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Cingulate cortical thickness in cocaine use disorder: mediation effect between early life stress and cocaine consumption
Published online by Cambridge University Press: 23 November 2022
Abstract
Objective:
The cingulate gyrus is implicated in the neurobiology of addiction, such as chronic cocaine consumption. Early life stress (ELS) is an important moderator of cocaine use disorder (CUD). Therefore, we investigated the effect of CUD on cingulate cortical thickness and tested whether a history of ELS could influence the effects of CUD.
Methods:
Participants aged 18–50 years (78 with CUD due to crack cocaine consumption and 53 healthy controls) underwent magnetic resonance imaging and the cingulate thickness (rostral anterior, caudal anterior, posterior, and isthmus regions) was analysed. The clinical assessment comprised the Childhood Trauma Questionnaire (CTQ) and the Addiction Severity Index. Group comparisons adjusting by sex, age, and education were performed. Mediation models were generated where lifetime cocaine use, CTQ score, and cortical thickness corresponded to the independent variable, intermediary variable, and outcome, respectively.
Results:
Group comparisons revealed significant differences in six out of eight cingulate cortices, showing lower thickness in the CUD group. Furthermore, years of regular cocaine use was the variable most associated with cingulate thickness. Negative correlations were found between CTQ scores and the isthmus cingulate (right hemisphere), as well as with the rostral anterior cingulate (left hemisphere). In the mediation analysis, we observed a significant negative direct effect of lifetime cocaine use on the isthmus cingulate and an indirect effect of cocaine use mediated by CTQ score.
Conclusion:
Our findings suggest that a history of ELS could aggravate the negative effects of chronic cocaine use on the cingulate gyrus, particularly in the right isthmus cingulate cortex
- Type
- Original Article
- Information
- Copyright
- © The Author(s), 2022. Published by Cambridge University Press on behalf of Scandinavian College of Neuropsychopharmacology
Footnotes
Thiago Wendt Viola and Rodrigo Grassi-Oliveira are senior authors with an equivalent contribution.
References
Andersen, SL and Teicher, MH (2009) Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neuroscience & Biobehavioral Reviews 33(4), 516–524.Google Scholar
Baker, LM, Williams, LM, Korgaonkar, MS, Cohen, RA, Heaps, JM and Paul, RH (2013) Impact of early vs. late childhood early life stress on brain morphometrics. Brain Imaging and Behavior 7(2), 196–203.Google Scholar
Bernstein, DP, Fink, L, Handelsman, L, Foote, J, Lovejoy, M, Wenzel, K, Sapareto, E and Ruggiero, J (1994) Initial reliability and validity of a new retrospective measure of child abuse and neglect. American Journal of Psychiatry 151(8), 1132–1136.Google ScholarPubMed
Bittencourt, AML, Bampi, VF, Sommer, RC, Schaker, V, Juruena, MFP, Soder, RB, Franco, AR, Sanvicente-Vieira, B, Grassi-Oliveira, R, Ferreira, PEMS (2021) Cortical thickness and subcortical volume abnormalities in male crack-cocaine users. Psychiatry Research: Neuroimaging 310, 111232.Google Scholar
Briggs, GG and Nebes, RD (1975) Patterns of hand preference in a student population. Cortex 11(3), 230–238.Google Scholar
Bubb, EJ, Metzler-Baddeley, C and Aggleton, JP (2018) The cingulum bundle: anatomy, function, and dysfunction. Neuroscience & Biobehavioral Reviews 92, 104–127.Google Scholar
Bush, G, L.U.U., P and Posner, MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4(6), 215–222.CrossRefGoogle ScholarPubMed
Calati, R, Maller, JJ, Meslin, C, Lopez-Castroman, J, Ritchie, K, Courtet, P and Artero, S (2018) Repatriation is associated with isthmus cingulate cortex reduction in community-dwelling elderly. The World Journal of Biological Psychiatry 19(6), 421–430.Google Scholar
Canterberry, M, Peltier, MR, Brady, KT and Hanlon, CA (2016) Attenuated neural response to emotional cues in cocaine-dependence: a preliminary analysis of gender differences. The American Journal of Drug and Alcohol Abuse 42(5), 577–586.Google Scholar
Childress, AR, Mozley, PD, Mcelgin, W, Fitzgerald, J, Reivich, M and O'brien, CP (1999) Limbic activation during cue-induced cocaine craving. American Journal of Psychiatry 156(1), 11–18.Google Scholar
Connolly, CG, Bell, RP, Foxe, JJ and Garavan, H (2013) Dissociated grey matter changes with prolonged addiction and extended abstinence in cocaine users. PLoS One 8(3), e59645.Google Scholar
Conti, CL and Nakamura-Palacios, EM (2014) Bilateral transcranial direct current stimulation over dorsolateral prefrontal cortex changes the drug-cued reactivity in the anterior cingulate cortex of crack-cocaine addicts. Brain Stimulation 7(1), 130–132.Google Scholar
Davis, KD, Taylor, KS, Hutchison, WD, Dostrovsky, JO, Mcandrews, MP, Richter, EO and Lozano, AM (2005) Human anterior cingulate cortex neurons encode cognitive and emotional demands. Journal of Neuroscience 25(37), 8402–8406.Google Scholar
De Bellis, MD, Morey, RA, Nooner, KB, Woolley, DP, Haswell, CC and Hooper, SR (2019) A pilot study of neurocognitive function and brain structures in adolescents with alcohol use disorders: does maltreatment history matter? Child Maltreat 24(4), 374–388.Google Scholar
Desikan, RS, Ségonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, Buckner, RL, Dale, AM, Maguire, RP, Hyman, BT, Albert, MS, Killiany, RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3), 968–980.Google Scholar
Ersche, KD, Jones, PS, Williams, GB, Turton, AJ, Robbins, TW and Bullmore, ET (2012) Abnormal brain structure implicated in stimulant drug addiction. Science 335(6068), 601–604.Google Scholar
Fischl, B and Dale, AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences U S A 97(20), 11050–11055.Google Scholar
Francke, ID, Viola, TW, Tractenberg, SG and Grassi-Oliveira, R (2013) Childhood neglect and increased withdrawal and depressive severity in crack cocaine users during early abstinence. Child Abuse & Neglect 37(10), 883–889.Google Scholar
Grassi-Oliveira, R, Stein, LM and Pezzi, JC (2006) [Translation and content validation of the Childhood Trauma Questionnaire into Portuguese language]. Revista de Saúde Pública 40(2), 249–255.Google Scholar
Hayes, AF and Preacher, KJ (2014) Statistical mediation analysis with a multicategorical independent variable. British Journal of Mathematical and Statistical Psychology 67(3), 451–470.Google Scholar
Irizar, P, Albein-Urios, N, Martínez-González, JM, Verdejo-Garcia, A and Lorenzetti, V (2020) Unpacking common and distinct neuroanatomical alterations in cocaine dependent versus pathological gambling. European Neuropsychopharmacology 33, 81–88.CrossRefGoogle ScholarPubMed
Kessler, F, Cacciola, J, Alterman, A, Faller, S, Souza-Formigoni, ML, Cruz, MS, Brasiliano, S and Pechansky, F (2012) Psychometric properties of the sixth version of the Addiction Severity Index (ASI-6) in Brazil. Revista Brasileira De Psiquiatria 34(1), 24–33.Google Scholar
Kilts, CD, Gross, RE, Ely, TD and Drexler, KP (2004) The neural correlates of cue-induced craving in cocaine-dependent women. American Journal of Psychiatry 161(2), 233–241.CrossRefGoogle ScholarPubMed
Kiluk, BD, Babuscio, TA, Nich, C and Carroll, KM (2013) Smokers versus snorters: do treatment outcomes differ according to route of cocaine administration? Experimental and Clinical Psychopharmacology 21(6), 490–498.Google Scholar
Li, Q, Yang, WC, Wang, YR, Huang, YF, Li, W, Zhu, J, Zhang, Y, Zhao, LY, Qin, W, Yuan, K, Von Deneen, KM, Wang, W, Tian, J (2013) Abnormal function of the posterior cingulate cortex in heroin addicted users during resting-state and drug-cue stimulation task. Chinese Medical Journal (England) 126(4), 734–739.Google Scholar
Lim, L and Khor, CC (2022) Examining the common and specific grey matter abnormalities in childhood maltreatment and peer victimisation. BJPsych Open 8(4), e132.Google Scholar
Mclellan, AT, Luborsky, L, Woody, GE and O'brien, CP (1980) An improved diagnostic evaluation instrument for substance abuse patients. The Addiction Severity Index. The Journal of Nervous and Mental Disease 168(1), 26–33.Google Scholar
Perrenoud, LO, Oikawa, KF, Williams, AV, Laranjeira, R, Fischer, B, Strang, J and Ribeiro, M (2021) Factors associated with crack-cocaine early initiation: a Brazilian multicenter study. BMC Public Health 21(1), 781.Google Scholar
Rainville, P, Duncan, GH, Price, DD, Carrier, B and Bushnell, MC (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277(5328), 968–971.Google Scholar
Reuter, M, Hd, Rosas and Fischl, B (2010) Highly accurate inverse consistent registration: a robust approach. Neuroimage 53(4), 1181–1196.Google Scholar
Ross, MC, Sartin-Tarm, AS, Letkiewicz, AM, Crombie, KM and Cisler, JM (2021) Distinct cortical thickness correlates of early life trauma exposure and posttraumatic stress disorder are shared among adolescent and adult females with interpersonal violence exposure. Neuropsychopharmacology 46(4), 741–749.CrossRefGoogle ScholarPubMed
Sled, JG, Zijdenbos, AP and Evans, AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging 17(1), 87–97.Google Scholar
Ségonne, F, Dale, AM, Busa, E, Glessner, M, Salat, D, Hahn, HK and Fischl, B (2004) A hybrid approach to the skull stripping problem in MRI. NeuroImage 22(3), 1060–1075.Google Scholar
Ségonne, F, Pacheco, J and Fischl, B (2007) Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Transactions on Medical Imaging 26(4), 518–529.Google Scholar
Teicher, MH and Samson, JA (2013) Childhood maltreatment and psychopathology: a case for ecophenotypic variants as clinically and neurobiologically distinct subtypes. American Journal of Psychiatry 170(10), 1114–1133.Google Scholar
Teicher, MH and Samson, JA (2016) Annual research review: enduring neurobiological effects of childhood abuse and neglect. Journal of Child Psychology and Psychiatry 57(3), 241–266.Google Scholar
Tondo, LP, Viola, TW, Fries, GR, Kluwe-Schiavon, B, Rothmann, LM, Cupertino, R, Ferreira, P, Franco, AR, Lane, SD, Stertz, L, Zhao, Z, Hu, R, Meyer, T, Schmitz, JM, Walss-Bass, C, Grassi-Oliveira, R (2021) White matter deficits in cocaine use disorder: convergent evidence from in vivo diffusion tensor imaging and ex vivo proteomic analysis. Translational Psychiatry 11(1), 252.Google Scholar
Tractenberg, SG, Viola, TW, Rosa, C, Donati, JM, Francke, ID, Pezzi, JC and Grassi-Oliveira, R (2012) Exposição a trauma e transtorno de estresse pós-traumático em usuárias de crack. Jornal Brasileiro de Psiquiatria 61(4), 206–213.Google Scholar
Volkow, ND and Fowler, JS (2000) Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cerebral Cortex 10(3), 318–325.Google Scholar
Volkow, ND, Koob, GF and Mclellan, AT (2016) Neurobiologic advances from the brain disease model of addiction. New England Journal of Medicine 374(4), 363–371.Google Scholar
Volkow, ND, Michaelides, M and Baler, R (2019) The neuroscience of drug reward and addiction. Physiological Reviews 99(4), 2115–2140.Google Scholar
Volkow, ND, Wang, GJ, Fowler, JS and Tomasi, D (2012) Addiction circuitry in the human brain. Annual Review of Pharmacology and Toxicology 52(1), 321–336.Google Scholar
Voon, P, Ti, L, Dong, H, Milloy, MJ, Wood, E, Kerr, T and Hayashi, K (2016) Risky and rushed public crack cocaine smoking: the potential for supervised inhalation facilities. BMC Public Health 16(1), 476.Google Scholar
Zhao, Y, Sallie, SN, Cui, H, Zeng, N, Du, J, Yuan, T, Li, D, De Ridder, D and Zhang, C (2021) Anterior cingulate cortex in addiction: new insights for neuromodulation. Neuromodulation 24(2), 187–196.Google Scholar