65
Views
0
CrossRef citations to date
0
Altmetric
Original Article

Cocaine self-administration behavior is associated with subcortical and cortical morphometry measures in individuals with cocaine use disorder

ORCID Icon, , , , &
Received 20 Sep 2023, Accepted 10 Feb 2024, Published online: 29 Mar 2024

References

  • Mustaquim D, Jones CM, Compton WM. Trends and correlates of cocaine use among adults in the United States, 2006–2019. Addict Behav. 2021;120:106950. doi:10.1016/j.addbeh.2021.106950.
  • Farrell M, Martin NK, Stockings E, Bórquez A, Cepeda JA, Degenhardt L, Ali R, Tran LT, Rehm J, Torrens M, et al. Responding to global stimulant use: challenges and opportunities. Lancet. 2019;394:1652–67.
  • De Wit H. Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol. 2009;14:22–31. doi:10.1111/j.1369-1600.2008.00129.x.
  • Perry JL, Carroll ME. The role of impulsive behavior in drug abuse. Psychopharmacology. 2008;200:1–26. doi:10.1007/s00213-008-1173-0.
  • Crunelle CL, Kaag AM, Van Wingen G, van den Munkhof HE, Homberg JR, Reneman L, Van Den Brink, W. Reduced frontal brain volume in non-treatment-seeking cocaine-dependent individuals: exploring the role of impulsivity, depression, and smoking. Front Hum Neurosci. 2014;8:7.
  • Ersche KD, Barnes A, Jones PS, Morein-Zamir S, Robbins TW, Bullmore ET. Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence. Brain. 2011;134:2013–24. doi:10.1093/brain/awr138.
  • Kaag AM, Crunelle CL, van Wingen G, Homberg J, van den Brink W, Reneman L. Relationship between trait impulsivity and cortical volume, thickness and surface area in male cocaine users and non-drug using controls. Drug Alcohol Depen. 2014;144:210–7. doi:10.1016/j.drugalcdep.2014.09.016.
  • Mackey S, Paulus M. Are there volumetric brain differences associated with the use of cocaine and amphetamine-type stimulants? Neurosci Biobehav Rev. 2013;37:300–16. doi:10.1016/j.neubiorev.2012.12.003.
  • Meade CS, Bell RP, Towe SL, Hall SA. Cocaine-related alterations in fronto-parietal gray matter volume correlate with trait and behavioral impulsivity. Drug Alcohol Depen. 2020;206:107757. doi:10.1016/j.drugalcdep.2019.107757.
  • Yip SW, Worhunsky PD, Xu J, Morie KP, Constable RT, Malison RT, Carroll KM, Potenza MN. Gray-matter relationships to diagnostic and transdiagnostic features of drug and behavioral addictions. Addict Biol. 2018;23:394–402. doi:10.1111/adb.12492.
  • Moreno-López L, Catena A, Fernández-Serrano MJ, Delgado-Rico E, Stamatakis EA, Pérez-García M, Verdejo-García A. Trait impulsivity and prefrontal gray matter reductions in cocaine dependent individuals. Drug Alcohol Depen. 2012;125:208–14. doi:10.1016/j.drugalcdep.2012.02.012.
  • Jones JD, Comer SD. A review of human drug self-administration procedures. Behav Pharmacol. 2013;24:384. doi:10.1097/FBP.0b013e3283641c3d.
  • Jones JA, Belin-Rauscent A, Jupp B, Fouyssac M, Sawiak SJ, Zuhlsdorff K, Zhukovsky, P, Hebdon, L, Sanchez, CV, Robbins, TW, Everitt, BJ. Neurobehavioral precursors of compulsive cocaine-seeking in dual fronto-striatal circuits. Biol Psychiatry Glob Open Sci. 2023;4(1): 194–202. doi:10.1016/j.bpsgos.2023.06.001.
  • Cannella N, Cosa‐Linan A, Büchler E, Falfan‐Melgoza C, Weber‐Fahr W, Spanagel R. In vivo structural imaging in rats reveals neuroanatomical correlates of behavioral sub‐dimensions of cocaine addiction. Addict Biol. 2018;23:182–95. doi:10.1111/adb.12500.
  • Beveridge TJR, Gill KE, Hanlon CA, Porrino LJ. Parallel studies of cocaine-related neural and cognitive impairment in humans and monkeys. Phil Trans R Soc B. 2008;363:3257–66. doi:10.1098/rstb.2008.0102.
  • Jedema HP, Song X, Aizenstein HJ, Bonner AR, Stein EA, Yang Y, Bradberry CW. Long-term cocaine self-administration produces structural brain changes that correlate with altered cognition. Biol Psychiatry. 2021;89:376–85. doi:10.1016/j.biopsych.2020.08.008.
  • Chye Y, Mackey S, Gutman BA, Ching CRK, Batalla A, Blaine S, Brooks S, Caparelli EC, Cousijn J, Dagher A, et al. Subcortical surface morphometry in substance dependence: an ENIGMA addiction working group study. Addict Biol. 2020;25:e12830.
  • Jacobsen LK, Giedd JN, Gottschalk C, Kosten TR, Krystal JH. Quantitative morphology of the caudate and putamen in patients with cocaine dependence. Am J Psychiatry. 2001;158:486–9. doi:10.1176/appi.ajp.158.3.486.
  • Pando-Naude V, Toxto S, Fernandez-Lozano S, Parsons CE, Alcauter S, Garza-Villarreal EA. Gray and white matter morphology in substance use disorders: a neuroimaging systematic review and meta-analysis. Transl Psychiatry. 2021;11:1–18. doi:10.1038/s41398-020-01128-2.
  • Ersche KD, Jones PS, Williams GB, Turton AJ, Robbins TW, Bullmore ET. Abnormal brain structure implicated in stimulant drug addiction. Science. 2012;335:601–4. doi:10.1126/science.1214463.
  • Ersche KD, Jones PS, Williams GB, Smith DG, Bullmore ET, Robbins TW. Distinctive personality traits and neural correlates associated with stimulant drug use versus familial risk of stimulant dependence. Biol Psychiatry. 2013;74:137–44. doi:10.1016/j.biopsych.2012.11.016.
  • Hirsiger S, Hänggi J, Germann J, Vonmoos M, Preller KH, Engeli EJE, Kirschner M, Reinhard C, Hulka LM, Baumgartner MR, et al. Longitudinal changes in cocaine intake and cognition are linked to cortical thickness adaptations in cocaine users. Neuroimage Clin. 2019;21:101652.
  • Makris N, Gasic GP, Kennedy DN, Hodge SM, Kaiser JR, Lee MJ, Kim BW, Blood AJ, Evins AE, Seidman LJ, et al. Cortical thickness abnormalities in cocaine addiction—a reflection of both drug use and a pre-existing disposition to drug abuse? Neuron. 2008;60:174–88.
  • Roberts CA, Lorenzetti V, Albein-Urios N, Kowalczyk MA, Martinez-Gonzalez JM, Verdejo-Garcia A. Do comorbid personality disorders in cocaine dependence exacerbate neuroanatomical alterations? A structural neuroimaging study. Prog Neuro-Psychopharmacol Biol Psychiatry. 2021;110:110298. doi:10.1016/j.pnpbp.2021.110298.
  • Regnier SD, Lile JA, Rush CR, Stoops WW. Clinical neuropharmacology of cocaine reinforcement: a narrative review of human laboratory self‐administration studies. J Exp Anal Behav. 2022;117:420–41. doi:10.1002/jeab.744.
  • Bartzokis G, Beckson, M, Lu, PH, Edwards, N, Rapoport, R, Wiseman, E, Bridge, P. Increased CSF volumes are associated with diminished subjective responses to cocaine infusion. Neuropsychopharmacology. 2000;23:468–73. doi:10.1016/S0893-133X(00)00122-6.
  • Bartzokis G, Beckson M, Lu PH, Edwards N, Rapoport R, Bridge P, Mintz J. Cortical gray matter volumes are associated with subjective responses to cocaine infusion. Am J Addict. 2004;13:64–73. doi:10.1080/10550490490265352.
  • Veeneman MM, Broekhoven MH, Damsteegt R, Vanderschuren LJ. Distinct contributions of dopamine in the dorsolateral striatum and nucleus accumbens shell to the reinforcing properties of cocaine. Neuropsychopharmacology. 2012;37:487–98. doi:10.1038/npp.2011.209.
  • McGregor A, Roberts DC. Dopaminergic antagonism within the nucleus accumbens or the amygdala produces differential effects on intravenous cocaine self-administration under fixed and progressive ratio schedules of reinforcement. Brain Res. 1993;624:245–52. doi:10.1016/0006-8993(93)90084-Z.
  • Schmeichel BE, Herman MA, Roberto M, Koob GF. Hypocretin neurotransmission within the central amygdala mediates escalated cocaine self-administration and stress-induced reinstatement in rats. Biol Psychiatry. 2017;81:606–15. doi:10.1016/j.biopsych.2016.06.010.
  • See RE, Fuchs RA, Ledford CC, McLaughlin J. Drug addiction, relapse, and the amygdala. Ann NY Acad Sci. 2003;985:294–307. doi:10.1111/j.1749-6632.2003.tb07089.x.
  • Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F. Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci. 2011;108:15037–42. doi:10.1073/pnas.1010654108.
  • McBride WJ, Murphy JM, Ikemoto S. Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies. Behav Brain Res. 1999;101:129–52. doi:10.1016/S0166-4328(99)00022-4.
  • Recinto P, Samant ARH, Chavez G, Kim A, Yuan CJ, Soleiman M, Grant Y, Edwards S, Wee S, Koob GF, et al. Levels of neural progenitors in the hippocampus predict memory impairment and relapse to drug seeking as a function of excessive methamphetamine self-administration. Neuropsychopharmacology. 2012;37:1275–87. doi:10.1038/npp.2011.315.
  • Xu J, Kober H, Wang X, DeVito EE, Carroll KM, Potenza MN. Hippocampal volume mediates the relationship between measures of pre-treatment cocaine use and within-treatment cocaine abstinence. Drug Alcohol Depen. 2014;143:74–80. doi:10.1016/j.drugalcdep.2014.07.007.
  • Porrino LJ, Daunais JB, Smith HR, Nader MA. The expanding effects of cocaine: studies in a nonhuman primate model of cocaine self-administration. Neurosci Biobehav Rev. 2004;27:813–20. doi:10.1016/j.neubiorev.2003.11.013.
  • Jasinska AJ, Chen BT, Bonci A, Stein EA. Dorsal medial prefrontal cortex (MPFC) circuitry in rodent models of cocaine use: implications for drug addiction therapies. Addict Biol. 2015;20:215–26. doi:10.1111/adb.12132.
  • Schoenbaum G, Roesch MR, Stalnaker TA. Orbitofrontal cortex, decision-making and drug addiction. Trends Neurosci. 2006;29:116–24. doi:10.1016/j.tins.2005.12.006.
  • Liu X, Matochik JA, Cadet JL, London ED. Smaller volume of prefrontal lobe in polysubstance abusers: a magnetic resonance imaging study. Neuropsychopharmacology. 1998;18:243–52. doi:10.1016/S0893-133X(97)00143-7.
  • Droutman V, Read SJ, Bechara A. Revisiting the role of the insula in addiction. Trends Cogn Sci. 2015;19:414–20. doi:10.1016/j.tics.2015.05.005.
  • Martinez D, Urban N, Grassetti A, Chang D, Hu M-C, Zangen A, Levin FR, Foltin R, Nunes EV. Transcranial magnetic stimulation of medial prefrontal and cingulate cortices reduces cocaine self-administration: a pilot study. Front Psychiatry. 2018;9:80. doi:10.3389/fpsyt.2018.00080.
  • Risinger RC, Salmeron BJ, Ross TJ, Amen SL, Sanfilipo M, Hoffmann RG, Bloom AS, Garavan H, Stein EA. Neural correlates of high and craving during cocaine self-administration using BOLD fMRI. Neuroimage. 2005;26:1097–108. doi:10.1016/j.neuroimage.2005.03.030.
  • Casey BJ, Jones RM. Neurobiology of the adolescent brain and behavior: implications for substance use disorders. J Am Acad Child Psy. 2010;49:1189–201. doi:10.1016/j.jaac.2010.08.017.
  • Parvaz MA, Moeller SJ, d’Oleire Uquillas F, Pflumm A, Maloney T, Alia‐Klein N, Goldstein RZ. Prefrontal gray matter volume recovery in treatment‐seeking cocaine‐addicted individuals: a longitudinal study. Addict Biol. 2017;22:1391–401. doi:10.1111/adb.12403.
  • Angarita GA, Matuskey D, Pittman B, Costeines JL, Potenza MN, Jastreboff AM, Schmidt HD, Malison RT. Testing the effects of the GLP-1 receptor agonist exenatide on cocaine self-administration and subjective responses in humans with cocaine use disorder. Drug Alcohol Depen. 2021;221:108614. doi:10.1016/j.drugalcdep.2021.108614.
  • Matuskey D, Bhagwagar Z, Planeta B, Pittman B, Gallezot J-D, Chen J, Wanyiri J, Najafzadeh S, Ropchan J, Geha P, et al. Reductions in brain 5-HT1B receptor availability in primarily cocaine-dependent humans. Biol Psychiatry. 2014;76:816–22.
  • Matuskey D, Pittman B, Chen J, Wanyiri J, Nadim H, Jatlow P, Gueorguieva R, Potenza MN, Morgan PT, Bhagwagar Z, et al. A single-day paradigm of self-regulated human cocaine administration. Pharmacol Biochem Behav. 2012;103:95–101.
  • First MB, Spitzer RL, Gibbon M, Williams JB. Structured clinical interview for DSM-IV axis I disorders-patient ed. New York: New York State Psychiatric Institute; 1995.
  • First MB, Williams JB, Karg RS, Spitzer RL. Structured clinical interview for DSM-5 disorders, clinician version (SCID-5-CV). Arlington, VA: American Psychiatric Association; 2016.
  • Haney M. Self‐administration of cocaine, cannabis and heroin in the human laboratory: benefits and pitfalls. Addict Biol. 2009;14:9–21. doi:10.1111/j.1369-1600.2008.00121.x.
  • Gasser P, Holstein D, Michel Y, Doblin R, Yazar-Klosinski B, Passie T, Brenneisen R. Safety and efficacy of lysergic acid diethylamide-assisted psychotherapy for anxiety associated with life-threatening diseases. J Nerv Ment Dis. 2014;202:513–20. doi:10.1097/NMD.0000000000000113.
  • Destrieux C, Fischl B, Dale A, Halgren E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage. 2010;53:1–15. doi:10.1016/j.neuroimage.2010.06.010.
  • Hutton C, Draganski B, Ashburner J, Weiskopf N. A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. Neuroimage. 2009;48:371–80. doi:10.1016/j.neuroimage.2009.06.043.
  • Schwarz CG, Gunter JL, Wiste HJ, Przybelski SA, Weigand SD, Ward CP, Senjem ML, Vemuri P, Murray ME, Dickson DW, et al. A large-scale comparison of cortical thickness and volume methods for measuring Alzheimer’s disease severity. Neuroimage Clin. 2016;11:802–12.
  • Jan RK, Lin JC, Miles SW, Kydd RR, Russell BR. Striatal volume increases in active methamphetamine-dependent individuals and correlation with cognitive performance. Brain Sci. 2012;2:553–72. doi:10.3390/brainsci2040553.
  • Ide JS, Zhang S, Hu S, Sinha R, Mazure CM, Chiang-Shan RL. Cerebral gray matter volumes and low-frequency fluctuation of BOLD signals in cocaine dependence: duration of use and gender difference. Drug Alcohol Depen. 2014;134:51–62. doi:10.1016/j.drugalcdep.2013.09.004.
  • Pizzagalli DA, Holmes AJ, Dillon DG, Goetz EL, Birk JL, Bogdan R, Dougherty DD, Iosifescu DV, Rauch SL, Fava M, et al. Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am J Psychiatry. 2009;166:702–10.
  • Tschernegg M, Pletzer B, Schwartenbeck P, Ludersdorfer P, Hoffmann U, Kronbichler M. Impulsivity relates to striatal gray matter volumes in humans: evidence from a delay discounting paradigm. Front Hum Neurosci. 2015;9:384. doi:10.3389/fnhum.2015.00384.
  • Whiteside SP, Lynam DR. The five factor model and impulsivity: using a structural model of personality to understand impulsivity. Pers Indiv Differ. 2001;30:669–89. doi:10.1016/S0191-8869(00)00064-7.
  • Singer T, Critchley HD, Preuschoff K. A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci. 2009;13:334–40. doi:10.1016/j.tics.2009.05.001.
  • Ranaldi R, Roberts D. Initiation, maintenance and extinction of cocaine self-administration with and without conditioned reward. Psychopharmacology. 1996;128:89–96. doi:10.1007/s002130050114.
  • Regner MF, Tregellas J, Kluger B, Wylie K, Gowin JL, Tanabe J. The insula in nicotine use disorder: functional neuroimaging and implications for neuromodulation. Neurosci Biobehav Rev. 2019;103:414–24. doi:10.1016/j.neubiorev.2019.06.002.
  • Siegel S. Drug tolerance, drug addiction, and drug anticipation. Curr Dir Psychol Sci. 2005;14:296–300. doi:10.1111/j.0963-7214.2005.00384.x.
  • Naqvi NH, Rudrauf D, Damasio H, Bechara A. Damage to the insula disrupts addiction to cigarette smoking. Science. 2007;315:531–4. doi:10.1126/science.1135926.
  • Abdolahi A, Williams GC, Benesch CG, Wang HZ, Spitzer EM, Scott BE, Block RC, van Wijngaarden E. Damage to the insula leads to decreased nicotine withdrawal during abstinence. Addiction. 2015;110:1994–2003. doi:10.1111/add.13061.
  • Naqvi NH, Bechara A. The hidden island of addiction: the insula. Trends Neurosci. 2009;32:56–67. doi:10.1016/j.tins.2008.09.009.
  • Pintzka CW, Hansen TI, Evensmoen HR, Håberg AK. Marked effects of intracranial volume correction methods on sex differences in neuroanatomical structures: a HUNT MRI study. Front Neurosci. 2015;9:238. doi:10.3389/fnins.2015.00238.
  • Sanchis-Segura C, Ibañez-Gual MV, Aguirre N, Cruz-Gómez ÁJ, Forn C. Effects of different intracranial volume correction methods on univariate sex differences in grey matter volume and multivariate sex prediction. Sci Rep. 2020;10:12953. doi:10.1038/s41598-020-69361-9.
  • Abdel Malek GS, Goudriaan AE, Kaag AM. The relationship between craving and insular morphometry in regular cocaine users: does sex matter? Addict Biol. 2022;27:e13157. doi:10.1111/adb.13157.
  • Pandey S, Elliott W. Suppressor variables in social work research: ways to identify in multiple regression models. J Soc Social Work Res. 2010;1:28–40. doi:10.5243/jsswr.2010.2.
  • Watson D, Clark LA, Chmielewski M, Kotov R. The value of suppressor effects in explicating the construct validity of symptom measures. Psychol Assess. 2013;25:929. doi:10.1037/a0032781.
  • Lichenstein SD, Roos C, Kohler R, Kiluk B, Carroll KM, Worhunsky PD, Witkiewitz K, Yip SW. Identification and validation of distinct latent neurodevelopmental profiles in the adolescent brain and cognitive development study. Biol Psychiatry. 2021;7:352–61. doi:10.1016/j.bpsc.2021.02.013.
  • Park HJ, Friston K. Structural and functional brain networks: from connections to cognition. Science. 2013;342:1238411. doi:10.1126/science.1238411.
  • Yip SW, Scheinost D, Potenza MN, Carroll KM. Connectome-based prediction of cocaine abstinence. Am J Psychiatry. 2019;176:156–64. doi:10.1176/appi.ajp.2018.17101147.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.