Subcortical Local Functional Hyperconnectivity in Cannabis Dependence

Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

Volumn 3, Issue 3, 2018, Pages 285-293

  Manza, Peter ^a   Tomasi, Dardo ^a   Volkow, Nora D ^a,b  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Addiction; Basal ganglia; Emotionality; fMRI; Graph theory; Marijuana; Resting state functional connectivity

Indexed keywords

CANNABIS;

ADULT; AGGRESSION; ALCOHOL CONSUMPTION; ALIENATION; AMYGDALA; ANGER; ARTICLE; BRAIN SIZE; BRAIN STEM; CANNABIS ADDICTION; CANNABIS USE; CONTROLLED STUDY; DELAY DISCOUNTING; EMOTIONALITY; EPISODIC MEMORY; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HOSTILITY; HUMAN; INTELLIGENCE; MAJOR CLINICAL STUDY; MALE; MESENCEPHALON; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; SPATIAL ORIENTATION; STRESS; SUBCORTEX; SUBSTANTIA NIGRA; THALAMUS LATERAL NUCLEUS; TOBACCO USE; VENTRAL STRIATUM; VENTRAL TEGMENTUM; WORKING MEMORY; YOUNG ADULT; ATTENTION; BRAIN; CONNECTOME; DIAGNOSTIC IMAGING; EMOTION; EXECUTIVE FUNCTION; MEMORY; NERVE CELL NETWORK; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOLOGY; REACTION TIME;

ADULT; ATTENTION; BRAIN; CONNECTOME; EMOTIONS; EXECUTIVE FUNCTION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MARIJUANA ABUSE; MEMORY; NERVE NET; NEUROPSYCHOLOGICAL TESTS; REACTION TIME;

EID: 85041107240     PISSN: 24519022     EISSN: 24519030     Source Type: Journal    
DOI: 10.1016/j.bpsc.2017.11.004     Document Type: Article

References (67)

1. Center for Behavioral Health Statistics and Quality. 2015 National Survey on Drug Use and Health: Detailed Tables. 2016, Substance Abuse and Mental Health Services Administration, Rockville, MD.
2. Wiers, C.E., Shokri-Kojori, E., Wong, C.T., Abi-Dargham, A., Demiral, Ş.B., Tomasi, D., et al. Cannabis abusers show hypofrontality and blunted brain responses to a stimulant challenge in females but not in males. Neuropsychopharmacology 41 (2016), 2596–2605.
3. Volkow, N.D., Wang, G.-J., Telang, F., Fowler, J.S., Alexoff, D., Logan, J., et al. Decreased dopamine brain reactivity in marijuana abusers is associated with negative emotionality and addiction severity. Proc Natl Acad Sci U S A 111 (2014), E3149–E3156.
4. Arseneault, L., Cannon, M., Poulton, R., Murray, R., Caspi, A., Moffitt, T.E., Cannabis use in adolescence and risk for adult psychosis: Longitudinal prospective study. BMJ 325 (2002), 1212–1213.
5. Andréasson, S., Engström, A., Allebeck, P., Rydberg, U., Cannabis and schizophrenia: A longitudinal study of Swedish conscripts. Lancet 330 (1987), 1483–1486.
6. Galvez-Buccollini, J.A., Proal, A.C., Tomaselli, V., Trachtenberg, M., Coconcea, C., Chun, J., et al. Association between age at onset of psychosis and age at onset of cannabis use in non-affective psychosis. Schizophr Res 139 (2012), 157–160.
7. Di Forti, M., Sallis, H., Allegri, F., Trotta, A., Ferraro, L., Stilo, S.A., et al. Daily use, especially of high-potency cannabis, drives the earlier onset of psychosis in cannabis users. Schizophr Bull 40 (2014), 1509–1517.
8. Van Os, J., Bak, M., Hanssen, M., Bijl, R.V., De Graaf, R., Verdoux, H., Cannabis use and psychosis: A longitudinal population-based study. Am J Epidemiol 156 (2002), 319–327.
9. Sherif, M., Radhakrishnan, R., D'Souza, D.C., Ranganathan, M., Human laboratory studies on cannabinoids and psychosis. Biol Psychiatry 79 (2016), 526–538.
10. Colizzi, M., Iyegbe, C., Powell, J., Ursini, G., Porcelli, A., Bonvino, A., et al. Interaction between functional genetic variation of DRD2 and cannabis use on risk of psychosis. Schizophr Bull 41 (2015), 1171–1182.
11. Bhattacharyya, S., Atakan, Z., Martin-Santos, R., Crippa, J.A., Kambeitz, J., Prata, D., et al. Preliminary report of biological basis of sensitivity to the effects of cannabis on psychosis: AKT1 and DAT1 genotype modulates the effects of δ-9-tetrahydrocannabinol on midbrain and striatal function. Mol Psychiatry 17 (2012), 1152–1155.
12. Di Forti, M., Iyegbe, C., Sallis, H., Kolliakou, A., Falcone, M.A., Paparelli, A., et al. Confirmation that the AKT1 (rs2494732) genotype influences the risk of psychosis in cannabis users. Biol Psychiatry 72 (2012), 811–816.
13. Park, I.H., Lee, B.C., Kim, J.J., Kim, J.I., Koo, M.S., Effort-based reinforcement processing and functional connectivity underlying amotivation in medicated patients with depression and schizophrenia. J Neurosci 37 (2017), 4370–4380.
14. Sarpal, D.K., Robinson, D.G., Fales, C., Lencz, T., Argyelan, M., Karlsgodt, K.H., et al. Relationship between duration of untreated psychosis and intrinsic corticostriatal connectivity in patients with early phase schizophrenia. Neuropsychopharmacology 42 (2017), 2214–2221.
15. Filbey, F.M., Aslan, S., Calhoun, V.D., Spence, J.S., Damaraju, E., Caprihan, A., et al. Long-term effects of marijuana use on the brain. Proc Natl Acad Sci U S A 111 (2014), 16913–16918.
16. Tomasi, D., Volkow, N.D., Functional connectivity density mapping. Proc Natl Acad Sci U S A 107 (2010), 9885–9890.
17. Tomasi, D., Wang, G., Volkow, N., Energetic cost of brain functional connectivity. Proc Natl Acad Sci U S A 110 (2013), 13642–13647.
18. Shokri-Kojori, E., Tomasi, D., Wiers, C.E., Wang, G.J., Volkow, N.D., Alcohol affects brain functional connectivity and its coupling with behavior: greater effects in male heavy drinkers. Mol Psychiatry 22 (2017), 1185–1195.
19. Wilson, S., Sponheim, S.R., Dimensions underlying psychotic and manic symptomatology: Extending normal-range personality traits to schizophrenia and bipolar spectra. Compr Psychiatry 55 (2014), 1809–1819.
20. Zhuo, C., Zhu, J., Wang, C., Qu, H., Ma, X., Tian, H., et al. Brain structural and functional dissociated patterns in schizophrenia. BMC Psychiatry, 17, 2017, 45.
21. Van Essen, D.C., Ugurbil, K., Auerbach, E., Barch, D., Behrens, T.E.J., Bucholz, R., et al. The Human Connectome Project: A data acquisition perspective. Neuroimage 62 (2012), 2222–2231.
22. Berenbaum, H., Fujita, F., Schizophrenia and personality: Exploring the boundaries and connections between vulnerability and outcome. J Abnorm Psychol 103 (1994), 148–158.
23. Watson, D., Clark, L.A., Harkness, A.R., Structures of personality and their relevance to psychopathology. J Abnorm Psychol 103 (1994), 18–31.
24. Kotov, R., Gamez, W., Schmidt, F., Watson, D., Linking “big” personality traits to anxiety, depressive, and substance use disorders: A meta-analysis. Psychol Bull 136 (2010), 768–821.
25. Krueger, R.F., Tackett, J.L., Personality and psychopathology: Working toward the bigger picture. J Pers Disord 17 (2003), 109–128.
26. Insel, T., Cuthbert, B., Garvie, M., Heinssen, R., Pine, D.S., Quinn, K., et al. Research Domain Criteria (RDoC): Toward a new classification framework for research on mental disorders. Am J Psychiatry 167 (2010), 748–751.
27. Horan, W.P., Blanchard, J.J., Clark, L.A., Green, M.F., Affective traits in schizophrenia and schizotypy. Schizophr Bull 34 (2008), 856–874.
28. Weiland, B.J., Thayer, R.E., Depue, B.E., Sabbineni, A., Bryan, A.D., Hutchison, K.E., Daily marijuana use is not associated with brain morphometric measures in adolescents or adults. J Neurosci 35 (2015), 1505–1512.
29. Orr, J.M., Paschall, C.J., Banich, M.T., Recreational marijuana use impacts white matter integrity and subcortical (but not cortical) morphometry. Neuroimage Clin 12 (2016), 47–56.
30. Volkow, N.D., Swanson, J.M., Evins, A.E., DeLisi, L.E., Meier, M.H., Gonzalez, R., et al. Effects of cannabis use on human behavior, including cognition, motivation, and psychosis: A review. JAMA Psychiatry 73 (2016), 292–297.
31. DeDora, D.J., Nedic, S., Katti, P., Arnab, S., Wald, L.L., Takahashi, A., et al. Signal fluctuation sensitivity: An improved metric for optimizing detection of resting-state fMRI networks. Front Neurosci 10 (2016), 1–15.
32. Manza, P., Zhang, S., Hu, S., Chao, H.H., Leung, H.-C., Li, C.-S.R., The effects of age on resting state functional connectivity of the basal ganglia from young to middle adulthood. Neuroimage 107 (2015), 311–322.
33. Manza, P., Zhang, S., Li, C.-S.R., Leung, H.-C., Resting-state functional connectivity of the striatum in early-stage Parkinson's disease: Cognitive decline and motor symptomatology. Hum Brain Mapp 37 (2016), 648–662.
34. Eklund, A., Nichols, T.E., Knutsson, H., Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. [published correction appears in Proc Natl Acad Sci U S A 2016; 113:E4929] Proc Natl Acad Sci U S A 113 (2016), 7900–7905.
35. Nader, D.A., Sanchez, Z.M., Effects of regular cannabis use on neurocognition, brain structure, and function: A systematic review of findings in adults. Am J Drug Alcohol Abuse 44 (2018), 4–18.
36. Meier, M.H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R.S.E., et al. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc Natl Acad Sci U S A 109 (2012), E2657–E2664.
37. Rolland, B., Amad, A., Poulet, E., Bordet, R., Vignaud, A., Bation, R., et al. Resting-state functional connectivity of the nucleus accumbens in auditory and visual hallucinations in schizophrenia. Schizophr Bull 41 (2015), 291–299.
38. Cole, D.M., Oei, N.Y., Soeter, R.P., Both, S., van Gerven, J.M., Rombouts, S.A., Beckmann, C.F., Dopamine-dependent architecture of cortico-subcortical network connectivity. Cereb Cortex 23 (2013), 1509–1516.
39. Cole, D.M., Beckmann, C.F., Oei, N.Y., Both, S., van Gerven, J.M., Rombouts, S.A., Differential and distributed effects of dopamine neuromodulations on resting-state network connectivity. Neuroimage 78 (2013), 59–67.
40. Pujol, J., Blanco-Hinojo, L., Batalla, A., López-Solà M., Harrison, B.J., Soriano-Mas, C., et al. Functional connectivity alterations in brain networks relevant to self-awareness in chronic cannabis users. J Psychiatr Res 51 (2014), 68–78.
41. Blanco-Hinojo, L., Pujol, J., Harrison, B.J., Macià D., Batalla, A., Nogué S., et al. Attenuated frontal and sensory inputs to the basal ganglia in cannabis users. Addict Biol 22 (2017), 1036–1047.
42. Tomasi, D., Volkow, N.D., Functional connectivity hubs in the human brain. Neuroimage 57 (2011), 908–917.
43. Tomasi, D., Volkow, N.D., Mapping small-world properties through development in the human brain: Disruption in schizophrenia. PLoS One, 9, 2014, e96176.
44. Tomasi, D., Volkow, N., Aging and functional brain networks. Mol Psychiatry 17 (2012), 549–558.
45. Tomasi, D., Volkow, N.D., Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71 (2012), 443–450.
46. Konova, A.B., Moeller, S.J., Tomasi, D., Goldstein, R.Z., Effects of chronic and acute stimulants on brain functional connectivity hubs. Brain Res 1628 (2015), 147–156.
47. Goldstein, R.Z., Volkow, N.D., Dysfunction of the prefrontal cortex in addiction: Neuroimaging findings and clinical implications. Nat Rev Neurosci 12 (2011), 652–669.
48. Volkow, N.D., Wang, G.-J., Kollins, S.H., Wigal, T.L., Newcorn, J.H., Telang, F., et al. Evaluating dopamine reward pathway in ADHD: Clinical implications. JAMA 302 (2009), 1084–1091.
49. Volkow, N.D., Wang, G.J., Fowler, J.S., Tomasi, D., Telang, F., Addiction: Beyond dopamine reward circuitry. Proc Natl Acad Sci U S A 108 (2011), 15037–15042.
50. Crossley, N.A., Mechelli, A., Scott, J., Carletti, F., Fox, P.T., Mcguire, P., Bullmore, E.T., The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137 (2014), 2382–2395.
51. Martz, M.E., Trucco, E.M., Cope, L.M., Hardee, J.E., Jester, J.M., Zucker, R.A., Heitzeg, M.M., Association of marijuana use with blunted nucleus accumbens response to reward anticipation. JAMA Psychiatry 370 (2016), 2219–2227.
52. van Hell, H.H., Vink, M., Ossewaarde, L., Jager, G., Kahn, R.S., Ramsey, N.F., Chronic effects of cannabis use on the human reward system: An fMRI study. Eur Neuropsychopharmacol 20 (2010), 153–163.
53. Frank, M.J., Dynamic dopamine modulation in the basal ganglia: A neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J Cogn Neurosci 17 (2005), 51–72.
54. Vukadinovic, Z., Herman, M.S., Rosenzweig, I., Cannabis, psychosis and the thalamus: A theoretical review. Neurosci Biobehav Rev 37 (2013), 658–667.
55. Buchy, L., Cannon, T.D., Anticevic, A., Lyngberg, K., Cadenhead, K.S., Cornblatt, B.A., et al. Evaluating the impact of cannabis use on thalamic connectivity in youth at clinical high risk of psychosis. BMC Psychiatry, 15, 2015, 276.
56. Filbey, F.M., Schacht, J.P., Myers, U.S., Chavez, R.S., Hutchison, K.E., Marijuana craving in the brain. Proc Natl Acad Sci U S A 106 (2009), 13016–13021.
57. Machielsen, M.W., Veltman, D.J., van den Brink, W., de Haan, L., Comparing the effect of clozapine and risperidone on cue reactivity in male patients with schizophrenia and a cannabis use disorder: A randomized fMRI study. [published online ahead of print Mar 25] J Psychopharmacol, 2017.
58. Herkenham, M., Lynn, A.B., Litrle, M.D., Johnsont, M.R., Melvin, L.S., De Costa, B.R., Riceo, K.C., Cannabinoid receptor localization in brain. Proc Natl Acad Sci U S A 87 (1990), 1932–1936.
59. Schierenbeck, T., Riemann, D., Berger, M., Hornyak, M., Effect of illicit recreational drugs upon sleep: Cocaine, ecstasy and marijuana. Sleep Med Rev 12 (2008), 381–389.
60. Conroy, D.A., Kurth, M.E., Strong, D.R., Brower, K.J., Stein, M.D., Marijuana use patterns and sleep among community-based young adults. J Addict Dis 35 (2016), 135–143.
61. Chabrol, H., Duconge, E., Roura, C., Casas, C., Relations between anxious, depressive and borderline symptomatology and frequency of cannabis use and dependence. [in French] Encephale 30 (2004), 141–146.
62. Hasler, B.P., Insana, S.P., James, J.A., Germain, A., Evening-type military veterans report worse lifetime posttraumatic stress symptoms and greater brainstem activity across wakefulness and REM sleep. Biol Psychol 94 (2013), 255–262.
63. Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., et al. Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2 (1999), 861–863.
64. Bossong, M.G., Niesink, R.J.M., Adolescent brain maturation, the endogenous cannabinoid system and the neurobiology of cannabis-induced schizophrenia. Prog Neurobiol 92 (2010), 370–385.
65. Pagliaccio, D., Barch, D.M., Bogdan, R., Wood, P.K., Lynskey, M.T., Heath, A.C., Agrawal, A., Shared predisposition in the association between cannabis use and subcortical brain structure. JAMA Psychiatry 72 (2015), 994–1001.
66. Bloomfield, M.A., Morgan, C.J., Egerton, A., Kapur, S., Curran, H.V., Howes, O.D., Dopaminergic function in cannabis users and its relationship to cannabis-induced psychotic symptoms. Biol Psychiatry 75 (2014), 470–478.
67. Thompson, J.L., Urban, N., Slifstein, M., Xu, X., Kegeles, L.S., Girgis, R.R., et al. Striatal dopamine release in schizophrenia comorbid with substance dependence. Mol Psychiatry 18 (2013), 909–915.