.1196/annals.1440.010.
13. Cheetham, A., Allen, N.B., Whittle, S., Simmons, J.G., Yucel, M., Lubman, D.I., Orbitofrontal volumes in early adolescence predict initiation of cannabis use: a 4-year longitudinal and prospective study. Biol. Psychiatry 71:8 (2012), 684–692, 10.1016/j.biopsych.2011.10.029.
14. Cousijn, J., Goudriaan, A.E., Wiers, R.W., Reaching out towards cannabis: approach-bias in heavy cannabis users predicts changes in cannabis use. Addiction 106:9 (2011), 1667–1674, 10.1111/j. 1360-0443.2011.03475.x.
15. Cousijn, J., Wiers, R.W., Ridderinkhof, K.R., van den Brink, W., Veltman, D.J., Goudriaan, A.E., Grey matter alterations associated with cannabis use: results of a VBM study in heavy cannabis users and healthy controls. Neuroimage 59:4 (2012), 3845–3851, 10.1016/j.neuroimage.2011.09.046.
16. Crews, F.T., Nixon, K., Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol Alcohol. 44:2 (2009), 115–127, 10.1093/alcalc/agn079.
17. Dale, A.M., Fischl, B., Sereno, M.I., Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:2 (1999), 179–194, 10.1006/nimg.1998.0395.
18. Demirakca, T., Sartorius, A., Ende, G., Meyer, N., Welzel, H., Skopp, G., Hermann, D., Diminished gray matter in the hippocampus of cannabis users: possible protective effects of cannabidiol. Drug Alcohol Depend. 114:2–3 (2011), 242–245, 10.1016/j.drugalcdep.2010.09.020.
19. Desikan, R.S., Segonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., Killiany, R.J., An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:3 (2006), 968–980, 10.1016/j.neuroimage.2006.01.021.
20. Filbey, F.M., Aslan, S., Calhoun, V.D., Spence, J.S., Damaraju, E., Caprihan, A., Segall, J., Long-term effects of marijuana use on the brain. Proc. Natl. Acad. Sci. U. S. A., 2014, 10.1073/pnas.1415297111.
21. Fischl, B., Dale, A.M., Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc. Natl. Acad. Sci. U. S. A. 97:20 (2000), 11050–11055.
22. Fischl, B., Sereno, M.I., Dale, A.M., Cortical surface-based analysis. II. Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:2 (1999), 195–207, 10.1006/nimg.1998.0396.
23. Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., Dale, A.M., Automatically parcellating the human cerebral cortex. Cereb. Cortex 14:1 (2004), 11–22.
24. Giedd, J.N., Structural magnetic resonance imaging of the adolescent brain. Ann. N. Y. Acad. Sci. 1021 (2004), 77–85, 10.1196/annals.1308.009.
25. Giedd, J.N., Lalonde, F.M., Celano, M.J., White, S.L., Wallace, G.L., Lee, N.R., Lenroot, R.K., Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J. Am. Acad. Child Adolesc. Psychiatry 48:5 (2009), 465–470, 10.1097/CHI.0b013e31819f2715.
26. Gilman, J.M., Kuster, J.K., Lee, S., Lee, M.J., Kim, B.W., Makris, N., Breiter, H.C., Cannabis use is quantitatively associated with nucleus accumbens and amygdala abnormalities in young adult recreational users. J. Neurosci. 34:16 (2014), 5529–5538, 10.1523/JNEUROSCI. 4745-13.2014.
27. Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., 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.
28. Hall, W., What has research over the past two decades revealed about the adverse health effects of recreational cannabis use?. Addiction, 2014, 10.1111/add.12703.
29. Han, X., Jovicich, J., Salat, D., van der Kouwe, A., Quinn, B., Czanner, S., Fischl, B., Reliability of MRI-derived measurements of human cerebral cortical thickness: the effects of field strength, scanner upgrade and manufacturer. Neuroimage 32:1 (2006), 180–194, 10.1016/j.neuroimage.2006.02.051.
30. Huestis, M.A., Cone, E.J., Differentiating new marijuana use from residual drug excretion in occasional marijuana users. J. Anal. Toxicol. 22 (1998), 445–454.
31. Huttenlocher, P.R., Dabholkar, A.S., Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387:2 (1997), 167–178.
32. Im, K., Lee, J.M., Lyttelton, O., Kim, S.H., Evans, A.C., Kim, S.I., Brain size and cortical structure in the adult human brain. Cereb. Cortex 18:9 (2008), 2181–2191, 10.1093/cercor/bhm244.
33. Iversen, L., Cannabis and the brain. Brain 126 (2003), 1252–1270.
34. Jacobus, J., Squeglia, L.M., Bava, S., Tapert, S.F., White matter characterization of adolescent binge drinking with and without co-occurring marijuana use: a 3-year investigation. Psychiatry Res. 214:3 (2013), 374–381, 10.1016/j.pscychresns.2013.07.014.
35. Jacobus, J., Squeglia, L.M., Infante, M.A., Bava, S., Tapert, S.F., White matter integrity pre- and post marijuana and alcohol initiation in adolescence. Brain Sci. 3:1 (2013), 396–414, 10.3390/brainsci3010396.
36. Jacobus, J., Squeglia, L.M., Sorg, S.F., Nguyen-Louie, T.T., Tapert, S.F., Cortical thickness and neurocognition in adolescent marijuana and alcohol users following 28 days of monitored abstinence. J. Stud. Alcohol Drugs 75:5 (2014), 729–743.
37. Johnston, L.D., O'Malley, P.M., Miech, R.A., Bachman, J.G., Schulenberg, J.E., Monitoring the Future National Survey Results on Drug Use: 1975-2014: Overview, Key Findings on Adolescent Drug Use. 2015, Institute for Social Research, The University of Michigan, Ann Arbor.
38. Kim, D., Thayer, S.A., Cannabinoids inhibit the formation of new synapses between hippocampal neurons in culture. J. Neurosci., 21(10), 2001, RC146.
39. Kim, H.J., Waataja, J.J., Thayer, S.A., Cannabinoids inhibit network-driven synapse loss between hippocampal neurons in culture. J. Pharmacol. Exp. Ther. 325:3 (2008), 850–858, 10.1124/jpet.107.131607.
40. Kuperberg, G.R., Broome, M.R., McGuire, P.K., David, A.S., Eddy, M., Ozawa, F., Fischl, B., Regionally localized thinning of the cerebral cortex in schizophrenia. Arch. Gen. Psychiatry 60:9 (2003), 878–888.
41. Lopez-Larson, M.P., Bogorodzki, P., Rogowska, J., McGlade, E., King, J.B., Terry, J., Yurgelun-Todd, D., Altered prefrontal and insular cortical thickness in adolescent marijuana users. Behav. Brain Res. 220 (2011), 164–172.
42. Lorenzetti, V., Solowij, N., Whittle, S., Fornito, A., Lubman, D.I., Pantelis, C., Yucel, M., Gross morphological brain changes with chronic, heavy cannabis use. Br. J. Psychiatry, 2014, 10.1192/bjp.bp.114.151407.
43. Lucas, C.P., Zhang, H., Fisher, P.W., Shaffer, D., Regier, D.A., Narrow, W.E., Friman, P., The DISC Predictive Scales (DPS): efficiently screening for diagnoses. J. Am. Acad. Child Adolesc. Psychiatry 40:4 (2001), 443–449, 10.1097/00004583-200104000-00013.
44. McQueeny, T., Padula, C.B., Price, J., Medina, K.L., Logan, P., Tapert, S.F., Gender effects on amygdala morphometry in adolescent marijuana users. Behav. Brain Res. 224:1 (2011), 128–134, 10.1016/j.bbr.2011.05.031.
45. Medina, K.L., Nagel, B.J., Tapert, S.F., Abnormal cerebellar morphometry in abstinent adolescent marijuana users. Psychiatry Res. 182:2 (2010), 152–159, 10.1016/j.pscychresns.2009.12.004.
46. Meier, M.H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R.S., Moffitt, T.E., Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc. Natl. Acad. Sci. U. S. A., 2012, 10.1073/pnas.1206820109.
47. Mountcastle, V.B., The columnar organization of the neocortex. Brain 120 (1997), 701–722.
48. Ostby, Y., Tamnes, C.K., Fjell, A.M., Westlye, L.T., Due-Tonnessen, P., Walhovd, K.B., Heterogeneity in subcortical brain development: A structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J. Neurosci. 29:38 (2009), 11772–11782, 10.1523/JNEUROSCI. 1242-09.2009.
49. Pakkenberg, B., Gundersen, H.J., Neocortical neuron number in humans: effect of sex and age. J. Comp. Neurol. 384:2 (1997), 312–320.
50. Paus, T., Keshavan, M., Giedd, J.N., Why do many psychiatric disorders emerge during adolescence?. Nat. Rev. Neurosci. 9:12 (2008), 947–957, 10.1038/nrn2513.
51. Rakic, P., Specification of cerebral cortical areas. Science 241:4862 (1988), 170–176.
52. Reuter, M., Rosas, H.D., Fischl, B., Highly accurate inverse consistent registration: a robust approach. Neuroimage 53:4 (2010), 1181–1196, 10.1016/j.neuroimage.2010.07.020.
53. Reuter, M., Schmansky, N.J., Rosas, H.D., Fischl, B., Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage 61:4 (2012), 1402–1418, 10.1016/j.neuroimage.2012.02.084.
54. Rice, J.P., Reich, T., Bucholz, K.K., Neuman, R.J., Fishman, R., Rochberg, N., Begleiter, H., Comparison of direct interview and family history diagnoses of alcohol dependence. Alcohol. Clin. Exp. Res. 19:4 (1995), 1018–1023.
55. Rosas, H.D., Liu, A.K., Hersch, S., Glessner, M., Ferrante, R.J., Salat, D.H., Fischl, B., Regional and progressive thinning of the cortical ribbon in Huntington's disease. Neurology 58:5 (2002), 695–701.
56. Rubino, T., Parolaro, D., Long lasting consequences of cannabis exposure in adolescence. Mol. Cell. Endocrinol. 286 (2008), S108–S113, 10.1016/j.mce.2008.02.003.
57. Salat, D.H., Buckner, R.L., Snyder, A.Z., Greve, D.N., Desikan, R.S., Busa, E., Fischl, B., Thinning of the cerebral cortex in aging. Cereb. Cortex 14:7 (2004), 721–730.
58. Sartor, C.E., Lynskey, M.T., Heath, A.C., Jacob, T., True, W., The role of childhood risk factors in initiation of alcohol use and progression to alcohol dependence. Addiction 102:2 (2007), 216–225.
59. Schacht, J.P., Hutchison, K.E., Filbey, F.M., Associations between cannabinoid receptor-1 (CNR1) variation and hippocampus and amygdala volumes in heavy cannabis users. Neuropsychopharmacology 37:11 (2012), 2368–2376, 10.1038/npp.2012.92.
60. Shaffer, D., Fisher, P., Dulcan, M.K., Davies, M., Piacentini, J., Schwab-Stone, M.E., Regier, D.A., The NIMH diagnostic interview schedule for children version 2.3 (DISC-2.3): description, acceptability, prevalence rates, and performance in the MECA Study. Methods for the epidemiology of child and adolescent mental disorders study. J. Am. Acad. Child Adolesc. Psychiatry 35:7 (1996), 865–877.
61. Simmonds, D.J., Hallquist, M.N., Asato, M., Luna, B., Developmental stages and sex differences of white matter and behavioral development through adolescence: a longitudinal diffusion tensor imaging (DTI) study. Neuroimage 92 (2014), 356–368, 10.1016/j.neuroimage.2013.12.044.
62. Smith, M.L., Barnes, A.J., Huestis, M.A., Identifying new cannabis use with urine creatinine-normalized THCCOOH concentrations and time intervals between specimen collections. J. Anal. Toxicol. 33 (2009), 185–189.
63. Sobell, L.C., Sobell, M.B., Timeline Follow Back. A Technique for Assessing Self-Reported Alcohol Consumption. 1992, Humana Press, New York, NY.
64. Sowell, E.R., Peterson, B.S., Thompson, P.M., Welcome, S.E., Henkenius, A.L., Toga, A.W., Mapping cortical change across the human life span. Nat. Neurosci. 6:3 (2003), 309–315, 10.1038/nn1008.
65. Spear, L.P., The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24:4 (2000), 417–463.
66. Spear, L.P., Varlinskaya, E.I., Adolescence. Alcohol sensitivity, tolerance, and intake. Recent Dev. Alcohol. 17 (2005), 143–159.
67. Spielberger, C., Gorsuch, R., Lushene, R., Manual for the State-Trait Anxiety Inventory. 1970, Consulting Psychologists Press, Palo Alto, CA, USA.
68. Squeglia, L.M., Jacobus, J., Brumback, T., Meloy, M.J., Tapert, S.F., White matter integrity in alcohol-naive youth with a family history of alcohol use disorders. Psychol. Med. 44:13 (2014), 2775–2786, 10.1017/S0033291714000609.
69. Squeglia, L.M., Sorg, S.F., Schweinsburg, A.D., Wetherill, R.R., Pulido, C., Tapert, S.F., Binge drinking differentially affects adolescent male and female brain morphometry. Psychopharmacology (Berl) 220:3 (2012), 529–539, 10.1007/s00213-011-2500-4.
70. Squeglia, L.M., Spadoni, A.D., Infante, M.A., Myers, M.G., Tapert, S.F., Initiating moderate to heavy alcohol use predicts changes in neuropsychological functioning for adolescent girls and boys. Psychol. Addict. Behav. 23:4 (2009), 715–722.
71. Squeglia, L.M., Tapert, S.F., Sullivan, E.V., Jacobus, J., Meloy, M.J., Rohlfing, T., Pfefferbaum, A., Brain development in heavy drinking adolescents. Am. J. Psychiatry, 2015 (in press).
72. Stella, N., Chronic THC intake modifies fundamental cerebellar functions. J. Clin. Invest., 2013, 10.1172/JCI70226.
73. Storsve, A.B., Fjell, A.M., Tamnes, C.K., Westlye, L.T., Overbye, K., Aasland, H.W., Walhovd, K.B., Differential longitudinal changes in cortical thickness, surface area and volume across the adult life span: regions of accelerating and decelerating change. J. Neurosci. 34:25 (2014), 8488–8498, 10.1523/JNEUROSCI. 0391-14.2014.
74. Tamnes, C.K., Ostby, Y., Fjell, A.M., Westlye, L.T., Due-Tonnessen, P., Walhovd, K.B., Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb. Cortex 20:3 (2009), 534–548.
75. Tapert, S.F., Granholm, E., Leedy, N.G., Brown, S.A., Substance use and withdrawal: neuropsychological functioning over 8 years in youth. J. Int. Neuropsychol. Soc. 8 (2002), 873–883.
76. Tsou, K., Brown, S., Sanudo-Pena, M.C., Mackie, K., Walker, J.M., Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:2 (1998), 393–411.
77. Wechsler, D., (eds.) Manual for the Wechsler Abbreviated Scale of Intelligence, 1999, Psychological Corporation, San Antonio, TX.
78. Yakovlev, P.I., Lecours, A.R., The myelogenetic cycles of regional maturation of the brain. Mikowski, A., (eds.) Regional Development of the Brain in Early Life, 1967, Blackwell Scientific, Oxford, England, 3–70.