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Brain Structure and Function

, Volume 220, Issue 1, pp 469–477 | Cite as

Higher volume of ventral striatum and right prefrontal cortex in pathological gambling

  • Saskia Koehler
  • Eva Hasselmann
  • Torsten Wüstenberg
  • Andreas Heinz
  • Nina Romanczuk-Seiferth
Original Article

Abstract

Functional neuroimaging studies have implicated an involvement of the prefrontal cortex and mesolimbic reward system (i.e., ventral striatum) in pathological gambling (PG). However, there is a lack of studies focusing on structural changes in frontostriatal brain regions in adult subjects with PG. In order to study differences in local grey matter volume, 20 male subjects with PG and 21 matched controls underwent structural magnetic resonance imaging. Structural brain data were analysed via voxel-based morphometry with a focus on prefrontal areas and ventral striatum. By comparing grey matter volumes in brain regions highly relevant for brain functional changes in PG, the present study found a higher volume in right ventral striatum and right prefrontal cortex by means of voxel-wise morphometry in PG subjects as compared to controls. Our findings demonstrate local grey matter changes in brain areas that have previously been associated with functional changes in PG. Hypertrophy in the prefrontal cortex might be an adaptation at least partly induced by the higher grey matter volume in the ventral striatum and may help to increase cognitive control over gambling impulses. Future research should explore the relationship between functional and structural alterations as well as the course of changes in PG.

Keywords

fMRI Gambling Striatum Behavioural addiction Reward system Voxel-based morphometry 

Notes

Acknowledgments

We thank all subjects for participation. The study was funded by “Senatsverwaltung für Gesundheit, Umwelt und Verbraucherschutz, Berlin” and Deutsche Forschungsgemeinschaft (DFG), graduate school 86 “Berlin School of Mind and Brain” (S.K.).

Conflict of interest

Professor Heinz has received research funding from the German Research Foundation (Deutsche Forschungsgemeinschaft; HE 2597/4-3; 7-3; 13-1;14-1;15-1; Excellence Cluster Exc 257 & STE 1430/2-1) and the German Federal Ministry of Education and Research (01GQ0411; 01QG87164; NGFN Plus 01 GS 08152 and 01 GS 08 159). He received unrestricted research grants from Eli Lilly & Company, Janssen-Cilag, and Bristol-Myers Squibb. All other authors declare no conflict of interest.

References

  1. APA (2000) Diagnostic and statistical manual of mental disorders, 4th edn, text rev. American Psychiatric Association, Washington DCGoogle Scholar
  2. Aron AR, Robbins TW, Ra Poldrack (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8(4):170–177. doi: 10.1016/j.tics.2004.02.010 PubMedCrossRefGoogle Scholar
  3. Ashburner J (2007) A fast diffeomorphic image registration algorithm. NeuroImage 38(1):95–113. doi: 10.1016/j.neuroimage.2007.07.007 PubMedCrossRefGoogle Scholar
  4. Aster M, Neubauer A, Horn R (2006) Wechsler Intelligenztest für Erwachsene (WIE). Deutschsprachige bearbeitung und adaption des WAIS-III von David Wechsler. Harcourt Test Services, FarnkfurtGoogle Scholar
  5. Balodis IM, Kober H, Worhunsky PD, Stevens MC, Pearlson GD, Potenza MN (2012) Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling. Biol Psychiatry 71(8):749–757. doi: 10.1016/j.biopsych.2012.01.006 PubMedCentralPubMedCrossRefGoogle Scholar
  6. 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(1):35–45. doi: 10.1002/hbm.20128 PubMedCrossRefGoogle Scholar
  7. Buhler M, Mann K (2011) Alcohol and the human brain: a systematic review of different neuroimaging methods. Alcohol Clin Exp Res 35(10):1771–1793. doi: 10.1111/j.1530-0277.2011.01540.x PubMedCrossRefGoogle Scholar
  8. Cannonieri GC, Bonilha L, Fernandes PT, Cendes F, Li LM (2007) Practice and perfect: length of training and structural brain changes in experienced typists. NeuroReport 18(10):1063–1066. doi: 10.1097/WNR.0b013e3281a030e5 PubMedCrossRefGoogle Scholar
  9. Cavedini P, Riboldi G, Keller R, D’Annucci A, Bellodi L (2002) Frontal lobe dysfunction in pathological gambling patients. Biol Psychiatry 51(04):334–341PubMedCrossRefGoogle Scholar
  10. Chamberlain SR, La Menzies, Na Fineberg, Del Campo N, Suckling J, Craig K, Müller U, Robbins TW, Bullmore ET, Sahakian BJ (2008) Grey matter abnormalities in trichotillomania: morphometric magnetic resonance imaging study. Br J Psychiatry 193(3):216–221. doi: 10.1192/bjp.bp.107.048314 PubMedCentralPubMedCrossRefGoogle Scholar
  11. Chang L, Alicata D, Ernst T, Volkow N (2007) Structural and metabolic brain changes in the striatum associated with methamphetamine abuse. Addiction 102(Suppl):16–32. doi: 10.1111/j.1360-0443.2006.01782.x PubMedCrossRefGoogle Scholar
  12. Clark L, Lawrence AJ, Astley-Jones F, Gray N (2009) Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry. Neuron 61(3):481–490. doi: 10.1016/j.neuron.2008.12.031 PubMedCentralPubMedCrossRefGoogle Scholar
  13. Cohen JR, Lieberman MD (2010) The common neural basis of exerting self-control in multiple domains. In: Hassin RR, Ochsner KN, Trope Y (eds) Oxford University Press, New YorkGoogle Scholar
  14. Crockford DN, Goodyear B, Edwards J, Quickfall J, El-Guebaly N (2005) Cue-induced brain activity in pathological gamblers. Biol Psychiatry 58(10):787–795. doi: 10.1016/j.biopsych.2005.04.037 PubMedCrossRefGoogle Scholar
  15. Dagher A, Robbins TW (2009) Personality, addiction, dopamine: insights from Parkinson’s disease. Neuron 61(4):502–510. doi: 10.1016/j.neuron.2009.01.031 PubMedCrossRefGoogle Scholar
  16. de Ruiter MB, Veltman DJ, Goudriaan AE, Oosterlaan J, Sjoerds Z, van Den Brink W (2009) Response perseveration and ventral prefrontal sensitivity to reward and punishment in male problem gamblers and smokers. Neuropsychopharmacology 34(4):1027–1038. doi: 10.1038/npp.2008.175 PubMedCrossRefGoogle Scholar
  17. Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A (2004) Neuroplasticity: changes in grey matter induced by training. Nature 427(6972):311–312. doi: 10.1038/427311a PubMedCrossRefGoogle Scholar
  18. First M, Spitzer R, Gibbon M, Williams J (2001) Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition with psychotic screen (SCID-I/PW/PSYSCREEN). Biometrics Research, New York State Psychiatric Institute, New YorkGoogle Scholar
  19. Fox PT, Lancaster JL (1994) Neuroscience on the net. Science 266(5187):994–996PubMedCrossRefGoogle Scholar
  20. Friston K (2012) Ten ironic rules for non-statistical reviewers. Neuroimage 61(4):1300–1310. doi: 10.1016/j.neuroimage.2012.04.018 PubMedCrossRefGoogle Scholar
  21. Goudriaan AE, Oosterlaan J, de Beurs E, van den Brink W (2005) Decision making in pathological gambling: a comparison between pathological gamblers, alcohol dependents, persons with Tourette syndrome, and normal controls. Brain Res Cogn Brain Res 23(1):137–151. doi: 10.1016/j.cogbrainres.2005.01.017 PubMedCrossRefGoogle Scholar
  22. 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(4):534–547. doi: 10.1111/j.1360-0443.2006.01380.x PubMedCrossRefGoogle Scholar
  23. Granert O, Peller M, Gaser C, Groppa S, Hallett M, Knutzen A, Deuschl G, Zeuner KE, Siebner HR (2011) Manual activity shapes structure and function in contralateral human motor hand area. NeuroImage 54(1):32–41. doi: 10.1016/j.neuroimage.2010.08.013 PubMedCrossRefGoogle Scholar
  24. Han DH, Lyoo IK, Renshaw PF (2012) Differential regional gray matter volumes in patients with on-line game addiction and professional gamers. J Psychiatr Res 46(4):507–515. doi: 10.1016/j.jpsychires.2012.01.004 PubMedCrossRefGoogle Scholar
  25. Haslinger B, Erhard P, Altenmuller E, Hennenlotter A, Schwaiger M, Grafin von Einsiedel H, Rummeny E, Conrad B, Ceballos-Baumann AO (2004) Reduced recruitment of motor association areas during bimanual coordination in concert pianists. Hum Brain Mapp 22(3):206–215. doi: 10.1002/hbm.20028 PubMedCrossRefGoogle Scholar
  26. Hong SB, Kim JW, Choi EJ, Kim HH, Suh JE, Kim CD, Klauser P, Whittle S, Yucel M, Pantelis C, Yi SH (2013) Reduced orbitofrontal cortical thickness in male adolescents with internet addiction. Behav Brain Funct 9:11. doi: 10.1186/1744-9081-9-11 PubMedCentralPubMedCrossRefGoogle Scholar
  27. Horstmann A, Busse FP, Mathar D, Müller K, Lepsien J, Schlögl H, Kabisch S, Kratzsch J, Neumann J, Stumvoll M, Villringer A, Pleger B (2011) Obesity-related differences between women and men in brain structure and goal-directed behavior. Front Hum Neurosci 5:58. doi: 10.3389/fnhum.2011.00058 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Jessup RK, O’Doherty JP (2011) Human dorsal striatal activity during choice discriminates reinforcement learning behavior from the gambler’s fallacy. J Neurosci 31(17):6296–6304. doi: 10.1523/JNEUROSCI.6421-10.2011 PubMedCrossRefGoogle Scholar
  29. Joutsa J, Saunavaara J, Parkkola R, Niemelä S, Kaasinen V (2011) Extensive abnormality of brain white matter integrity in pathological gambling. Psychiatry Res 194(3):340–346. doi: 10.1016/j.pscychresns.2011.08.001 PubMedCrossRefGoogle Scholar
  30. Joutsa J, Johansson J, Niemela S, Ollikainen A, Hirvonen MM, Piepponen P, Arponen E, Alho H, Voon V, Rinne JO, Hietala J, Kaasinen V (2012) Mesolimbic dopamine release is linked to symptom severity in pathological gambling. NeuroImage 60(4):1992–1999. doi: 10.1016/j.neuroimage.2012.02.006 PubMedCrossRefGoogle Scholar
  31. Kim SW, Grant JE, Potenza MN, Blanco C, Hollander E (2009) The Gambling Symptom Assessment Scale (G-SAS): a reliability and validity study. Psychiatry Res 166(1):76–84. doi: 10.1016/j.psychres.2007.11.008 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Knoch D, Fehr E (2007) Resisting the power of temptations: the right prefrontal cortex and self-control. Ann N Y Acad Sci 1104:123–134. doi: 10.1196/annals.1390.004 PubMedCrossRefGoogle Scholar
  33. Knoch D, Gianotti LR, Pascual-Leone A, Treyer V, Regard M, Hohmann M, Brugger P (2006) Disruption of right prefrontal cortex by low-frequency repetitive transcranial magnetic stimulation induces risk-taking behavior. J Neurosci 26(24):6469–6472. doi: 10.1523/JNEUROSCI.0804-06.2006 PubMedCrossRefGoogle Scholar
  34. Knutson B, Fong GW, Bennett SM, Adams CM, Hommer D (2003) A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. NeuroImage 18(2):263–272PubMedCrossRefGoogle Scholar
  35. Koechlin E, Hyafil A (2007) Anterior prefrontal function and the limits of human decision-making. Science 318(5850):594–598. doi: 10.1126/science.1142995 PubMedCrossRefGoogle Scholar
  36. Koechlin E, Basso G, Pietrini P, Panzer S, Grafman J (1999) The role of the anterior prefrontal cortex in human cognition. Nature 399(6732):148–151. doi: 10.1038/20178 PubMedCrossRefGoogle Scholar
  37. Kubota M, Nakazaki S, Hirai S, Saeki N, Yamaura A, Kusaka T (2001) Alcohol consumption and frontal lobe shrinkage: study of 1432 non-alcoholic subjects. J Neurol Neurosurg Psychiatry 71(1):104–106PubMedCentralPubMedCrossRefGoogle Scholar
  38. Kuhn S, Romanowski A, Schilling C, Lorenz R, Morsen C, Seiferth N, Banaschewski T, Barbot A, Barker GJ, Buchel C, Conrod PJ, Dalley JW, Flor H, Garavan H, Ittermann B, Mann K, Martinot JL, Paus T, Rietschel M, Smolka MN, Strohle A, Walaszek B, Schumann G, Heinz A, Gallinat J (2011) The neural basis of video gaming. Transl Psychiatry 1:e53. doi: 10.1038/tp.2011.53 PubMedCentralPubMedCrossRefGoogle Scholar
  39. Li X, Lu ZL, D’Argembeau A (2010) The Iowa gambling task in fMRI images. Hum Brain Mapp 31(3):410–423. doi: 10.1002/hbm.20875.The PubMedCentralPubMedGoogle Scholar
  40. Lin F, Zhou Y, Du Y, Qin L, Zhao Z, Xu J, Lei H (2012) Abnormal white matter integrity in adolescents with internet addiction disorder: a tract-based spatial statistics study. PLoS ONE 7(1):e30253. doi: 10.1371/journal.pone.0030253 PubMedCentralPubMedCrossRefGoogle Scholar
  41. Linnet J, Peterson E, Doudet DJ, Gjedde A, Moller A (2010) Dopamine release in ventral striatum of pathological gamblers losing money. Acta Psychiatr Scand 122(4):326–333. doi: 10.1111/j.1600-0447.2010.01591.x PubMedCrossRefGoogle Scholar
  42. Maguire EA, Spiers HJ, Good CD, Hartley T, Frackowiak RS, Burgess N (2003) Navigation expertise and the human hippocampus: a structural brain imaging analysis. Hippocampus 13(2):250–259. doi: 10.1002/hipo.10087 PubMedCrossRefGoogle Scholar
  43. Marazziti D, Catena M, Osso D, Conversano C, Consoli G, Vivarelli L, Mungai F, Nasso ED, Golia F (2008) Clinical practice and epidemiology executive function abnormalities in pathological gamblers. Clin Pract Epidemiol Ment Health 4:7. doi: 10.1186/1745-0179-4-Received PubMedCentralPubMedCrossRefGoogle Scholar
  44. McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306(5695):503–507. doi: 10.1126/science.1100907 PubMedCrossRefGoogle Scholar
  45. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202. doi: 10.1146/annurev.neuro.24.1.167 PubMedCrossRefGoogle Scholar
  46. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113PubMedCrossRefGoogle Scholar
  47. Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt impulsiveness scale. J Clin Psychol 51(6):768–774PubMedCrossRefGoogle Scholar
  48. Petry J, Baulig T (1996) KFG: Kurzfragebogen zum Glücksspielverhalten. Psychologie Verlags Union, Weinheim, pp 300–302Google Scholar
  49. Potenza MN, Leung HC, Blumberg HP, Peterson BS, Fulbright RK, Lacadie CM, Skudlarski P, Gore JC (2003) An FMRI Stroop task study of ventromedial prefrontal cortical function in pathological gamblers. Am J Psychiatry 160(11):1990–1994PubMedCrossRefGoogle Scholar
  50. Reuter J, Raedler T, Rose M, Hand I, Gläscher J, Büchel C (2005) Pathological gambling is linked to reduced activation of the mesolimbic reward system. Nat Neurosci 8(2):147–148. doi: 10.1038/nn1378 PubMedCrossRefGoogle Scholar
  51. Schmidt-Wilcke T, Rosengarth K, Luerding R, Bogdahn U, Greenlee MW (2010) Distinct patterns of functional and structural neuroplasticity associated with learning Morse code. NeuroImage 51(3):1234–1241. doi: 10.1016/j.neuroimage.2010.03.042 PubMedCrossRefGoogle Scholar
  52. Schwartz DL, Mitchell AD, Lahna DL, Luber HS, Huckans MS, Mitchell SH, Hoffman WF (2010) Global and local morphometric differences in recently abstinent methamphetamine-dependent individuals. NeuroImage 50(4):1392–1401. doi: 10.1016/j.neuroimage.2010.01.056 PubMedCentralPubMedCrossRefGoogle Scholar
  53. Simmonds DJ, Pekar JJ, Mostofsky SH (2008) Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46(1):224–232. doi: 10.1016/j.neuropsychologia.2007.07.015 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6(3):309–315. doi: 10.1038/nn1008 PubMedCrossRefGoogle Scholar
  55. Steeves TDL, Miyasaki J, Zurowski M, Lang aE, Pellecchia G, Van Eimeren T, Rusjan P, Houle S, Strafella aP (2009) Increased striatal dopamine release in Parkinsonian patients with pathological gambling: a [11C] raclopride PET study. Brain 132(Pt 5):1376–1385. doi: 10.1093/brain/awp054 PubMedCentralPubMedCrossRefGoogle Scholar
  56. Sullivan EV, Deshmukh A, De Rosa E, Rosenbloom MJ, Pfefferbaum A (2005) Striatal and forebrain nuclei volumes: contribution to motor function and working memory deficits in alcoholism. Biol Psychiatry 57(7):768–776. doi: 10.1016/j.biopsych.2004.12.012 PubMedCrossRefGoogle Scholar
  57. Sun AY, Sun GY (2001) Ethanol and oxidative mechanisms in the brain. J Biomed Sci 8(1):37–43. doi: 10.1159/000054011 PubMedCrossRefGoogle Scholar
  58. van Holst RJ, de Ruiter MB, van den Brink W, Veltman DJ, Goudriaan AE (2012a) A voxel-based morphometry study comparing problem gamblers, alcohol abusers, and healthy controls. Drug Alcohol Depend 124(1–2):142–148. doi: 10.1016/j.drugalcdep.2011.12.025 PubMedCrossRefGoogle Scholar
  59. van Holst RJ, van Holstein M, van den Brink W, Veltman DJ, Goudriaan AE (2012b) Response inhibition during cue reactivity in problem gamblers: an fMRI study. PloS ONE 7(3):e30909–e30909. doi: 10.1371/journal.pone.0030909 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Wrase J, Makris N, Braus DF, Mann K, Smolka MN, Kennedy DN, Caviness VS, Hodge SM, Tang L, Albaugh M, Ziegler DA, Davis OC, Kissling C, Schumann G, Breiter HC, Heinz A (2008) Amygdala volume associated with alcohol abuse relapse and craving. Am J Psychiatry 165(9):1179–1184. doi: 10.1176/appi.ajp.2008.07121877 PubMedCrossRefGoogle Scholar
  61. Yip SW, Lacadie C, Xu J, Worhunsky PD, Fulbright RK, Constable RT, Potenza MN (2011) Reduced genual corpus callosal white matter integrity in pathological gambling and its relationship to alcohol abuse or dependence. World J Biol Psychiatry. doi: 10.3109/15622975.2011.568068 PubMedCentralPubMedGoogle Scholar
  62. Yuan K, Qin W, Wang G, Zeng F, Zhao L, Yang X, Liu P, Liu J, Sun J, von Deneen KM, Gong Q, Liu Y, Tian J (2011) Microstructure abnormalities in adolescents with internet addiction disorder. PLoS ONE 6(6):e20708. doi: 10.1371/journal.pone.0020708 PubMedCentralPubMedCrossRefGoogle Scholar
  63. Zarei M, Mataix-Cols D, Heyman I, Hough M, Doherty J, Burge L, Winmill L, Nijhawan S, Matthews PM, James A (2011) Changes in gray matter volume and white matter microstructure in adolescents with obsessive-compulsive disorder. Biol Psychiatry 70(11):1083–1090. doi: 10.1016/j.biopsych.2011.06.032 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Saskia Koehler
    • 1
    • 2
    • 3
  • Eva Hasselmann
    • 1
  • Torsten Wüstenberg
    • 1
  • Andreas Heinz
    • 1
    • 2
  • Nina Romanczuk-Seiferth
    • 1
  1. 1.Department of Psychiatry and PsychotherapyCharité-Universitätsmedizin BerlinBerlinGermany
  2. 2.Berlin School of Mind and Brain and The Mind-Brain Institute, Humboldt-Universität zu BerlinBerlinGermany
  3. 3.Department of PsychologyHumboldt-Universität zu BerlinBerlinGermany

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