Resting-State Functional Connectivity of the Dorsal and Ventral Striatum, Impulsivity, and Severity of Use in Recently Abstinent Cocaine-Dependent Individuals

Overview

Journal Int J Neuropsychopharmacol

Publisher Oxford University Press

Specialty Psychiatry

Date 2023 Aug 14

PMID 37579016

Authors

Xue Dong

Simon Zhornitsky

Wuyi Wang

Thang M Le

Yu Chen

Shefali Chaudhary

Chiang-Shan R Li

Sheng Zhang

Affiliations

Soon will be listed here.

Abstract

Background: Previous studies have focused on both ventral striatum (VS) and dorsal striatum (DS) in characterizing dopaminergic deficits in addiction. Animal studies suggest VS and DS dysfunction each in association with impulsive and compulsive cocaine use during early and later stages of addiction. However, few human studies have aimed to distinguish the roles of VS and DS dysfunction in cocaine misuse.

Methods: We examined VS and DS resting-state functional connectivity (rsFC) of 122 recently abstinent cocaine-dependent individuals (CDs) and 122 healthy controls (HCs) in 2 separate cohorts. We followed published routines in imaging data analyses and evaluated the results at a corrected threshold with age, sex, years of drinking, and smoking accounted for.

Results: CDs relative to HCs showed higher VS rsFC with the left inferior frontal cortex (IFC), lower VS rsFC with the hippocampus, and higher DS rsFC with the left orbitofrontal cortex. Region-of-interest analyses confirmed the findings in the 2 cohorts examined separately. In CDs, VS-left IFC and VS-hippocampus connectivity was positively and negatively correlated with average monthly cocaine use in the prior year, respectively. In the second cohort where participants were assessed with the Barratt Impulsivity Scale (BIS-11), VS-left IFC and VS-hippocampus connectivity was also positively and negatively correlated with BIS-11 scores in CDs. In contrast, DS-orbitofrontal cortex connectivity did not relate significantly to cocaine use metrics or BIS-11 scores.

Conclusion: These findings associate VS rsFC with impulsivity and the severity of recent cocaine use. How DS connectivity partakes in cocaine misuse remains to be investigated.

Citing Articles

Polygenic risk for depression and resting-state functional connectivity of subgenual anterior cingulate cortex in young adults.

Chen Y, Li H, Luo X, Li G, Ide J, Li C J Psychiatry Neurosci. 2025; 50(1):E31-E44.

PMID: 39809531 PMC: 11737878. DOI: 10.1503/jpn.240087.

References

Porrino L, Lyons D, Smith H, Daunais J, Nader M . Cocaine self-administration produces a progressive involvement of limbic, association, and sensorimotor striatal domains. J Neurosci. 2004; 24(14):3554-62. PMC: 6729741. DOI: 10.1523/JNEUROSCI.5578-03.2004. View

Zhang J, Yao Y, Li C, Zang Y, Shen Z, Liu L . Altered resting-state functional connectivity of the insula in young adults with Internet gaming disorder. Addict Biol. 2015; 21(3):743-51. PMC: 4615265. DOI: 10.1111/adb.12247. View

Berry K, Mielke Jr P . A Monte Carlo investigation of the Fisher Z transformation for normal and nonnormal distributions. Psychol Rep. 2001; 87(3 Pt 2):1101-14. DOI: 10.2466/pr0.2000.87.3f.1101. View

Goldstein R, Volkow N . Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci. 2011; 12(11):652-69. PMC: 3462342. DOI: 10.1038/nrn3119. View

Tiffany S, Singleton E, HAERTZEN C, Henningfield J . The development of a cocaine craving questionnaire. Drug Alcohol Depend. 1993; 34(1):19-28. DOI: 10.1016/0376-8716(93)90042-o. View

Smyser C, Inder T, Shimony J, Hill J, Degnan A, Snyder A . Longitudinal analysis of neural network development in preterm infants. Cereb Cortex. 2010; 20(12):2852-62. PMC: 2978240. DOI: 10.1093/cercor/bhq035. View

Alexander G, DeLong M, Strick P . Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986; 9:357-81. DOI: 10.1146/annurev.ne.09.030186.002041. View

Risinger R, Salmeron B, Ross T, Amen S, Sanfilipo M, Hoffmann R . Neural correlates of high and craving during cocaine self-administration using BOLD fMRI. Neuroimage. 2005; 26(4):1097-108. DOI: 10.1016/j.neuroimage.2005.03.030. View

Sinha R, Lacadie C, Skudlarski P, Fulbright R, Rounsaville B, Kosten T . Neural activity associated with stress-induced cocaine craving: a functional magnetic resonance imaging study. Psychopharmacology (Berl). 2005; 183(2):171-80. DOI: 10.1007/s00213-005-0147-8. View

10.

Ding X, Lee S . Cocaine addiction related reproducible brain regions of abnormal default-mode network functional connectivity: a group ICA study with different model orders. Neurosci Lett. 2013; 548:110-4. DOI: 10.1016/j.neulet.2013.05.029. View

11.

McClure S, Laibson D, Loewenstein G, Cohen J . Separate neural systems value immediate and delayed monetary rewards. Science. 2004; 306(5695):503-7. DOI: 10.1126/science.1100907. View

12.

Behan B, Stone A, Garavan H . Right prefrontal and ventral striatum interactions underlying impulsive choice and impulsive responding. Hum Brain Mapp. 2014; 36(1):187-98. PMC: 6869022. DOI: 10.1002/hbm.22621. View

13.

Adinoff B, Gu H, Merrick C, McHugh M, Jeon-Slaughter H, Lu H . Basal Hippocampal Activity and Its Functional Connectivity Predicts Cocaine Relapse. Biol Psychiatry. 2015; 78(7):496-504. PMC: 5671769. DOI: 10.1016/j.biopsych.2014.12.027. View

14.

Luscher C, Robbins T, Everitt B . The transition to compulsion in addiction. Nat Rev Neurosci. 2020; 21(5):247-263. PMC: 7610550. DOI: 10.1038/s41583-020-0289-z. View

15.

Goto Y, Grace A . Dopamine-dependent interactions between limbic and prefrontal cortical plasticity in the nucleus accumbens: disruption by cocaine sensitization. Neuron. 2005; 47(2):255-66. DOI: 10.1016/j.neuron.2005.06.017. View

16.

Zhukovsky P, Morein-Zamir S, Ziauddeen H, Fernandez-Egea E, Meng C, Regenthal R . Prefrontal Cortex Activation and Stopping Performance Underlie the Beneficial Effects of Atomoxetine on Response Inhibition in Healthy Volunteers and Those With Cocaine Use Disorder. Biol Psychiatry Cogn Neurosci Neuroimaging. 2021; 7(11):1116-1126. DOI: 10.1016/j.bpsc.2021.08.010. View

17.

Fotros A, Casey K, Larcher K, Verhaeghe J, Cox S, Gravel P . Cocaine cue-induced dopamine release in amygdala and hippocampus: a high-resolution PET [¹⁸F]fallypride study in cocaine dependent participants. Neuropsychopharmacology. 2013; 38(9):1780-8. PMC: 3717549. DOI: 10.1038/npp.2013.77. View

18.

Gu H, Salmeron B, Ross T, Geng X, Zhan W, Stein E . Mesocorticolimbic circuits are impaired in chronic cocaine users as demonstrated by resting-state functional connectivity. Neuroimage. 2010; 53(2):593-601. PMC: 2930044. DOI: 10.1016/j.neuroimage.2010.06.066. View

19.

Walter M, Denier N, Gerber H, Schmid O, Lanz C, Brenneisen R . Orbitofrontal response to drug-related stimuli after heroin administration. Addict Biol. 2014; 20(3):570-9. DOI: 10.1111/adb.12145. View

20.

Smith K, Graybiel A . A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron. 2013; 79(2):361-74. PMC: 3951965. DOI: 10.1016/j.neuron.2013.05.038. View