Effect of long-term cannabis use on axonal fibre connectivity

Brain

Volumn 135, Issue 7, 2012, Pages 2245-2255

  Zalesky, Andrew ^a   Solowij, Nadia ^b   Yücel, Murat ^a   Lubman, Dan I ^c   Takagi, Michael ^a   Harding, Ian H ^a   Lorenzetti, Valentina ^a   Wang, Ruopeng ^d   Searle, Karissa ^a   Pantelis, Christos ^a   Seal, Marc ^e  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF WOLLONGONG   (Australia)

^c EASTERN HEALTH   (Australia)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

Axonal connectivity; Cannabis; Diffusion tensor imaging; Diffusion weighted imaging; White matter

Indexed keywords

CANNABIS;

ADULT; AGE; ARTICLE; BRAIN FORNIX; BRAIN MAPPING; CONTROLLED STUDY; CORPUS CALLOSUM; DIFFUSION WEIGHTED IMAGING; FEMALE; HUMAN; MALE; NERVE FIBER; PRIORITY JOURNAL; WHITE MATTER;

EID: 84863204350     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws136     Document Type: Article

References (74)

1. Ahuja RK, Magnanti TL, Orlin JB. Network flows: theory algorithms and applications. Englewood Cliffs, NJ: Prentice Hall; 1993.
2. Arnone D, Abou-Saleh MT, Barrick TR. Diffusion tensor imaging of the corpus callosum in addiction. Neuropsychobiology 2006; 54: 107-13. (Pubitemid 46143893)
3. Arnone D, Barrick TR, Chengappa S, Mackay CE, Clark CA, Abou-Saleh MT. Corpus callosum damage in heavy marijuana use: preliminary evidence from diffusion tensor tractography and tract-based spatial statistics. Neuroimage 2008; 41: 1067-74.
4. Ashtari M, Cervellione K, Cottone J, Ardekani BA, Sevy S, Kumra S. Diffusion abnormalities in adolescents and young adults with a history of heavy cannabis use. J Psychiatr Res 2009; 43: 189-204.
5. Bai F, Shu N, Yuan Y, Shi Y, Yu H, Wu D, et al. Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J Neurosci 2012; 32: 4307-18.
6. Barnea-Goraly N, Menon V, Eckert M, Tamm L, Bammer R, Karchemskiy A, et al. White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb Cortex 2005; 15: 1848-54. (Pubitemid 41628326)
7. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, et al. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 1992; 70: 31-46.
8. Bava S, Jacobus J, Mahmood O, Yang TT, Tapert SF. Neurocognitive correlates of white matter quality in adolescent substance users. Brain Cogn 2010; 72: 347-54.
9. Block RI, O'Leary DS, Ehrhardt JC, Augustinack JC, Ghoneim MM, Arndt S, et al. Effects of frequent marijuana use on brain tissue volume and composition. Neuroreport 2000; 11: 491-6.
10. Buchan BJ, L Dennis M, Tims FM, Diamond GS. Cannabis use: consistency and validity of self-report, on-site urine testing and laboratory testing. Addiction 2002; 1: 98-108. (Pubitemid 36009096)
11. Budde MD, Xie M, Cross AH, Song SK. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. J Neurosci 2009; 29: 2805-13.
12. Bullmore ET, Sporns O. Complex brain networks: graph-theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009; 10: 186-98.
13. Catani M, Howard RJ, Pajevic S, Jones DK. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 2002; 17: 77-94.
14. Cohen M, Rasser PE, Peck G, Carr VJ, Ward PB, Thompson PM, et al. Cerebellar grey-matter deficits, cannabis use and first-episode schizophrenia in adolescents and young adults. Int J Neuropsychopharmacol 2012; 15: 297-307.
15. Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 1999; 96: 10422-7. (Pubitemid 29422574)
16. Cousijn J, Wiers RW, Ridderinkhof KR, van den Brink W, Veltman DJ, Goudriaan AE. Grey matter alterations associated with cannabis use: results of a VBM study in heavy cannabis users and healthy controls. Neuroimage 2012; 59: 3845-51.
17. Dalton VS, Zavitsanou K. Cannabinoid effects on CB1 receptor density in the adolescent brain: an autoradiographic study using the synthetic cannabinoid HU210. Synapse 2010; 64: 845-54.
18. Dekker N, Schmitz N, Peters BD, van Amelsvoort TA, Linszen DH, de Haan L. Cannabis use and callosal white matter structure and integrity in recent-onset schizophrenia. Psychiatry Res 2010; 181: 51-6.
19. Delisi LE, Bertisch HC, Szulc KU, Majcher M, Brown K, Bappal A, et al. A preliminary DTI study showing no brain structural change associated with adolescent cannabis use. Harm Reduct J 2006; 3: 17.
20. Fornito A, Yoon J, Zalesky A, Bullmore ET, Carter CS. General and specific functional connectivity disturbances in first episode schizophrenia during cognitive control performance. Biol Psychiatry 2011; 70: 64-72.
21. Glass M, Dragunow M, Faull RL. Cannabinoid receptors in the human brain: a detailed anatomical and quantitative autoradiographic study in the fetal, neonatal and adult human brain. Neuroscience 1998; 77: 299-318. (Pubitemid 27079604)
22. Gruber SA, Silveri MM, Dahlgren MK, Yurgelun-Todd D. Why so impulsive? White matter alterations are associated with impulsivity in chronic marijuana smokers. Exp Clin Psychopharmacol 2011; 19: 231-42.
23. Gruber SA, Yurgelun-Todd DA. Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Brain Res Cogn Brain Res 2005; 23: 107-18. (Pubitemid 40417511)
24. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, et al. Mapping the structural core of human cerebral cortex. PLoS Biol 2008; 6: e159.
25. Harrison L. The validity of self-reported drug use in survey research: an overview and critique of research methods. NIDA Res Monogr 1997; 167: 17-36.
26. Hayasaka S, Laurienti PJ. Comparison of characteristics between region-and voxel-based network analyses in resting-state fMRI data. Neuroimage 2010; 50: 499-508.
27. He Y, Evans A. Graph theoretical modeling of brain connectivity. Curr Opin Neurol 2010; 23: 341-50.
28. Ho BC, Wassink TH, Ziebell S, Andreasen NC. Cannabinoid receptor 1 gene polymorphisms and marijuana misuse interactions on white matter and cognitive deficits in schizophrenia. Schizophr Res 2011; 128: 66-75.
29. Jacobus J, McQueeny T, Bava S, Schweinsburg BC, Frank LR, Yang TT, et al. White matter integrity in adolescents with histories of marijuana use and binge drinking. Neurotoxicol Teratol 2009; 31: 349-55.
30. Jager G, Van Hell HH, De Win MM, Kahn RS, Van Den Brink W, Van Ree JM, et al. Effects of frequent cannabis use on hippocampal activity during an associative memory task. Eur Neuropsychopharmacol 2007; 17: 289-97. (Pubitemid 46156994)
31. James A, Hough M, James S, Winmill L, Burge L, Nijhawan S, et al. Greater white and grey matter changes associated with early cannabis use in adolescent-onset schizophrenia (AOS). Schizophr Res 2011; 128: 91-7.
32. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002; 17: 825-41. (Pubitemid 35317016)
33. Kim D-J, Skosnik PD, Cheng H, Pruce BJ, Brumbaugh MS, Vollmer JM, et al. Structural network topology revealed by white matter tractography in cannabis users: a graph theoretical analysis. Brain Connect 2011; 1: 473-83.
34. Kumra S. Schizophrenia and cannabis use. Minn Med 2007; 90: 36-8.
35. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001; 13: 534-46. (Pubitemid 32231507)
36. Lim KO, Helpern JA. Neuropsychiatric applications of DTI: a review. NMR Biomed 2002; 15: 587-93.
37. Lorenzetti V, Lubman DI, Whittle S, Solowij N, Yücel M. Structural MRI findings in long-term cannabis users: what do we know? Subst Use Misuse 2010; 45: 1787-808.
38. Martin-Santos R, Fagundo AB, Crippa JA, Atakan Z, Bhattacharyya S, Allen P, et al. Neuroimaging in cannabis use: a systematic review of the literature. Psychol Med 2010; 40: 383-98.
39. Matochik JA, Eldreth DA, Cadet JL, Bolla KI. Altered brain tissue composition in heavy marijuana users. Drug Alcohol Depend 2005; 77: 23-30. (Pubitemid 39656096)
40. Medina KL, Schweinsburg AD, Cohen-Zion M, Nagel BJ, Tapert SF. Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicol Teratol 2007; 29: 141-52. (Pubitemid 46205161)
41. Molina-Holgado E, Vela JM, Arevalo-Martin A, Almazan G, Molina-Holgado F, Borrell J, et al. Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling. J Neurosci 2002; 22: 9742-53. (Pubitemid 35332857)
42. Nichols TE, Hayasaka S. Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res 2003; 12: 419-46. (Pubitemid 37368969)
43. Peters BD, de Haan L, Vlieger EJ, Majoie CB, den Heeten GJ, Linszen DH. Recent-onset schizophrenia and adolescent cannabis use: MRI evidence for structural hyperconnectivity? Psychopharmacol Bull 2009; 42: 75-88.
44. Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 1996; 6: 893-906. (Pubitemid 26396817)
45. Rais M, Cahn W, Van Haren N, Schnack H, Caspers E, Hulshoff Pol H, et al. Excessive brain volume loss over time in cannabis-using first-episode schizophrenia patients. Am J Psychiatry 2008; 165: 490-6. (Pubitemid 351694292)
46. Romero J, Garcia-Palomero E, Berrendero F, Garcia-Gil L, Hernandez ML, Ramos JA, et al. Atypical location of cannabinoid receptors in white matter areas during rat brain development. Synapse 1997; 26: 317-23. (Pubitemid 27240747)
47. Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretation. Neuroimage 2010; 52: 1059-69.
48. Sobell LC, Sobell MB. Timeline follow-back: a technique for assessing self-reported alcohol consumption. In: Litten RZ, Allen JP, editors. Measuring alcohol consumption: psychosocial and biochemical methods. Totowa, NJ: Humana; 1992. p. 41-72.
49. Solowij N, Jones KA, Rozman ME, Davis SM, Ciarrochi J, Heaven PCL, et al. Verbal learning and memory in adolescent cannabis users, alcohol users and non-users. Psychopharmacology 2011a; 216: 131-44.
50. Solowij N, Jones KA, Rozman ME, Davis SM, Ciarrochi J, Heaven PCL, et al. Reflection impulsivity in adolescent cannabis users: a comparison with alcohol-using and non-substance using adolescents. Psychopharmacology 2012; 219: 575-86.
51. Solowij N, Pesa N. Cannabis and cognition: short and long-term effects. In: Castle D, Murray R, D'Souza DC, editors. Marijuana and madness. 2nd edn. Cambridge: Cambridge University Press; 2012. p. 91-102.
52. Solowij N, Yücel M, Respondek C, Whittle S, Lindsay E, Pantelis C, et al. Cerebellar white-matter changes in cannabis users with and without schizophrenia. Psychol Med 2011b; 41: 2349-59.
53. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26: 132-40. (Pubitemid 40602893)
54. Swift W, Copeland J, Hall W. Choosing a diagnostic cut-off for cannabis dependence. Addiction 1998; 93: 1681-92. (Pubitemid 28523974)
55. Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP. Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 2008; 42: 617-25.
56. Tzilos GK, Cintron CB, Wood JB, Simpson NS, Young AD, Pope HG Jr, et al. Lack of hippocampal volume change in long term heavy cannabis users. Am J Addict 2005; 14: 64-72. (Pubitemid 40204735)
57. van den Heuvel MP, Hulshoff Pol HE. Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 2010; 20: 519-34.
58. van den Heuvel MP, Stam CJ, Boersma M, Hulshoff Pol HE. Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain. Neuroimage 2008; 3: 528-39.
59. Verstraete E, Veldink JH, Mandl RCW, van den Berg LH, van den Heuvel MP. Impaired structural motor connectome in amyotrophic lateral sclerosis. PLoS One 2011; 6: e24239.
60. Vollmar C, O'Muircheartaigh J, Barker GJ, Symms MR, Thompson P, Kumari V, et al. Identical, but not the same: intra-site and inter-site reproducibility of fractional anisotropy measures on two 3.0 T scanners. Neuroimage 2010; 51: 1384-94.
61. Walterfang M, Velakoulis D, Whitford TJ, Pantelis C. Understanding aberrant white matter development in schizophrenia: an avenue for therapy? Expert Rev Neurother 2011; 11: 971-87.
62. Wang R, Benner T, Sorensen AG, Wedeen VJ. Diffusion Toolkit: a software package for diffusion imaging data processing and tractography. Proc Intl Soc Mag Reson Med 2007; 15: 3720.
63. Westin C-F, Maier SE, Mamata H, Nabavi A, Jolesz FA, Kikinis R. Processing and visualization for diffusion tensor MRI. Med Image Anal 2002; 6: 93-108. (Pubitemid 35282820)
64. Wexler BE, Zhu H, Bell MD, Nicholls SS, Fulbright RK, Gore JC, et al. Neuropsychological near normality and brain structure abnormality in schizophrenia. Am J Psychiatry 2009; 166: 189-95.
65. Wheeler-Kingshott CA, Cercignani M. About "axial" and "radial" diffusivities. Magn Reson Med 2009; 61: 1255-60.
66. Wig GS, Schlaggar BL, Petersen SE. Concepts and principles in the analysis of brain networks. Ann N Y Acad Sci 2011; 1224: 126-46.
67. Yücel M, Solowij N, Respondek C, Whittle S, Fornito A, Pantelis C, et al. Regional brain abnormalities associated with long-term heavy cannabis use. Arch Gen Psychiatry 2008; 65: 694-701. (Pubitemid 351787240)
68. Yücel M, Zalesky A, Takagi M, Bora E, Fornito A, Ditchfield M, et al. White-matter abnormalities in adolescents with long-term inhalant and cannabis use: a diffusion magnetic resonance imaging study. J Psychiatr Neurosci 2010; 35: 409-12.
69. Zalesky A, Cocchi L, Fornito A, Murray MM, Bullmore E. Connectivity differences in brain networks. Neuroimage 2012; 60: 1055-62.
70. Zalesky A, Fornito A. A DTI-derived measure of cortico-cortical connectivity. IEEE Trans Med Imag 2009; 28: 1023-36.
71. Zalesky A, Fornito A, Bullmore ET. Network-based statistic: identifying differences in brain networks. Neuroimage 2010a; 53: 1197-207.
72. Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, et al. Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 2010b; 50: 970-83.
73. Zalesky A, Fornito A, Seal ML, Cocchi L, Westin C-F, Bullmore ET, et al. Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry 2011; 69: 80-9.
74. Zhang J, Wang J, Wu Q, Kuang W, Huang X, He Y, et al. Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biol Psychiatry 2011; 70: 334-42.