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Research Article

Decreased dopamine brain reactivity in marijuana abusers is associated with negative emotionality and addiction severity

Nora D. Volkow, Gene-Jack Wang, Frank Telang, Joanna S. Fowler, David Alexoff, Jean Logan, Millard Jayne, Christopher Wong, and Dardo Tomasi
PNAS July 29, 2014 111 (30) E3149-E3156; first published July 14, 2014; https://doi.org/10.1073/pnas.1411228111
Nora D. Volkow
aLaboratory of Neuroimaging, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20857;
bNational Institute on Drug Abuse, Rockville, MD 20857;
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  • For correspondence: nvolkow@nida.nih.gov fowler@bnl.gov
Gene-Jack Wang
aLaboratory of Neuroimaging, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20857;
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Frank Telang
aLaboratory of Neuroimaging, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20857;
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Joanna S. Fowler
cBiosciences Department, Brookhaven National Laboratory, Upton, NY 11973; and
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  • For correspondence: nvolkow@nida.nih.gov fowler@bnl.gov
David Alexoff
cBiosciences Department, Brookhaven National Laboratory, Upton, NY 11973; and
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Jean Logan
dDepartment of Radiology, New York University Langone Medical Center, New York, NY 10016
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Millard Jayne
aLaboratory of Neuroimaging, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20857;
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Christopher Wong
aLaboratory of Neuroimaging, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20857;
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Dardo Tomasi
aLaboratory of Neuroimaging, National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20857;
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  1. Contributed by Joanna S. Fowler, June 20, 2014 (sent for review April 9, 2014; reviewed by Bertha Madras, Harvard University Medical School, and Karen Berman, National Institute of Mental Health)

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  • Neuroadaptive changes in marijuana abusers
    - Aug 11, 2014
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  • Fig. 1.
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    Fig. 1.

    Behavioral (A) and cardiovascular (B) effects in healthy controls (black symbols) and marijuana abusers (gray symbols) after placebo (PL; dashed lines) and after MP (continuous lines). (A) MP-induced increases in self-reports of high, drug effects, anxiety, and restlessness were significantly lower for marijuana abusers than controls (P < 0.05). (B) MP-induced increases in heart rate and diastolic blood pressure were lower for marijuana abusers than controls (P < 0.05). BPM, beats per minute.

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    Fig. 2.

    (A) SPM results for the comparison of MP’s effects on DVs (delta measures) between controls and marijuana abusers. The figure shows the contrast controls > abusers, indicating stronger MP-induced decreases in DV in controls (P < 0.005), and color bars indicate t scores. There were no regions where marijuana abusers showed greater decreases than controls. (B) Individual DV values in cerebellum and putamen after placebo (PL) and after MP for the marijuana abusers and the controls. *P < 0.05; **P < 0.005.

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    Fig. 3.

    (A) SPM results for the comparison of MP vs. placebo on the BPND images from [11C]raclopride in marijuana abusers (MA) and in healthy controls (HC) (Puncorr < 0.005) and group comparisons for the effects of MP (ΔBPND) (P < 0.01, cluster size of 10 voxels). The contrast MA > HC indicates that MP induced greater decreases in BPND in midbrain in marijuana abusers (red circles), and color bars indicate t scores. There were no regions where MP decreased BPND more in controls than marijuana abusers. (B) SPM results for the voxel-wise correlation between MP-induced decreases in BPND (ΔBPND) and scores in negative emotionality (NEM). (C) Regression slopes for the correlation between MP-induced changes in BPND (ΔBPND) in the ventral striatum and NEM in healthy controls (blue) and in marijuana abusers (red). The larger the decreases in BPND, the lower were the scores in NEM.

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    Table 1.

    Demographics, clinical characteristics, and personality scores (positive emotionality, negative emotionality, and constraint) of participants, and the significance for the comparisons between healthy controls and marijuana abusers

    ParameterHealthy controls(n = 24)Marijuana abusers(n = 24)P
    Age28.2 ± 626.9 ± 7NS
    Sex50% males50% males
    Education13.9 ± 213.2 ± 1NS
    Body mass index24.3 ± 324.1 ± 4NS
    Tobacco3 active10 active0.02
    1 former2 former
    Marijuana initiation15 ± 3 y of age
    Days per week4.9 ± 3
    Joints per day4.8 ± 3
    Years of abuse10.5 ± 2
    Scores on MDQ5.4 ± 3
    Positive emotionality52.3 ± 647.2 ± 100.05
    Negative emotionality13.7 ± 922.4 ± 90.001
    Constraint51.3 ± 1047.7 ± 8NS
    • MDQ, marijuana dependency questionnaire; NS, not significant.

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    Table 2.

    Statistical information for clusters showing significant changes for BPND in marijuana abusers and in healthy controls for the contrast placebo BPND > MP BPND, and for clusters showing significant differences for ΔBPND for the contrast marijuana abusers > controls (A > C)

    Brain regionMNI coordinates, mm Cluster size (k) # voxelsAbusers,
    t score
    Controls,
    t score
    A > C,
    t score
    xyz
    Placebo BPND > MP BPND
     Putamen30−6093011.714.4
     Ventral striatum1414−67.39.3
     Globus pallidum−24−4081810.212.3
     Ventral striatum−412−87.87.2
     Caudate−142046.65.9
    Abusers ΔBPND > Controls ΔBPND
     Left midbrain−12−14−101323.5NS3.1
     Right midbrain14−18−827NS−3.42.9
    • Statistical threshold for comparisons of placebo > MP: t score = 5 (PFWE < 0.05); statistical threshold for comparisons abusers > controls: t score = 2.4 (P < 0.01, uncorrected; 10 voxels).

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Decreased brain DA reactivity in marijuana abusers
Nora D. Volkow, Gene-Jack Wang, Frank Telang, Joanna S. Fowler, David Alexoff, Jean Logan, Millard Jayne, Christopher Wong, Dardo Tomasi
Proceedings of the National Academy of Sciences Jul 2014, 111 (30) E3149-E3156; DOI: 10.1073/pnas.1411228111

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Decreased brain DA reactivity in marijuana abusers
Nora D. Volkow, Gene-Jack Wang, Frank Telang, Joanna S. Fowler, David Alexoff, Jean Logan, Millard Jayne, Christopher Wong, Dardo Tomasi
Proceedings of the National Academy of Sciences Jul 2014, 111 (30) E3149-E3156; DOI: 10.1073/pnas.1411228111
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