Advertisement

Journal of Neurology

, Volume 266, Issue 5, pp 1113–1119 | Cite as

Deep brain stimulation of the subthalamic nucleus and the temporal discounting of primary and secondary rewards

  • M. AielloEmail author
  • D. Terenzi
  • G. Furlanis
  • M. Catalan
  • P. Manganotti
  • R. Eleopra
  • E. Belgrado
  • R. I. Rumiati
Original Communication

Abstract

Although deep brain stimulation of the subthalamic nucleus is an effective surgical treatment for Parkinson’s disease, it may expose patients to non-motor side effects such as increased impulsivity and changes in decision-making behavior. Even if several studies have shown that stimulation of the subthalamic nucleus increases the incentive salience of food rewards in both humans and animals, temporal discounting for food rewards has never been investigated in patients who underwent STN-DBS. In this study, we measured inter-temporal choice after STN-DBS, using both primary and secondary rewards. In particular, PD patients who underwent STN-DBS (in ON medication/ON stimulation), PD patients without STN-DBS (in ON medication) and healthy matched controls (C) performed three temporal discounting tasks with food (primary reward), money and discount vouchers (secondary rewards). Participants performed also neuropsychological tests assessing memory and executive functions. Our results show that STN-DBS patients and PD without DBS behave as healthy controls. Even PD patients who after DBS experienced weight gain and/or eating alterations did not show an increased temporal discounting for food rewards. Interestingly, patients taking a higher dosage of dopaminergic medications, fewer years from DBS surgery and, unexpectedly, with better episodic memory were also those who discounted rewards more. In conclusion, this study shows that STN-DBS does not affect temporal discounting of primary and secondary rewards. Furthermore, by revealing interesting correlations between clinical measures and temporal discounting, it also shed light on the clinical outcomes that follow STN-DBS in patients with PD.

Keywords

Parkinson’s disease Temporal discounting Food reward Deep brain stimulation Subthalamic nucleus 

Notes

Compliance with ethical standards

Conflicts of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standards

All participants gave written informed consent to participate in the study that was approved by SISSA Ethics Committee and has, therefore, been performed in accordance with the ethical standards of the Declaration of Helsinki.

References

  1. 1.
    Castrioto A, Lhommée E, Moro E, Krack P (2014) Mood and behavioural effects of subthalamic stimulation in Parkinson’s disease. Lancet Neurol 13:287–305.  https://doi.org/10.1016/S1474-4422(13)70294-1 CrossRefPubMedGoogle Scholar
  2. 2.
    Okun MS, Fernandez HH, Wu SS et al (2009) Cognition and mood in Parkinson disease in STN versus GPi DBS: the COMPARE trial. Ann Neurol 65:586–595.  https://doi.org/10.1002/ana.21596 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Aiello M, Eleopra R, Lettieri C et al (2014) Emotion recognition in Parkinson’s disease after subthalamic deep brain stimulation: differential effects of microlesion and STN stimulation. Cortex 51:35–45.  https://doi.org/10.1016/j.cortex.2013.11.003 CrossRefPubMedGoogle Scholar
  4. 4.
    Tröster AI, Jankovic J, Tagliati M et al (2017) Neuropsychological outcomes from constant current deep brain stimulation for Parkinson’s disease. Mov Disord 32:433–440.  https://doi.org/10.1002/mds.26827 CrossRefPubMedGoogle Scholar
  5. 5.
    Jahanshahi M, Obeso I, Baunez C et al (2015) Parkinson’s disease, the subthalamic nucleus, inhibition, and impulsivity. Mov Disord 30:128–140.  https://doi.org/10.1002/mds.26049 CrossRefPubMedGoogle Scholar
  6. 6.
    Kjær SW (2018) A systematic review of decision-making impairments in Parkinson’s Disease: dopaminergic medication and methodological variability. Basal Ganglia 14:31–40.  https://doi.org/10.1016/j.baga.2018.07.003 CrossRefGoogle Scholar
  7. 7.
    Pham U, Solbakk A-K, Skogseid I-M et al (2015) Personality changes after deep brain stimulation in Parkinson’s disease. Parkinsons Dis. https://www.hindawi.com/journals/pd/2015/490507/abs/. Accessed 2015
  8. 8.
    Kirby KN, Herrnstein RJ (1995) Preference reversals due to myopic discounting of delayed reward. Psychol Sci 6:83–89.  https://doi.org/10.1111/j.1467-9280.1995.tb00311.x CrossRefGoogle Scholar
  9. 9.
    Evens R, Stankevich Y, Dshemuchadse M et al (2015) The impact of Parkinson’s disease and subthalamic deep brain stimulation on reward processing. Neuropsychologia 75:11–19.  https://doi.org/10.1016/j.neuropsychologia.2015.05.005 CrossRefPubMedGoogle Scholar
  10. 10.
    Seymour B, Barbe M, Dayan P et al (2016) Deep brain stimulation of the subthalamic nucleus modulates sensitivity to decision outcome value in Parkinson’s disease. Sci Rep 6:32509.  https://doi.org/10.1038/srep32509 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Seinstra M, Wojtecki L, Storzer L et al (2016) No effect of subthalamic deep brain stimulation on intertemporal decision-making in Parkinson patients. eNeuro.  https://doi.org/10.1523/ENEURO.0019-16.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Uslaner JM, Yang P, Robinson TE (2005) Subthalamic nucleus lesions enhance the psychomotor-activating, incentive motivational, and neurobiological effects of cocaine. J Neurosci 25:8407–8415.  https://doi.org/10.1523/JNEUROSCI.1910-05.2005 CrossRefPubMedGoogle Scholar
  13. 13.
    Serranová T, Jech R, Dušek P et al (2011) Subthalamic nucleus stimulation affects incentive salience attribution in Parkinson’s disease. Mov Disord 26:2260–2266.  https://doi.org/10.1002/mds.23880 CrossRefPubMedGoogle Scholar
  14. 14.
    Serranová T, Sieger T, Dušek P et al (2013) Sex, food and threat: startling changes after subthalamic stimulation in Parkinson’s disease. Brain Stimulation 6:740–745.  https://doi.org/10.1016/j.brs.2013.03.009 CrossRefPubMedGoogle Scholar
  15. 15.
    Aiello M, Eleopra R, Foroni F et al (2017) Weight gain after STN-DBS: the role of reward sensitivity and impulsivity. Cortex 92:150–161.  https://doi.org/10.1016/j.cortex.2017.04.005 CrossRefPubMedGoogle Scholar
  16. 16.
    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 CrossRefGoogle Scholar
  17. 17.
    Appollonio I, Leone M, Isella V et al (2005) The Frontal Assessment Battery (FAB): normative values in an Italian population sample. Neurol Sci 26:108–116.  https://doi.org/10.1007/s10072-005-0443-4 CrossRefGoogle Scholar
  18. 18.
    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 Neuro Sci 8:537–548.  https://doi.org/10.1007/BF02333660 CrossRefGoogle Scholar
  19. 19.
    Novelli G, Papagno C, Capitani E et al (1986) Tre test clinici di ricerca e produzione lessicale. Taratura su sogetti normali. [Three clinical tests to research and rate the lexical performance of normal subjects.]. Arch Psicol Neurol Psichiatria 47:477–506Google Scholar
  20. 20.
    Carlesimo GA, Caltagirone C, Gainotti G et al (1996) The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. Eur Neurol 36:378–384CrossRefGoogle Scholar
  21. 21.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Smith CL, Hantula DA (2008) Methodological considerations in the study of delay discounting in intertemporal choice: a comparison of tasks and modes. Behav Res Methods 40:940–953.  https://doi.org/10.3758/BRM.40.4.940 CrossRefPubMedGoogle Scholar
  23. 23.
    Baunez C, Dias C, Cador M, Amalric M (2005) The subthalamic nucleus exerts opposite control on cocaine and `natural’ rewards. Nat Neurosci 8:484–489.  https://doi.org/10.1038/nn1429 CrossRefPubMedGoogle Scholar
  24. 24.
    Rouaud T, Lardeux S, Panayotis N et al (2010) Reducing the desire for cocaine with subthalamic nucleus deep brain stimulation. Proc Natl Acad Sci USA 107:1196–1200.  https://doi.org/10.1073/pnas.0908189107 CrossRefPubMedGoogle Scholar
  25. 25.
    Aiello M, Eleopra R, Rumiati RI (2015) Body weight and food intake in Parkinson’s disease. A review of the association to non-motor symptoms. Appetite 84:204–211.  https://doi.org/10.1016/j.appet.2014.10.011 CrossRefPubMedGoogle Scholar
  26. 26.
    Moeller FG, Barratt ES, Dougherty DM et al (2001) Psychiatric aspects of impulsivity. Am J Psychiatry 158:1783–1793.  https://doi.org/10.1176/appi.ajp.158.11.1783 CrossRefGoogle Scholar
  27. 27.
    Witt K (2017) Chap. 25—The subthalamic nucleus in impulsivity. In: Dreher J-C, Tremblay L (eds) Decision neuroscience. Academic Press, San Diego, pp 315–325CrossRefGoogle Scholar
  28. 28.
    Broos N, Schmaal L, Wiskerke J et al (2012) The relationship between impulsive choice and impulsive action: a cross-species translational study. PLOS One 7:e36781.  https://doi.org/10.1371/journal.pone.0036781 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Abbes M, Lhommée E, Thobois S et al (2018) Subthalamic stimulation and neuropsychiatric symptoms in Parkinson’s disease: results from a long-term follow-up cohort study. J Neurol Neurosurg Psychiatry 89:836–843.  https://doi.org/10.1136/jnnp-2017-316373 CrossRefPubMedGoogle Scholar
  30. 30.
    Pine A, Shiner T, Seymour B, Dolan RJ (2010) Dopamine, time, and impulsivity in humans. J Neurosci 30:8888–8896.  https://doi.org/10.1523/JNEUROSCI.6028-09.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Bobova L, Finn PR, Rickert ME, Lucas J (2009) Disinhibitory psychopathology and delay discounting in alcohol dependence: personality and cognitive correlates. Exp Clin Psychopharmacol 17:51–61.  https://doi.org/10.1037/a0014503 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Shamosh NA, DeYoung CG, Green AE et al (2008) Individual differences in delay discounting: relation to intelligence, working memory, and anterior prefrontal cortex. Psychol Sci 19:904–911CrossRefGoogle Scholar
  33. 33.
    Heerey EA, Robinson BM, McMahon RR, Gold JM (2007) Delay discounting in schizophrenia. Cognitive Neuropsychiatry 12:213–221.  https://doi.org/10.1080/13546800601005900 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Hendrickson KL, Rasmussen EB (2017) Mindful eating reduces impulsive food choice in adolescents and adults. Health Psychol 36:226–235.  https://doi.org/10.1037/hea0000440 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Area of NeuroscienceSISSATriesteItaly
  2. 2.Azienda Ospedaliero-Universitaria “Ospedali Riuniti” of TriesteTriesteItaly
  3. 3.Fondazione IRCCS Istituto Neurologico Carlo BestaMilanItaly
  4. 4.S.O.C. NeurologiaAzienda Ospedaliero UniversitariaUdineItaly
  5. 5.ANVURRomaItaly

Personalised recommendations