Skip to main content

Advertisement

SpringerLink
Log in

Effects of tDCS on reward responsiveness and valuation in Parkinson’s patients with impulse control disorders

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Parkinson’s disease (PD) patients with impulse control disorders (ICD) frequently report hypersensitivity to rewards. However, a few studies have explored the effectiveness of modulation techniques on symptoms experienced by these patients. In this study, we assessed the effect of anodal tDCS over the DLPFC on reward responsiveness and valuation in PD patients with ICD. 43 participants (15 PD patients with ICD, 13 PD without ICD, and 15 healthy matched controls) were asked to perform a reward-craving test employing both explicit (self-ratings of liking and wanting) and implicit (heart rate and skin conductance response) measures, as well as two temporal discounting tasks with food and money rewards. Each participant performed the experimental tasks during active anodal tDCS of the left dorsolateral prefrontal cortex (DLPFC), anodal tDCS of the primary motor cortex (M1), and sham tDCS. Results showed increased wanting and a steeper temporal discounting of rewards in PD with ICD compared to the other groups. Moreover, we found that PD without ICD exhibit reduced liking for rewards. tDCS results capable to modulate the altered intensity of PD patients’ liking, but not wanting and temporal discounting of rewards in PD patients with ICD. These findings confirm that alterations in reward responsiveness and valuation are characteristics of impulse control disorders in patients with PD but suggest that anodal tDCS over the left DLPFC is not capable to influence these processes. At the same time, they provide new insight into affective experience of rewards in PD.

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

Similar content being viewed by others

References

  1. O’Sullivan SS, Wu K, Politis M et al (2011) Cue-induced striatal dopamine release in Parkinson’s disease-associated impulsive-compulsive behaviours. Brain 134:969–978. https://doi.org/10.1093/brain/awr003

    Article  PubMed  Google Scholar 

  2. Politis M, Loane C, Wu K et al (2013) Neural response to visual sexual cues in dopamine treatment-linked hypersexuality in Parkinson’s disease. Brain 136:400–411. https://doi.org/10.1093/brain/aws326

    Article  PubMed  Google Scholar 

  3. Olney JJ, Warlow SM, Naffziger EE, Berridge KC (2018) Current perspectives on incentive salience and applications to clinical disorders. Curr Opin Behav Sci 22:59–69

    Article  Google Scholar 

  4. Kable JW (2014) Valuation, intertemporal choice, and self-control. Neuroeconomics, pp 173–192

  5. Terenzi D, Mainetto E, Barbato M et al (2019) Temporal and effort cost decision-making in healthy individuals with subclinical psychotic symptoms. Sci Rep 9:1–9. https://doi.org/10.1038/s41598-018-38284-x

    Article  CAS  Google Scholar 

  6. Paz-Alonso PM, Navalpotro-Gomez I, Boddy P et al (2020) Functional inhibitory control dynamics in impulse control disorders in Parkinson’s disease. Mov Disord 35:316–325

    Article  Google Scholar 

  7. Voon V, Reynolds B, Brezing C et al (2010) Impulsive choice and response in dopamine agonist-related impulse control behaviors. Psychopharmacology 207:645–659. https://doi.org/10.1007/s00213-009-1697-y

    Article  CAS  PubMed  Google Scholar 

  8. Housden CR, O’Sullivan SS, Joyce EM et al (2010) Intact reward learning but elevated delay discounting in Parkinson’s disease patients with impulsive-compulsive spectrum behaviors. Neuropsychopharmacology 35:2155–2164. https://doi.org/10.1038/npp.2010.84

    Article  PubMed  PubMed Central  Google Scholar 

  9. Spielberg JM, Stewart JL, Levin RL et al (2008) Prefrontal cortex, emotion, and approach/withdrawal motivation. Soc Personal Psychol Compass 2:135–153. https://doi.org/10.1111/j.1751-9004.2007.00064.x

    Article  PubMed  PubMed Central  Google Scholar 

  10. Staudinger MR, Erk S, Walter H (2011) Dorsolateral prefrontal cortex modulates striatal reward encoding during reappraisal of reward anticipation. Cereb Cortex. https://doi.org/10.1093/cercor/bhr041

    Article  PubMed  Google Scholar 

  11. Sellitto M, Ciaramelli E, di Pellegrino G (2010) Myopic discounting of future rewards after medial orbitofrontal damage in humans. J Neurosci 30:16429–16436. https://doi.org/10.1523/JNEUROSCI.2516-10.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Trojak B, Soudry-Faure A, Abello N et al (2016) Efficacy of transcranial direct current stimulation (tDCS) in reducing consumption in patients with alcohol use disorders: study protocol for a randomized controlled trial. Trials 17:250. https://doi.org/10.1186/s13063-016-1363-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. 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. https://doi.org/10.3389/fpsyg.2016.01421

    Article  PubMed  PubMed Central  Google Scholar 

  14. Terenzi D, Rumiati RI, Catalan M et al (2018) Reward sensitivity in Parkinson’s patients with binge eating. Park Relat Disord 51:79–84

    Article  Google Scholar 

  15. Kuoppa P, Pulkkinen K, Tarvainen MP et al (2016) Psychophysiological responses to positive and negative food and nonfood visual stimuli. J Neurosci Psychol Econ 9:78. https://doi.org/10.1037/npe0000053

    Article  Google Scholar 

  16. Cecchetto C, Rumiati RI, Aiello M (2017) Alexithymia and emotional reactions to odors. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-14404-x

    Article  CAS  Google Scholar 

  17. Boggio PS, Ferrucci R, Rigonatti SP et al (2006) Effects of transcranial direct current stimulation on working memory in patients with Parkinson’s disease. J Neurol Sci 249:31–38. https://doi.org/10.1016/j.jns.2006.05.062

    Article  PubMed  Google Scholar 

  18. Valentino F, Cosentino G, Brighina F et al (2014) Transcranial direct current stimulation for treatment of freezing of gait: a cross-over study. Mov Disord. https://doi.org/10.1002/mds.25897

    Article  PubMed  Google Scholar 

  19. Da Silva DCL, Lemos T, De Sá FA et al (2018) Effects of acute transcranial direct current stimulation on gait kinematics of individuals with parkinson disease. Top Geriatr Rehabil. https://doi.org/10.1097/TGR.0000000000000203

    Article  Google Scholar 

  20. Manenti R, Brambilla M, Rosini S et al (2014) Time up and go task performance improves after transcranial direct current stimulation in patient affected by Parkinson’s disease. Neurosci Lett. https://doi.org/10.1016/j.neulet.2014.07.052

    Article  PubMed  Google Scholar 

  21. Fertonani A, Ferrari C, Miniussi C (2015) What do you feel if I apply transcranial electric stimulation? Safety, sensations and secondary induced effects. Clin Neurophysiol 126:2181–2188. https://doi.org/10.1016/j.clinph.2015.03.015

    Article  PubMed  Google Scholar 

  22. Weintraub D, Mamikonyan E, Papay K et al (2012) Questionnaire for impulsive-compulsive disorders in Parkinson’s disease-rating scale. Mov Disord 27:242–247. https://doi.org/10.1002/mds.24023

    Article  PubMed  Google Scholar 

  23. Tomlinson CL, Stowe R, Patel S et al (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653. https://doi.org/10.1002/mds.23429

    Article  PubMed  Google Scholar 

  24. Mengotti P, Aiello M, Terenzi D et al (2018) How brain response and eating habits modulate food energy estimation. Physiol Behav. https://doi.org/10.1016/j.physbeh.2018.01.015

    Article  PubMed  Google Scholar 

  25. Petschow C, Scheef L, Paus S et al (2016) Central pain processing in early-stage Parkinson’s disease: a laser Pain fMRI study. PLoS ONE 11:e0164607. https://doi.org/10.1371/journal.pone.0164607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Measso G, Cavarzeran F, Zappalà G et al (1993) The mini-mental state examination: normative study of an Italian random sample. Dev Neuropsychol 9:77–85. https://doi.org/10.1080/87565649109540545

    Article  Google Scholar 

  27. Orsini A, Grossi D, Capitani E et al (1987) Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. Ital J Neurol Sci 8:537–548. https://doi.org/10.1007/BF02333660

    Article  Google Scholar 

  28. Spinnler H, Tognoni G (1987) Gruppo italiano per lo studio neuropsicologico dell’invecchiamento. Standardizzazione e taratura italiana di Test Neuropsicologici. Ital J Neurol Sci 12:461–466. https://doi.org/10.1136/emj.2008.070474

    Article  Google Scholar 

  29. Shamosh NA, Gray JR (2008) Delay discounting and intelligence: a meta-analysis. Intelligence 36:289–305

    Article  Google Scholar 

  30. Costantini M, Musso M, Viterbori P et al (1999) Detecting psychological distress in cancer patients: validity of the Italian version of the hospital anxiety and depression scale. Support Care Cancer 7:121–127. https://doi.org/10.1007/s005209900026

    Article  CAS  PubMed  Google Scholar 

  31. Kapur S, Mizrahi R, Li M (2005) From dopamine to salience to psychosis-linking biology, pharmacology and phenomenology of psychosis. Schizophr Res 79(1):59–68

    Article  Google Scholar 

  32. Sienkiewicz-Jarosz H, Scinska A, Swiecicki L et al (2013) Sweet liking in patients with Parkinson’s disease. J Neurol Sci 329:17–22. https://doi.org/10.1016/j.jns.2013.03.005

    Article  PubMed  Google Scholar 

  33. Loas G, Duru C, Godefroy O, Krystkowiak P (2014) Hedonic deficits in Parkinson’s disease: is consummatory anhedonia specific? Front Neurol. https://doi.org/10.3389/fneur.2014.00024

    Article  PubMed  PubMed Central  Google Scholar 

  34. Spalletta G, Fagioli S, Meco G et al (2013) Hedonic tone and its mood and cognitive correlates in Parkinson’s disease. Depress Anxiety 30:85–91. https://doi.org/10.1002/da.22036

    Article  PubMed  Google Scholar 

  35. Pettorruso M, Spagnolo PA, Leggio L et al (2018) Repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex may improve symptoms of anhedonia in individuals with cocaine use disorder: a pilot study. Brain Stimul 11(5):1195–1197

    Article  Google Scholar 

  36. Song S, Zilverstand A, Gui W et al (2019) Effects of single-session versus multi-session non-invasive brain stimulation on craving and consumption in individuals with drug addiction, eating disorders or obesity: a meta-analysis. Brain Stimul 12(3):606–618

    Article  Google Scholar 

  37. Kekic M, McClelland J, Campbell I et al (2014) The effects of prefrontal cortex transcranial direct current stimulation (tDCS) on food craving and temporal discounting in women with frequent food cravings. Appetite. https://doi.org/10.1016/j.appet.2014.03.010

    Article  PubMed  Google Scholar 

  38. Castrellon JJ, Meade J, Greenwald L et al (2021) Dopaminergic modulation of reward discounting in healthy rats: a systematic review and meta-analysis. Psychopharmacology. https://doi.org/10.1007/s00213-020-05723-5

    Article  PubMed  Google Scholar 

  39. Girard R, Obeso I, Thobois S et al (2019) Wait and you shall see: sexual delay discounting in hypersexual Parkinson’s disease. Brain. https://doi.org/10.1093/brain/awy298

    Article  PubMed  Google Scholar 

  40. Simioni AC, Dagher A, Fellows LK (2012) Dissecting the effects of disease and treatment on impulsivity in Parkinson’s disease. J Internat Neuropsychol Soc 18(6):942–951

    Article  Google Scholar 

  41. Minarik T, Berger B, Althaus L et al (2016) The importance of sample size for reproducibility of tDCS effects. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2016.00453

    Article  PubMed  PubMed Central  Google Scholar 

  42. Foroni F, Pergola G, Argiris G, Rumiati RI (2013) The FoodCast research image database (FRIDa). Front Hum Neurosci 7:51. https://doi.org/10.3389/fnhum.2013.00051

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the participants for the time they gave to participate in this study.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Area of Neuroscience, SISSA, Via Bonomea, 265, Trieste, TS, Italy

    Damiano Terenzi, Raffaella I. Rumiati & Marilena Aiello

  2. Department of Decision Neuroscience and Nutrition, German Institute of Human Nutrition, Potsdam Rehbrücke, Nuthetal, Germany

    Damiano Terenzi

  3. Berlin Institute of Health, Neuroscience Research Center, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität Zu Berlin, Berlin, Germany

    Damiano Terenzi

  4. Deutsches Zentrum Für Diabetes, Neuherberg, Germany

    Damiano Terenzi

  5. Clinical Unit of Neurology, Department of Medical Sciences, University Hospital and Health Services of Trieste, University of Trieste, Trieste, Italy

    Mauro Catalan, Paola Polverino, Claudio Bertolotti & Paolo Manganotti

  6. SSAS – Scuola superiore di Studi Avanzati Sapienza, Rome, Italy

    Raffaella I. Rumiati

Authors
  1. Damiano Terenzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mauro Catalan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paola Polverino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claudio Bertolotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paolo Manganotti
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Raffaella I. Rumiati
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marilena Aiello
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DT: conceptualization, methodology, investigation, data curation, formal analysis, and writing original draft; MC: organization of research project, review and critique; PP: organization of research project; CB: organization of research project; PM: review and critique; RIR: review and critique; MA: conceptualization, methodology, formal analysis, writing original draft, review and critique. All the authors have approved the final article.

Corresponding author

Correspondence to Marilena Aiello.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Ethics approval

The study was approved by SISSA Ethics Committee. The study was performed in line with the principles of the 1964 Helsinki Declaration.

Consent to participate

All the participants gave written informed consent to participate in the study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 69 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Terenzi, D., Catalan, M., Polverino, P. et al. Effects of tDCS on reward responsiveness and valuation in Parkinson’s patients with impulse control disorders. J Neurol 269, 1557–1565 (2022). https://doi.org/10.1007/s00415-021-10733-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-021-10733-0

Keywords

Search

Navigation