Effect of transcranial direct current stimulation on decision making and cognitive flexibility in gambling disorder Original Paper First Online: 26 October 2018 Abstract
Decision making and cognitive flexibility are two components of cognitive control that play a critical role in the emergence, persistence, and relapse of gambling disorder. Transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex (DLPFC) has been reported to enhance decision making and cognitive flexibility in healthy volunteers and individuals with addictive disorders. In this triple-blind randomized sham-controlled parallel study, we aimed to determine whether tDCS over DLPFC would modulate decision making and cognitive flexibility in individuals with gambling disorder. Twenty participants with gambling disorder were administered Iowa Gambling Task (IGT) and Wisconsin Card Sorting Test (WCST). Subsequently, participants were administered three every other day sessions of active right anodal /left cathodal tDCS (20 min, 2 mA) or sham stimulation over bilateral DLPFC. WCST and IGT were readministered following the last session. Baseline clinical severity, depression, impulsivity levels, and cognitive performance were similar between groups. TDCS over the DLPFC resulted in more advantageous decision making (
F 1,16 = 8.128, p = 0.01, ɳp 2 =0.33) and better cognitive flexibility ( F 1,16 =8.782, p = 0.009, ɳp 2 = 0.35), representing large effect sizes. The results suggest for the first time that tDCS enhanced decision making and cognitive flexibility in gambling disorder. Therefore, tDCS may be a promising neuromodulation-based therapeutic approach in gambling disorder. Trial registration: Clinicaltrials.gov NCT03477799. Keywords Addictive disorders Gambling disorder Transcranial direct current stimulation Decision making Executive functions Cognitive functions Abbreviations BART
Balloon analog risk task
Beck depression inventory
Barratt Impulsivity Scale-11
Dorsolateral prefrontal cortex
Diagnostic and statistical manual of mental disorders-5
Functional magnetic resonance imaging
Iowa gambling task
Pathological Gambling Severity Index
South oaks gambling screen
Transcranial direct current stimulation
Ventromedial prefrontal cortex
Wisconsin card sorting test
Ahmet Zihni Soyata and Serkan Aksu contributed equally to this work.
The authors would like to thank all the participants who have kindly taken part in this study. The authors gratefully acknowledge the assistance of Mustafa Çetinkaya for referring participants and Göktuğ Aşçı for the preparation of the equipment.
Compliance with ethical standards Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition (DSM-5)
Morton JB, Ezekiel F, Wilk HA (2011) Cognitive control: easy to identify but hard to define. Top Cogn Sci 3:212–216.
https://doi.org/10.1111/j.1756-8765.2011.01139.x CrossRef Google Scholar
Achab S, Karila L, Khazaal Y (2014) Pathological gambling: update on decision making and neuro-functional studies in clinical samples. Curr Pharm Des 20:4000–4011
CrossRef Google Scholar
Alvarez-Moya EM, Ochoa C, Jiménez-Murcia S et al (2011) Effect of executive functioning, decision-making and self-reported impulsivity on the treatment outcome of pathologic gambling. J Psychiatry Neurosci 36:165–175.
https://doi.org/10.1503/jpn.090095 CrossRef Google Scholar
Brevers D, Bechara A, Cleeremans A, Noël X (2013) Iowa Gambling Task (IGT): twenty years after – gambling disorder and IGT. Front Psychol 4:665.
https://doi.org/10.3389/fpsyg.2013.00665 CrossRef Google Scholar
Wiehler A, Peters J (2015) Reward-based decision making in pathological gambling: the roles of risk and delay. Neurosci Res 90:3–14.
https://doi.org/10.1016/j.neures.2014.09.008 CrossRef Google Scholar
Leppink EW, Redden SA, Chamberlain SR, Grant JE (2016) Cognitive flexibility correlates with gambling severity in young adults. J Psychiatr Res 81:9–15.
https://doi.org/10.1016/j.jpsychires.2016.06.010 CrossRef Google Scholar
Coutlee CG, Huettel SA (2012) The functional neuroanatomy of decision making: Prefrontal control of thought and action. Brain Res 1428:3–12.
https://doi.org/10.1016/j.brainres.2011.05.053 CrossRef Google Scholar
Lee D (2013) Decision making: from neuroscience to psychiatry. Neuron 78:233–248.
https://doi.org/10.1016/j.neuron.2013.04.008 CrossRef Google Scholar
Malloy-Diniz LF, Miranda DM, Grassi-Oliveira R (2017) Editorial: executive functions in psychiatric disorders. Front Psychol 8:1461.
https://doi.org/10.3389/fpsyg.2017.01461 CrossRef Google Scholar
Martin CS, Langenbucher JW, Chung T, Sher KJ (2014) Truth or consequences in the diagnosis of substance use disorders. Addiction 109:1773–1778.
https://doi.org/10.1111/add.12615 CrossRef Google Scholar
Engel A, Caceda R (2015) Can decision making research provide a better understanding of chemical and behavioral addictions? Curr Drug Abuse Rev 8:75–85.
https://doi.org/10.2174/1874473708666150916113131 CrossRef Google Scholar
Amlung M, Vedelago L, Acker J et al (2017) Steep delay discounting and addictive behavior: a meta-analysis of continuous associations. Addiction 112:51–62.
https://doi.org/10.1111/add.13535 CrossRef Google Scholar
Fecteau S, Fregni F, Boggio PS et al (2010) Neuromodulation of decision-making in the addictive brain. Subst Use Misuse 45:1766–1786.
https://doi.org/10.3109/10826084.2010.482434 CrossRef Google Scholar
Bickel WK, Jarmolowicz DP, Mueller ET et al (2012) Are executive function and impulsivity antipodes? A conceptual reconstruction with special reference to addiction. Psychopharmacology 221:361–387.
https://doi.org/10.1007/s00213-012-2689-x CrossRef Google Scholar
Probst C, Manthey J, Martinez A, Rehm J (2015) Alcohol use disorder severity and reported reasons not to seek treatment: a cross-sectional study in European primary care practices. Subst Abuse Treat Prev Policy 10:32.
https://doi.org/10.1186/s13011-015-0028-z CrossRef Google Scholar
Maremmani AGI, Rovai L, Rugani F et al (2012) Correlations between awareness of illness (insight) and history of addiction in heroin-addicted patients. Front Psychiatry 3:61.
https://doi.org/10.3389/fpsyt.2012.00061 CrossRef Google Scholar
Fauth-Bühler M, Mann K, Potenza MN (2017) Pathological gambling: a review of the neurobiological evidence relevant for its classification as an addictive disorder. Addict Biol 22:885–897.
https://doi.org/10.1111/adb.12378 CrossRef Google Scholar
Potenza MN (2014) The neural bases of cognitive processes in gambling disorder. Trends Cogn Sci 18:429–438.
https://doi.org/10.1016/j.tics.2014.03.007 CrossRef Google Scholar
Kapsomenakis A, Simos PG, Konstantakopoulos G, Kasselimis DS (2018) In search of executive impairment in pathological gambling: a neuropsychological study on non-treatment seeking gamblers. J Gambl Stud.
https://doi.org/10.1007/s10899-018-9758-y Google Scholar
Ledgerwood DM, Orr ES, Kaploun KA et al (2012) Executive function in pathological gamblers and healthy controls. J Gambl Stud 28:89–103.
https://doi.org/10.1007/s10899-010-9237-6 CrossRef Google Scholar
Kovács I, Richman MJ, Janka Z et al (2017) Decision making measured by the Iowa Gambling Task in alcohol use disorder and gambling disorder: a systematic review and meta-analysis. Drug Alcohol Depend 181:152–161.
https://doi.org/10.1016/j.drugalcdep.2017.09.023 CrossRef Google Scholar
Clark L, Averbeck B, Payer D et al (2013) Pathological choice: the neuroscience of gambling and gambling addiction. J Neurosci 33:17617–17623.
https://doi.org/10.1523/JNEUROSCI.3231-13.2013 CrossRef Google Scholar
Brevers D, Cleeremans A, Goudriaan AE et al (2012) Decision making under ambiguity but not under risk is related to problem gambling severity. Psychiatry Res 200:568–574.
https://doi.org/10.1016/j.psychres.2012.03.053 CrossRef Google Scholar
Li X, Lu Z-L, D’Argembeau A et al (2010) The iowa gambling task in fMRI images. Hum Brain Mapp 31:410–423.
https://doi.org/10.1002/hbm.20875 Google Scholar
Fleck MS, Daselaar SM, Dobbins IG, Cabeza R (2006) Role of prefrontal and anterior cingulate regions in decision-making processes shared by memory and nonmemory tasks. Cereb Cortex 16:1623–1630.
https://doi.org/10.1093/cercor/bhj097 CrossRef Google Scholar
Brevers D, Noël X, He Q et al (2016) Increased ventral-striatal activity during monetary decision making is a marker of problem poker gambling severity. Addict Biol 21:688–699.
https://doi.org/10.1111/adb.12239 CrossRef Google Scholar
Jurado MB, Rosselli M (2007) The elusive nature of executive functions: a review of our current understanding. Neuropsychol Rev 17:213–233.
https://doi.org/10.1007/s11065-007-9040-z CrossRef Google Scholar
Domínguez-Salas S, Díaz-Batanero C, Lozano-Rojas OM, Verdejo-García A (2016) Impact of general cognition and executive function deficits on addiction treatment outcomes: Systematic review and discussion of neurocognitive pathways. Neurosci Biobehav Rev 71:772–801.
https://doi.org/10.1016/j.neubiorev.2016.09.030 CrossRef Google Scholar
Goudriaan AE, Oosterlaan J, de Beurs E, van den Brink W (2006) Neurocognitive functions in pathological gambling: a comparison with alcohol dependence, Tourette syndrome and normal controls. Addiction 101:534–547.
https://doi.org/10.1111/j.1360-0443.2006.01380.x CrossRef Google Scholar
Ochoa C, Alvarez-Moya EM, Penelo E et al (2013) Decision-making deficits in pathological gambling: the role of executive functions, explicit knowledge and impulsivity in relation to decisions made under ambiguity and risk. Am J Addict 22:492–499.
https://doi.org/10.1111/j.1521-0391.2013.12061.x CrossRef Google Scholar
Brand M, Recknor EC, Grabenhorst F, Bechara A (2007) Decisions under ambiguity and decisions under risk: correlations with executive functions and comparisons of two different gambling tasks with implicit and explicit rules. J Clin Exp Neuropsychol 29:86–99.
https://doi.org/10.1080/13803390500507196 CrossRef Google Scholar
Iudicello JE, Woods SP, Cattie JE et al (2013) Risky decision-making in HIV-associated neurocognitive disorders (HAND). Clin Neuropsychol 27:256–275.
https://doi.org/10.1080/13854046.2012.740077 CrossRef Google Scholar
Dong X, Du X, Qi B (2016) Conceptual knowledge influences decision making differently in individuals with high or low cognitive flexibility: an ERP study. PLoS One 11:e0158875.
https://doi.org/10.1371/journal.pone.0158875 CrossRef Google Scholar
Buchsbaum BR, Greer S, Chang W-L, Berman KF (2005) Meta-analysis of neuroimaging studies of the Wisconsin card-sorting task and component processes. Hum Brain Mapp 25:35–45.
https://doi.org/10.1002/hbm.20128 CrossRef Google Scholar
Alvarez JA, Emory E (2006) Executive function and the frontal lobes: a meta-analytic review. Neuropsychol Rev 16:17–42.
https://doi.org/10.1007/s11065-006-9002-x CrossRef Google Scholar
Moccia L, Pettorruso M, De Crescenzo F et al (2017) Neural correlates of cognitive control in gambling disorder: a systematic review of fMRI studies. Neurosci Biobehav Rev 78:104–116.
https://doi.org/10.1016/j.neubiorev.2017.04.025 CrossRef Google Scholar
Nitsche MA, Cohen LG, Wassermann EM et al (2008) Transcranial direct current stimulation: State of the art 2008. Brain Stimul 1:206–223.
https://doi.org/10.1016/j.brs.2008.06.004 CrossRef Google Scholar
Fecteau S, Knoch D, Fregni F et al (2007) Diminishing risk-taking behavior by modulating activity in the prefrontal cortex: a direct current stimulation study. J Neurosci 27:12500–12505.
https://doi.org/10.1523/JNEUROSCI.3283-07.2007 CrossRef Google Scholar
Fecteau S, Pascual-Leone A, Zald DH et al (2007) Activation of prefrontal cortex by transcranial direct current stimulation reduces appetite for risk during ambiguous decision making. J Neurosci 27:6212–6218.
https://doi.org/10.1523/JNEUROSCI.0314-07.2007 CrossRef Google Scholar
Cheng GLF, Lee TMC (2016) Altering risky decision-making: Influence of impulsivity on the neuromodulation of prefrontal cortex. Soc Neurosci 11:353–364.
https://doi.org/10.1080/17470919.2015.1085895 CrossRef Google Scholar
Gilmore CS, Dickmann PJ, Nelson BG et al (2018) Transcranial Direct Current Stimulation (tDCS) paired with a decision-making task reduces risk-taking in a clinically impulsive sample. Brain Stimul 11:302–309.
https://doi.org/10.1016/j.brs.2017.11.011 CrossRef Google Scholar
Gorini A, Lucchiari C, Russell-Edu W, Pravettoni G (2014) Modulation of risky choices in recently abstinent dependent cocaine users: a transcranial direct-current stimulation study. Front Hum Neurosci 8:661.
https://doi.org/10.3389/fnhum.2014.00661 CrossRef Google Scholar
Boggio PS, Campanhã C, Valasek CA et al (2010) Modulation of decision-making in a gambling task in older adults with transcranial direct current stimulation. Eur J Neurosci 31:593–597.
https://doi.org/10.1111/j.1460-9568.2010.07080.x CrossRef Google Scholar
Mansouri FA, Fehring DJ, Feizpour A et al (2016) Direct current stimulation of prefrontal cortex modulates error-induced behavioral adjustments. Eur J Neurosci 44:1856–1869.
https://doi.org/10.1111/ejn.13281 CrossRef Google Scholar
Luft CDB, Zioga I, Banissy MJ, Bhattacharya J (2017) Relaxing learned constraints through cathodal tDCS on the left dorsolateral prefrontal cortex. Sci Rep 7:2916.
https://doi.org/10.1038/s41598-017-03022-2 CrossRef Google Scholar
Zack M, Cho SS, Parlee J et al (2016) Effects of high frequency repeated transcranial magnetic stimulation and continuous theta burst stimulation on gambling reinforcement, delay discounting, and stroop interference in men with pathological gambling. Brain Stimul 9:867–875.
https://doi.org/10.1016/j.brs.2016.06.003 CrossRef Google Scholar
Gay A, Boutet C, Sigaud T et al (2017) A single session of repetitive transcranial magnetic stimulation of the prefrontal cortex reduces cue-induced craving in patients with gambling disorder. Eur Psychiatry 41:68–74.
https://doi.org/10.1016/j.eurpsy.2016.11.001 CrossRef Google Scholar
Sauvaget A, Bulteau S, Guilleux A et al (2018) Both active and sham low-frequency rTMS single sessions over the right DLPFC decrease cue-induced cravings among pathological gamblers seeking treatment: a randomized, double-blind, sham-controlled crossover trial. J Behav Addict 7:126–136.
https://doi.org/10.1556/2006.7.2018.14 CrossRef Google Scholar
Dickler M, Lenglos C, Renauld E et al (2018) Online effects of transcranial direct current stimulation on prefrontal metabolites in gambling disorder. Neuropharmacology 131:51–57.
https://doi.org/10.1016/j.neuropharm.2017.12.002 CrossRef Google Scholar
Lesieur HR, Blume SB (1987) The South Oaks Gambling Screen (SOGS): a new instrument for the identification of pathological gamblers. Am J Psychiatry 144:1184–1188.
https://doi.org/10.1176/ajp.144.9.1184 CrossRef Google Scholar
Ferris J, Consultants HW, Ladouceur R et al (2001) THE CANADIAN PROBLEM GAMBLING INDEX: FINAL REPORT The Canadian Problem Gambling Index: Final Report Submitted for the Canadian Centre on Substance Abuse (CCSA)
Beck AT, Ward CH, Mendelson M et al (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571
CrossRef Google Scholar
Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt impulsiveness scale. J Clin Psychol 51:768–774
CrossRef Google Scholar
Brunoni AR, Amadera J, Berbel B et al (2011) A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int J Neuropsychopharmacol 14:1133–1145.
https://doi.org/10.1017/S1461145710001690 CrossRef Google Scholar
Woods AJ, Antal A, Bikson M et al (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol 127:1031–1048
CrossRef Google Scholar
Gandiga PC, Hummel FC, Cohen LG (2006) Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol 117:845–850.
https://doi.org/10.1016/j.clinph.2005.12.003 CrossRef Google Scholar
Icellioglu S (2015) Iowa Kumar Testi: Normatif veriler ve yürütücü işlevlerle ilişkisi. Dusunen Adam J Psychiatry Neurol Sci 222–230.
Heaton SK, Chelune GJ, Talley JL, Kay GG, Curtiss G (1993) Wisconsin Card Sorting Test Manual: Revised and expanded. Odessa, Florida
Boggio PS, Zaghi S, Villani AB et al (2010) Modulation of risk-taking in marijuana users by transcranial direct current stimulation (tDCS) of the dorsolateral prefrontal cortex (DLPFC). Drug Alcohol Depend 112:220–225.
https://doi.org/10.1016/j.drugalcdep.2010.06.019 CrossRef Google Scholar
He Q, Chen M, Chen C et al (2016) Anodal stimulation of the left DLPFC increases IGT scores and decreases delay discounting rate in healthy males. Front Psychol 7:1421.
https://doi.org/10.3389/fpsyg.2016.01421 Google Scholar
Benussi A, Alberici A, Cantoni V et al (2017) Modulating risky decision-making in Parkinson’s disease by transcranial direct current stimulation. Eur J Neurol 24:751–754.
https://doi.org/10.1111/ene.13286 CrossRef Google Scholar
Ouerchefani R, Ouerchefani N, Allain P et al (2017) Contribution of different regions of the prefrontal cortex and lesion laterality to deficit of decision-making on the Iowa Gambling Task. Brain Cogn 111:73–85.
https://doi.org/10.1016/j.bandc.2016.06.010 CrossRef Google Scholar
Fellows LK, Farah MJ (2005) Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. Cereb Cortex 15:58–63.
https://doi.org/10.1093/cercor/bhh108 CrossRef Google Scholar
Baumgartner T, Knoch D, Hotz P et al (2011) Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14:1468–1474.
https://doi.org/10.1038/nn.2933 CrossRef Google Scholar
Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324:646–648.
https://doi.org/10.1126/science.1168450 CrossRef Google Scholar
Boog M, Höppener P, Wetering VD, et al (2014) Cognitive inflexibility in gamblers is primarily present in reward-related decision making. Front Hum Neurosci 8:569.
https://doi.org/10.3389/fnhum.2014.00569 CrossRef Google Scholar
Cavedini P, Riboldi G, Keller R et al (2002) Frontal lobe dysfunction in pathological gambling patients. Biol Psychiatry 51:334–341
CrossRef Google Scholar
Gleichgerrcht E, Ibáñez A, Roca M et al (2010) Decision-making cognition in neurodegenerative diseases. Nat Rev Neurol 6:611–623.
https://doi.org/10.1038/nrneurol.2010.148 CrossRef Google Scholar
Brand M, Labudda K, Markowitsch HJ (2006) Neuropsychological correlates of decision-making in ambiguous and risky situations. Neural Netw 19:1266–1276.
https://doi.org/10.1016/j.neunet.2006.03.001 CrossRef Google Scholar
Toplak ME, Sorge GB, Benoit A et al (2010) Decision-making and cognitive abilities: a review of associations between Iowa Gambling Task performance, executive functions, and intelligence. Clin Psychol Rev 30:562–581.
https://doi.org/10.1016/j.cpr.2010.04.002 CrossRef Google Scholar
Overman WH, Frassrand K, Ansel S et al (2004) Performance on the IOWA card task by adolescents and adults. Neuropsychologia 42:1838–1851.
https://doi.org/10.1016/j.neuropsychologia.2004.03.014 CrossRef Google Scholar
Nakamura-Palacios EM, Lopes IBC, Souza RA et al (2016) Ventral medial prefrontal cortex (vmPFC) as a target of the dorsolateral prefrontal modulation by transcranial direct current stimulation (tDCS) in drug addiction. J Neural Transm 123:1179–1194.
https://doi.org/10.1007/s00702-016-1559-9 CrossRef Google Scholar
Ouellet J, McGirr A, Van den Eynde F et al (2015) Enhancing decision-making and cognitive impulse control with transcranial direct current stimulation (tDCS) applied over the orbitofrontal cortex (OFC): A randomized and sham-controlled exploratory study. J Psychiatr Res 69:27–34.
https://doi.org/10.1016/j.jpsychires.2015.07.018 CrossRef Google Scholar
The Lancet (2017) Problem gambling is a public health concern. Lancet 390:913.
https://doi.org/10.1016/S0140-6736(17)32333-4 CrossRef Google Scholar
Choi S-W, Shin Y-C, Kim D-J et al (2017) Treatment modalities for patients with gambling disorder. Ann Gen Psychiatry 16:23.
https://doi.org/10.1186/s12991-017-0146-2 CrossRef Google Scholar
Ronzitti S, Soldini E, Smith N et al (2018) Are Treatment Outcomes Determined by Type of Gambling? A UK Study. J Gambl Stud, In Press.
Pfund RA, Peter SC, Whelan JP, Meyers AW (2017) When Does Premature Treatment Termination Occur? Examining Session-by-Session Dropout Among Clients with Gambling Disorder. J Gambl Stud 34:617–630.
https://doi.org/10.1007/s10899-017-9733-z CrossRef Google Scholar
Challet-Bouju G, Bruneau M, Group IGNACE C, et al (2017) Cognitive Remediation Interventions for Gambling Disorder: A Systematic Review. Front Psychol 8:1961.
https://doi.org/10.3389/fpsyg.2017.01961 CrossRef Google Scholar
Perkins FN, Freeman KB (2018) Pharmacotherapies for decreasing maladaptive choice in drug addiction: targeting the behavior and the drug. Pharmacol Biochem Behav 164:40–49.
https://doi.org/10.1016/j.pbb.2017.06.015 CrossRef Google Scholar
Bickel WK, Quisenberry AJ, Moody L, Wilson AG (2015) Therapeutic opportunities for self-control repair in addiction and related disorders: change and the limits of change in trans-disease processes. Clin Psychol Sci 3:140–153.
https://doi.org/10.1177/2167702614541260 CrossRef Google Scholar
Verdejo-Garcia A (2016) Cognitive training for substance use disorders: Neuroscientific mechanisms. Neurosci Biobehav Rev 68:270–281.
https://doi.org/10.1016/j.neubiorev.2016.05.018 CrossRef Google Scholar
Leblond J, Ladouceur R, Blaszczynski A (2003) Which pathological gamblers will complete treatment? Br J Clin Psychol 42:205–209.
https://doi.org/10.1348/014466503321903607 CrossRef Google Scholar
van den Bos R, Homberg J, de Visser L (2013) A critical review of sex differences in decision-making tasks: focus on the Iowa Gambling Task. Behav Brain Res 238:95–108.
https://doi.org/10.1016/j.bbr.2012.10.002 CrossRef Google Scholar
Reber J, Tranel D (2017) Sex differences in the functional lateralization of emotion and decision making in the human brain. J Neurosci Res 95:270–278.
https://doi.org/10.1002/jnr.23829 CrossRef Google Scholar Copyright information
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