Neural and neurocognitive markers of vulnerability to gambling disorder: a study of unaffected siblings.
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
27
03
2019
accepted:
12
09
2019
revised:
26
08
2019
pubmed:
10
10
2019
medline:
29
12
2020
entrez:
10
10
2019
Statut:
ppublish
Résumé
Psychological and neurobiological markers in individuals with gambling disorder (GD) could reflect transdiagnostic vulnerability to addiction or neuroadaptive consequences of long-term gambling. Using an endophenotypic approach to identify vulnerability markers, we tested the biological relatives of cases with GD. Male participants seeking treatment for GD (n = 20) were compared with a male control group (n = 18). Biological siblings of cases with GD (n = 17, unrelated to the current GD group) were compared with a separate control group (n = 19) that overlapped partially with the GD control group. Participants completed a comprehensive assessment of clinical scales, neurocognitive functioning, and fMRI of unexpected financial reward. The GD group displayed elevated levels of self-report impulsivity and delay discounting, and increased risk-taking on the Cambridge Gamble Task. We did not observe impaired motor impulsivity on the stop-signal task. Siblings of GD showed some overlapping effects; namely, elevated impulsivity (negative urgency) and increased risk-taking on the Cambridge Gamble Task. We did not observe any differences in the neural response to win outcomes, either in the GD or sibling analysis compared with their control group. Within the GD group, activity in the thalamus and caudate correlated negatively with gambling severity. Increased impulsivity and risk-taking in GD are present in biological relatives of cases with GD, suggesting these markers may represent pre-existing vulnerability to GD.
Identifiants
pubmed: 31597159
doi: 10.1038/s41386-019-0534-1
pii: 10.1038/s41386-019-0534-1
pmc: PMC6901470
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
292-300Subventions
Organisme : Medical Research Council
ID : G1100554
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N00616X/1
Pays : United Kingdom
Références
Verdejo-García A, Lawrence AJ, Clark L. Impulsivity as a vulnerability marker for substance-use disorders: review of findings from high-risk research, problem gamblers and genetic association studies. Neurosci Biobehav Rev. 2008;32:777–810.
pubmed: 18295884
Bechara A. Risky business: emotion, decision-making, and addiction. J Gambl Stud. 2003;19:23–51.
pubmed: 12635539
Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature. 2004;427:311–2.
pubmed: 14737157
Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160:636–45.
pubmed: 12668349
Ersche KD, Turton AJ, Pradhan S, Bullmore ET, Robbins TW. Drug addiction endophenotypes: impulsive versus sensation-seeking personality traits. Biol Psychiatry. 2010;68:770–3.
pubmed: 20678754
pmcid: 3485555
Robbins TW, Gillan CM, Smith DG, de Wit S, Ersche KD. Neurocognitive endophenotypes of impulsivity and compulsivity: towards dimensional psychiatry. Trends Cogn Sci. 2012;16:81–91.
pubmed: 22155014
Black DW, Monahan PO, Temkit M’hamed, Shaw M. A family study of pathological gambling. Psychiatry Res. 2006;141:295–303.
pubmed: 16499975
Walters GD. Behavior genetic research on gambling and problem gambling: a preliminary meta-analysis of available data. J Gambl Stud. 2001;17:255–71.
pubmed: 11842524
Mann K, Lemenager T, Zois E, Hoffmann S, Nakovics H, Beutel M, et al. Comorbidity, family history and personality traits in pathological gamblers compared with healthy controls. Eur Psychiatry. 2017;42:120–8.
pubmed: 28364687
Hodgins DC, Schopflocher DP, el-Guebaly N, Casey DM, Smith GJ, Williams RJ, et al. The association between childhood maltreatment and gambling problems in a community sample of adult men and women. Psychol Addict Behav. 2010;24:548–54.
pubmed: 20853942
Slutske WS, Eisen S, True WR, Lyons MJ, Goldberg J, Tsuang M. Common genetic vulnerability for pathological gambling and alcohol dependence in men. Arch Gen Psychiatry. 2000;57:666–73.
pubmed: 10891037
Lobo DSS. Genetic aspects of gambling disorders: recent developments and future directions. Curr Neurol Neurosci Rep. 2016;3:58–66.
Kräplin A, Dshemuchadse M, Behrendt S, Scherbaum S, Goschke T, Bühringer G. Dysfunctional decision-making in pathological gambling: Pattern specificity and the role of impulsivity. Psychiatry Res. 2014;215:675–82.
pubmed: 24434041
Michalczuk R, Bowden-Jones H, Verdejo-Garcia A, Clark L. Impulsivity and cognitive distortions in pathological gamblers attending the UK National Problem Gambling Clinic: a preliminary report. Psychol Med. 2011;41:2625–35.
pubmed: 21733207
pmcid: 3206226
MacKillop J, Amlung MT, Few LR, Ray LA, Sweet LH, Munafò MR. Delayed reward discounting and addictive behavior: a meta-analysis. Psychopharmacol. 2011;216:305–21.
Chowdhury NS, Livesey EJ, Blaszczynski A, Harris JA. Pathological gambling and motor impulsivity: a systematic review with meta-analysis. J Gambl Stud. 2017;33:1213–39.
pubmed: 28255940
Kovács I, Richman MJ, Janka Z, Maraz A, Andó B. Decision making measured by the Iowa Gambling Task in alcohol use disorder and gambling disorder: a systematic review and meta-analysis. Drug Alcohol Depend. 2017;181:152–61.
pubmed: 29055269
Wilson MJ, Vassileva J. Decision-making under risk, but not under ambiguity, predicts pathological gambling in discrete types of abstinent substance users. Front Psychiatry. 2018;9:239.
pubmed: 29922190
pmcid: 5996080
Zois E, Kortlang N, Vollstädt-Klein S, Lemènager T, Beutel M, Mann K, et al. Decision-making deficits in patients diagnosed with disordered gambling using the Cambridge Gambling task: the effects of substance use disorder comorbidity. Brain Behav. 2014;4:484–94.
pubmed: 25161815
pmcid: 4107466
Lawrence AJ, Luty J, Bogdan NA, Sahakian BJ, Clark L. Problem gamblers share deficits in impulsive decision-making with alcohol-dependent individuals. Addiction. 2009;104:1006–15.
pubmed: 19466924
pmcid: 2773538
Grant JE, Chamberlain SR, Schreiber LRN, Odlaug BL, Kim SW. Selective decision-making deficits in at-risk gamblers. Psychiatry Res. 2011;189:115–20.
pubmed: 21715016
pmcid: 3401062
Kreek MJ, Nielsen DA, Butelman ER, LaForge KS. Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction. Nat Neurosci. 2005;8:1450–7.
pubmed: 16251987
Stevens L, Verdejo-García A, Goudriaan AE, Roeyers H, Dom G, Vanderplasschen W. Impulsivity as a vulnerability factor for poor addiction treatment outcomes: a review of neurocognitive findings among individuals with substance use disorders. J Subst Abus Treat. 2014;47:58–72.
Luijten M, Schellekens AF, Kühn S, Machielse MWJ, Sescousse G. Disruption of reward processing in addiction: an image-based meta-analysis of functional magnetic resonance imaging studies. JAMA Psychiatry. 2017;74:387–98.
pubmed: 28146248
Reuter J, Raedler T, Rose M, Hand I, Gläscher J, Büchel C. Pathological gambling is linked to reduced activation of the mesolimbic reward system. Nat Neurosci. 2005;8:147–8.
pubmed: 15643429
De Ruiter MB, Veltman DJ, Goudriaan AE, Oosterlaan J, Sjoerds Z, Van Den Brink W. Response perseveration and ventral prefrontal sensitivity to reward and punishment in male problem gamblers and smokers. Neuropsychopharmacology. 2009;34:1027–38.
pubmed: 18830241
Balodis IM, Kober H, Worhunsky PD, Stevens MC, Pearlson GD, Potenza MN. Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biol Psychiatry. 2012;71:749–57.
pubmed: 22336565
pmcid: 3460522
Romanczuk-Seiferth N, Koehler S, Dreesen C, Wüstenberg T, Heinz A. Pathological gambling and alcohol dependence: neural disturbances in reward and loss avoidance processing. Addict Biol. 2015;20:557–69.
pubmed: 24754423
Sescousse G, Janssen LK, Hashemi MM, Timmer MHM, Geurts DEM, Ter Huurne NP, et al. Amplified striatal responses to near-miss outcomes in pathological gamblers. Neuropsychopharmacology. 2016;41:2614–23.
pubmed: 27006113
pmcid: 4987843
Sescousse G, Barbalat G, Domenech P, Dreher J-C. Imbalance in the sensitivity to different types of rewards in pathological gambling. Brain. 2013;136:2527–38.
pubmed: 23757765
Miedl SF, Fehr T, Meyer G, Herrmann M. Neurobiological correlates of problem gambling in a quasi-realistic blackjack scenario as revealed by fMRI. Psychiatry Res. 2010;181:165–73.
pubmed: 20138482
Blum K, Gardner E, Oscar-Berman M, Gold M. ‘Liking’ and ‘wanting’ linked to Reward Deficiency Syndrome (RDS): hypothesizing differential responsivity in brain reward circuitry. Curr Pharm Des. 2012;18:113–8.
pubmed: 22236117
pmcid: 3651846
Gold MS, Badgaiyan RD, Blum K. A shared molecular and genetic basis for food and drug addiction: overcoming hypodopaminergic trait/state by incorporating dopamine agonistic therapy in psychiatry. Psychiatr Clin North Am. 2015;38:419–62.
pubmed: 26300032
Robinson TE, Berridge KC. Review. The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci. 2008;363:3137–46.
pubmed: 18640920
pmcid: 2607325
Robinson TE, Berridge KC. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev. 1993;18:247–91.
pubmed: 8401595
Limbrick-Oldfield EH, van Holst RJ, Clark L. Fronto-striatal dysregulation in drug addiction and pathological gambling: consistent inconsistencies? NeuroImage: Clin. 2013;2:385–93.
Büchel C, Peters J, Banaschewski T, Bokde ALW, Bromberg U, Conrod PJ, et al. Blunted ventral striatal responses to anticipated rewards foreshadow problematic drug use in novelty-seeking adolescents. Nat Commun. 2017;8:14140.
pubmed: 28221370
pmcid: 5321762
Whelan R, Watts R, Orr CA, Althoff RR, Artiges E, Banaschewski T, et al. Neuropsychosocial profiles of current and future adolescent alcohol misusers. Nature. 2014;512:185–9.
pubmed: 25043041
pmcid: 4486207
Heinrich A, Müller KU, Banaschewski T, Barker GJ, Bokde ALW, Bromberg U, et al. Prediction of alcohol drinking in adolescents: Personality-traits, behavior, brain responses, and genetic variations in the context of reward sensitivity. Biol Psychol. 2016;118:79–87.
pubmed: 27180911
Ersche KD, Turton AJ, Chamberlain SR, Müller U, Bullmore ET, Robbins TW. Cognitive dysfunction and anxious-impulsive personality traits are endophenotypes for drug dependence. Am J Psychiatry. 2012;169:926–36.
pubmed: 22952072
pmcid: 3533378
Ferris J, Wynne H. The Canadian problem gambling index. Final report. Ottawa: Canadian Centre on Substance Abuse; 2001.
Wechsler D. Wechsler abbreviated scale of intelligence: WASI. 1999.
Beck AT, Steer RA, Brown GK. Manual for Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation; 1996.
Beck AT, Epstein N, Brown G, Steer RA. An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol. 1988;56:893–831.
pubmed: 3204199
Bush K, Kivlahan DR, McDonell MB, Fihn SD, Bradley KA. for the Ambulatory Care Quality Improvement Project. The AUDIT Alcohol Consumption Questions (AUDIT-C): An Effective Brief Screening Test for Problem Drinking. Arch Intern Med. 1998;158:1789.
pubmed: 9738608
Skinner HA. The drug abuse screening test. Addict Behav. 1982;7:363–71.
pubmed: 7183189
Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom K-O. The Fagerström test for nicotine dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict. 1991;86:1119–27.
pubmed: 1932883
Kessler RC, Hwang I, LaBrie R, Petukhova M, Sampson NA, Winters KC, et al. DSM-IV pathological gambling in the National Comorbidity Survey Replication. Psychol Med. 2008;38:1351–60.
pubmed: 18257941
pmcid: 2293303
Bernstein DP, Stein JA, Newcomb MD, Walker E, Pogge D, Ahluvalia T, et al. Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abus Negl. 2003;27:169–90.
Lesieur HR, Blume SB. The South Oaks Gambling Screen (SOGS): a new instrument for the identification of pathological gamblers. Am J Psychiatry. 1987;144:1184–8.
pubmed: 3631315
Cyders MA, Smith GT, Spillane NS, Fischer S, Annus AM, Peterson C. Integration of impulsivity and positive mood to predict risky behavior: development and validation of a measure of positive urgency. Psychol Assess. 2007;19:107–18.
pubmed: 17371126
Kirby KN, Petry NM, Bickel WK. Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. J Exp Psychol Gen. 1999;128:78–87.
pubmed: 10100392
Logan GD, Cowan WB, Davis KA. On the ability to inhibit simple and choice reaction time responses: a model and a method. J Exp Psychol Hum Percept Perform. 1984;10:276–91.
pubmed: 6232345
Rogers RD, Everitt BJ, Baldacchino A, Blackshaw AJ, Swainson R, Wynne K, et al. Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: evidence for monoaminergic mechanisms. Neuropsychopharmacology. 1999;20:322–39.
pubmed: 10088133
Chase HW, Clark L. Gambling severity predicts midbrain response to near-miss outcomes. J Neurosci. 2010;30:6180–7.
pubmed: 20445043
pmcid: 2929454
Clark L, Lawrence AJ, Astley-Jones F, Gray N. Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry. Neuron. 2009;61:481–90.
pubmed: 19217383
pmcid: 2658737
Clark L, Studer B, Bruss J, Tranel D, Bechara A. Damage to insula abolishes cognitive distortions during simulated gambling. Proc Natl Acad Sci USA. 2014;111:6098–103.
pubmed: 24711387
van Timmeren T, Zhutovsky P, van Holst RJ, Goudriaan AE. Connectivity networks in gambling disorder: a resting-state fMRI study. Int Gambl Stud. 2018;18:242–58.
Segarra N, Metastasio A, Ziauddeen H, Spencer J, Reinders NR, Dudas RB, et al. Abnormal Frontostriatal Activity During Unexpected Reward Receipt in Depression and Schizophrenia: Relationship to Anhedonia. Neuropsychopharmacology. 2016;41:2001–10.
pubmed: 26708106
pmcid: 4820052
Clark L, Boileau I, Zack M. Neuroimaging of reward mechanisms in Gambling disorder: an integrative review. Mol Psychiatry. 2019;24:674–93.
pubmed: 30214041
Leyton M, Vezina P. Striatal ups and downs: their roles in vulnerability to addictions in humans. Neurosci Biobehav Rev. 2013;37:1999–2014.
pubmed: 23333263
Fauth-Bühler M, Zois E, Vollstädt-Klein S, Lemènager T, Beutel M, Mann K. Insula and striatum activity in effort-related monetary reward processing in gambling disorder: the role of depressive symptomatology. NeuroImage: Clin. 2014;6:243–51.
van Holst RJ, Veltman DJ, Büchel C, Van Den Brink W, Goudriaan AE. Distorted expectancy coding in problem gambling: is the addictive in the anticipation? Biol Psychiatry. 2012;71:741–8.
pubmed: 22342105
Billieux J, Lagrange G, Van der Linden M, Lançon C, Adida M, Jeanningros R. Investigation of impulsivity in a sample of treatment-seeking pathological gamblers: a multidimensional perspective. Psychiatry Res. 2012;198:291–6.
pubmed: 22421073
Navas JF, Billieux J, Perandrés-Gómez A, López-Torrecillas F, Cándido A, Perales JC. Impulsivity traits and gambling cognitions associated with gambling preferences and clinical status. Int Gambl Stud. 2017;17:102–24.
Volkow ND, Wang G-J, Begleiter H, Porjesz B, Fowler JS, Telang F, et al. High levels of dopamine D2 receptors in unaffected members of alcoholic families. Arch Gen Psychiat. 2006;63:999.
pubmed: 16953002
Tuvblad C, Gao Y, Wang P, Raine A, Botwick T, Baker LA. The genetic and environmental etiology of decision-making: a longitudinal twin study. J Adolesc. 2013;36:245–55.
pubmed: 23261073
Wilson D, da Silva Lobo DS, Tavares H, Gentil V, Vallada H. Family-based association analysis of serotonin genes in pathological gambling disorder: evidence of vulnerability risk in the 5HT-2A receptor gene. J Mol Neurosci. 2013;49:550–3.
pubmed: 22740152
Lobo DSS, Aleksandrova L, Knight J, Casey DM, el-Guebaly N, Nobrega JN, et al. Addiction-related genes in gambling disorders: new insights from parallel human and pre-clinical models. Mol Psychiatry. 2015;20:1002–10.
pubmed: 25266122
Comings DE, Rosenthal RJ, Lesieur HR, Rugle LJ, Muhleman D, Chiu C, et al. A study of the dopamine D2 receptor gene in pathological gambling. Pharmacogenetics. 1996;6:223–34.
pubmed: 8807661
Qin H, Zeng J, Chen H, Deng L, Su L, Can Your DNA. Influence your bet-placing? the impact of cannabinoid receptor 1 gene on gambling tasks. Front Hum Neurosci 2018;12:458.
pubmed: 30546300
pmcid: 6278673
Nees F, Tzschoppe J, Patrick CJ, Vollstädt-Klein S, Steiner S, Poustka L, et al. Determinants of early alcohol use in healthy adolescents: the differential contribution of neuroimaging and psychological factors. Neuropsychopharmacology. 2012;37:986–95.
pubmed: 22113088
Morales AM, Jones SA, Ehlers A, Lavine JB, Nagel BJ. Ventral striatal response during decision making involving risk and reward is associated with future binge drinking in adolescents. Neuropsychopharmacology. 2018;43:1884–90.
pubmed: 29789576
pmcid: 6046057
Galvan A, Hare TA, Parra CE, Penn J, Voss H, Glover G, et al. Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci. 2006;26:6885–92.
pubmed: 16793895
pmcid: 6673830
Hoogendam JM, Kahn RS, Hillegers MHJ, van Buuren M, Vink M. Different developmental trajectories for anticipation and receipt of reward during adolescence. Dev Cogn Neurosci. 2013;6:113–24.
pubmed: 24055865
Volkow ND, Wang GJ, Fowler JS, Logan J, Gatley SJ, Hitzemann R, et al. Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects. Nature. 1997;386:830–3.
pubmed: 9126741
Hommer DW, Bjork JM, Gilman JM. Imaging brain response to reward in addictive disorders. Ann N Y Acad Sci. 2011;1216:50–61.
pubmed: 21272010
Clark L, Bechara A, Damasio H, Aitken MRF, Sahakian BJ, Robbins TW. Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making. Brain. 2008;131:1311–22.
pubmed: 18390562
pmcid: 2367692
Li Y, Wang Z, Boileau I, Dreher J-C, Gelskov S, Genauck A, et al. Altered orbitofrontal sulcogyral patterns in gambling disorder: a multicenter study. Transl Psychiatry. 2019;9:186.
pubmed: 31383841
pmcid: 6683128
Goodwin BC, Browne M, Rockloff M, Rose J. A typical problem gambler affects six others. Int Gambl Stud. 2017;17:276–89.
Slutske WS, Zhu G, Meier MH, Martin NG. Genetic and environmental influences on disordered gambling in men and women. Arch Gen Psychiatry. 2010;67:624–30.
pubmed: 20530012
pmcid: 3600804
Vitaro F, Hartl AC, Brendgen M, Laursen B, Dionne G, Boivin M. Genetic and environmental influences on gambling and substance use in early adolescence. Behav Genet. 2014;44:347–55.
pubmed: 24824822
Hoehne A, Richard-Devantoy S, Ding Y, Turecki G, Jollant F. First-degree relatives of suicide completers may have impaired decision-making but functional cognitive control. J Psychiatr Res. 2015;68:192–7.
pubmed: 26228419
Cavedini P, Zorzi C, Piccinni M, Cavallini MC, Bellodi L. Executive dysfunctions in obsessive-compulsive patients and unaffected relatives: searching for a new intermediate phenotype. Biol Psychiatry. 2010;67:1178–84.
pubmed: 20381015