Skip to main content
SpringerLink
Log in

Functional anatomy of outcome evaluation during Iowa Gambling Task performance in patients with Parkinson’s disease: an fMRI study

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate the functional anatomy of decision-making during the Iowa Gambling Task in patients with Parkinson’s disease. We used event-related functional magnetic resonance imaging (fMRI) during a computerized version of IGT to compare 18 PD patients on dopaminergic medication in the ON state and 18 healthy control subjects. Our analyses focused on outcome evaluation following card selection, because we expected this aspect of decision-making to be impaired in PD patients. The PD patients exhibited lower activation of the left putamen than the control group as a reaction to penalty. Using psychophysiological interaction analysis, we identified decreased functional connectivity between the right globus pallidus internus and the left anterior cingulate gyrus in the PD group. In contrast, increased connectivity between these structures was observed after penalty in the control group. Our results suggest altered functioning of the basal ganglia and their connections with the cortical structures involved in the limbic loop (e.g., the limbic fronto-striatal circuit of the basal ganglia) during decision-making in PD patients. Differences in the response to loss could be associated with insufficient negative reinforcement after a loss in PD patients in the ON state in comparison to a healthy population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Dunn BD, Dalgleish T, Lawrence AD (2006) The somatic marker hypothesis: a critical evaluation. Neurosci Biobehav Rev 30:239–271

    Article  PubMed  Google Scholar 

  2. Pessiglione M, Seymour B, Flandin G et al (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442(7106):1042–1045

    Article  PubMed  CAS  Google Scholar 

  3. Poletti M, Cavedini P, Bonuccelli U (2011) Iowa Gambling Task in Parkinson’s disease. J Clin Exp Neuropsychol 33(4):395–409

    Article  PubMed  Google Scholar 

  4. Poletti M, Frosini D, Lucetti C et al (2010) Decision making in de novo Parkinson’s disease. Mov Disord 25(10):1432–1436

    Article  PubMed  Google Scholar 

  5. Pagonabarraga J, García-Sánchez C, Llebaria G et al (2007) Controlled study of decision-making and cognitive impairment in Parkinson’s disease. Mov Disord 22(10):1430–1435

    Article  PubMed  Google Scholar 

  6. Kobayakawa M, Koyama S, Mimura M, Kawamura M (2008) Decision making in Parkinson’s disease: analysis of behavioral and psychological patterns in the Iowa gambling task. Mov Disord 23(4):547–552

    Article  PubMed  Google Scholar 

  7. Mimura M, Oeda R, Kawamura M (2006) Impaired decision-making in Parkinson’s disease. Parkinsonism Relat Disord 12:169–175

    Article  PubMed  Google Scholar 

  8. Czernecki V, Pillon B, Houeto JL et al (2002) Motivation, reward and Parkinson’s disease: influence of dopatherapy. Neuropsychologia 40(13):2257–2267

    Article  PubMed  CAS  Google Scholar 

  9. Delazer M, Sinz H, Zamarian L et al (2009) Decision making under risk and under ambiguity in Parkinson’s disease. Neuropsychologia 47(8–9):1901–1908

    Article  PubMed  CAS  Google Scholar 

  10. Ibarretxe-Bilbao N, Junque C, Tolosa E et al (2009) Neuroanatomical correlates of impaired decision making and facial emotion recognition in early Parkinson’s disease. Eur J Neurosci 30(6):1162–1171

    Article  PubMed  Google Scholar 

  11. Peretta JG, Pari G, Beninger RJ (2005) Effects of Parkinson’s disease on two putative nondeclarative learning tasks: probabilistic classification and gambling. Cogn Behav Neurol 18(4):185–192

    Article  Google Scholar 

  12. Euteneuer F, Schaefer F, Stuermer R et al (2009) Dissociation of decision-making under ambiguity and decision-making under risk in patients with Parkinson’s disease: a neuropsychological and psychophysiological study. Neuropsychologia 47(13):2882–2890

    Article  PubMed  Google Scholar 

  13. Rossi M, Gerschcovich ER, de Achaval D et al (2010) Decision-making in Parkinson’s disease patients with and without pathological gambling. Eur J Neurol 17(1):97–102

    Article  PubMed  CAS  Google Scholar 

  14. Poletti M, Bonucelli U (2012) Impulse control disorders in Parkinson’s disease: the role of personality and cognitive status. J Neurol 259(11):2269–2277

    Article  PubMed  Google Scholar 

  15. Thiel A, Hilker R, Kessler J et al (2003) Activation of basal ganglia loops in idiopathic Parkinson’s disease: a PET study. J Neural Transm 110:1289–1301

    Article  PubMed  CAS  Google Scholar 

  16. Gescheidt T, Czekóová K, Urbánek T et al (2012) Iowa Gambling Task in patients with early-onset Parkinson’s disease: strategy analysis. Neurol Sci 33(6):1329–1335

    Article  PubMed  Google Scholar 

  17. Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50(1–3):7–15

    Article  PubMed  CAS  Google Scholar 

  18. Ernst M, Paulus MP (2005) Neurobiology of decision making: a selective review from a neurocognitive and clinical perspective. Biol Psychiatry 58(8):597–604

    Article  PubMed  Google Scholar 

  19. Li X, Lu ZL, D’Argembau A et al (2010) The Iowa Gambling Task in fMRI images. Hum Brain Mapp 31(3):410–423

    PubMed  CAS  Google Scholar 

  20. Bechara A (2004) Disturbances of emotion regulation after focal brain lesions. Int Rev Neurobiol 62:159–193

    Article  PubMed  Google Scholar 

  21. Eldridge LL, Knowlton BJ, Furmanski CS et al (2000) Remembering episodes: a selective role for the hippocampus during retrieval. Nat Neurosci 3(11):1149–1152

    Article  PubMed  CAS  Google Scholar 

  22. Gleichgerrcht E, Ibáñez A, Roca M et al (2010) Decision-making congnition in neurodegenerative diseases. Nat Rev Neurol 6(11):611–623

    Article  PubMed  CAS  Google Scholar 

  23. Toplak ME, Sorge GB, Benoit A et al (2010) A review of associations between Iowa Gambling Task performance, executive functions and intelligence. Clin Psychol Rev 30:562–581

    Article  PubMed  Google Scholar 

  24. Ernst M, Bolla K, Mouratidis M, Contoreggi C et al (2002) Decision-making in a risk-taking task: a PET study. Neuropysychopharmacology 26:682–691

    Article  Google Scholar 

  25. Clark L, Manes F, Antoun N et al (2003) The contribution of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage. Neuropsychologia 41(11):1474–1483

    Article  PubMed  Google Scholar 

  26. Ward CD, Gibb WR (1990) Research diagnostic criteria for Parkinson’s disease. Adv Neurol 53:245–249

    PubMed  CAS  Google Scholar 

  27. Fahn S, Elton RL, and members of the UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne DB, Goldstein M (eds) Recent developments in Parkinson’s disease. Macmillan Healthcare Information, Florham Park, NJ pp 153–163

  28. Hoehn M, Yahr M (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442

    Article  PubMed  CAS  Google Scholar 

  29. Tomlinson CL, Stowe R, Patel S et al (2010) Systematic review of levodopa dose Equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653

    Article  PubMed  Google Scholar 

  30. Montgomery SA, Asberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134(4):382–389

    Article  PubMed  CAS  Google Scholar 

  31. Lesieur HR, Blume SB (1987) The South Oaks Gambling Screen (SOGS): a new instrument for the identification of pathologic gamblers. Am J Psychiatry 144(9):1184–1188

    PubMed  CAS  Google Scholar 

  32. Christenson GA, Faber RJ, de Zwaan M et al (1994) Compulsive buying: descriptive characteristics and psychiatric comorbidity. J Clin Psychiatry 55:5–11

    PubMed  CAS  Google Scholar 

  33. Fukui H, Murai T, Fukuyama H et al (2005) Functional activity related to risk anticipation during performance of the Iowa gambling task. Neuroimage 24(1):253–259

    Article  PubMed  Google Scholar 

  34. Buelow MT, Suhr JA (2009) Construct validity of the Iowa Gambling Task. Neuropsychol Rev 19(1):102–114

    Article  PubMed  Google Scholar 

  35. Hayasaka S, Nichols TE (2003) Validating cluster size inference: random field and permutation methods. Neuroimage 20(4):2343–2356

    Article  PubMed  Google Scholar 

  36. Hayasaka S, Phan KL, Liberzon I et al (2004) Nonstationary cluster-size inference with random field and permutation methods. Neuroimage 22(2):676–687

    Article  PubMed  Google Scholar 

  37. Friston KJ, Buechel C, Fink GR et al (1997) Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6(3):218–229

    Article  PubMed  CAS  Google Scholar 

  38. Christakau A, Brammer M, Giampietro V et al (2009) Right ventromedial and dorsolateral prefrontal cortices mediate adaptive decisions under ambiguity by integrating choice utility and outcome evaluation. J Neurosci 29(35):11020–11028

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the project “CEITEC Central European Institute of Technology” (CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund. The participation of T.U. was supported by a research project of the Czech Science Foundation, no. P407/12/2432. The participation of J.V. was supported by the European Regional Development Fund Project FNUSA-ICRC (No.CZ.1.05/1.1.00/02.0123).

Ethical standards

The study has been approved by appropriate ethics committee and has therefore been performed in accordance with ethical standards laid down in the 1964 declaration of Helsinki.

Author information

Authors and Affiliations

  1. CEITEC-Central European Institute of Technology, Behavioral and Social Neuroscience Research Group, Masaryk University, University Campus Bohunice, Building A4, Brno, Czech Republic

    Tomáš Gescheidt, Kristína Czekóová, Daniel J. Shaw & Martin Bareš

  2. Department of Neurology, Medical Faculty Masaryk University and St. Anne’s University Hospital, Brno, Czech Republic

    Tomáš Gescheidt & Martin Bareš

  3. CEITEC-Central European Institute of Technology, Molecular and Functional Imaging Research Group, Masaryk University, Brno, Czech Republic

    Radek Mareček & Michal Mikl

  4. Institute of Psychology, Academy of Sciences of the Czech Republic, Brno, Czech Republic

    Tomáš Urbánek

  5. Department of Medical Imaging, Medical Faculty Masaryk University and St. Anne’s University Hospital, Brno, Czech Republic

    Jiří Vaníček

  6. International Clinical Research Center (ICRC), St. Anne’s University Hospital, Brno, Czech Republic

    Jiří Vaníček

Authors
  1. Tomáš Gescheidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Radek Mareček
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michal Mikl
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kristína Czekóová
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tomáš Urbánek
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiří Vaníček
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Daniel J. Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Martin Bareš
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Bareš.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 30 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gescheidt, T., Mareček, R., Mikl, M. et al. Functional anatomy of outcome evaluation during Iowa Gambling Task performance in patients with Parkinson’s disease: an fMRI study. Neurol Sci 34, 2159–2166 (2013). https://doi.org/10.1007/s10072-013-1439-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-013-1439-0

Keywords

Search

Navigation