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Deep brain stimulation of the subthalamic nucleus modulates reward processing and action selection in Parkinson patients

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Abstract

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is an effective treatment for motor impairments in Parkinson’s disease (PD) but its effect on the motivational regulation of action control is still not fully understood. We investigated whether DBS of the STN influences the ability of PD patients to act for anticipated reward or loss, or whether DBS improves action execution independent of motivational valence. 16 PD patients (12 male, mean age = 58.5 ± 10.17 years) treated with bilateral STN-DBS and an age- and gender-matched group of healthy controls (HC) performed a go/no-go task whose contingencies explicitly decouple valence and action. Patients were tested with (ON) and without (OFF) active STN stimulation. For HC, there was a benefit in performing rewarded actions when compared to actions that avoided punishment. PD patients showed such a benefit reliably only when STN stimulation was ON. In fact, the relative behavioral benefit for go for reward over go to avoid losing was stronger in the PD patients under DBS ON than in HC. In PD patients, rather than generally improving motor functions independent of motivational valence, modulation of the STN by DBS improves action execution specifically when rewards are anticipated. Thus, STN-DBS establishes a reliable congruency between action and reward (“Pavlovian congruency”) and remarkably enhances it over the level observed in HC.

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Acknowledgments

This work was funded by DFG-SFB 779/TPA 2 (T.Z., H.-J.H. and ED), TPA 3 (H.-J.H.) TPA 7 (ED) and TP A11 (J.V. and H.-J.H.), and DFG He 1531/11-1 (J.V. and H.-J.H.).

Conflicts of interest

CW & TZ report no disclosure. IG received honoraria for speaking from GlaxoSmithKline, TEVA pharma, Medronic and St. Jude Medical. JV is member of the Medtronic Inc. advisory board and receives occasionally honoraria. MGM reports no disclosure. HJH reports no disclosure. ED reports no disclosure.

Ethical standard

This study has been approved by the local ethics committee (University of Magdeburg, Germany) and has been performed in accordance with the ethical standards of the 1964 Declaration of Helsinki.

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    Authors and Affiliations

    1. Departments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University Magdeburg, 39120, Magdeburg, Germany

      Caroline Wagenbreth, Tino Zaehle, Imke Galazky, Jürgen Voges & Hans-Jochen Heinze

    2. Department of Behavioral Neurology, Leibniz Institute of Neurobiology, Magdeburg, Germany

      Jürgen Voges & Hans-Jochen Heinze

    3. Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London, WC1N 3BG, UK

      Marc Guitart-Masip

    4. Ageing Research Centre, Karolinska Institute, SE-11330, Stockholm, Sweden

      Marc Guitart-Masip

    5. Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke-University Magdeburg, Magdeburg, Germany

      Emrah Düzel

    6. German Center for Neurodegenerative Diseases (DZNE), Site Magdeburg, Magdeburg, Germany

      Emrah Düzel

    7. Center for Behavioral and Brain Sciences, CBBS, Magdeburg, Germany

      Emrah Düzel

    Authors
    1. Caroline Wagenbreth
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    2. Tino Zaehle
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    5. Marc Guitart-Masip
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    Correspondence to Tino Zaehle.

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    C. Wagenbreth and T. Zaehle contributed equally.

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    Wagenbreth, C., Zaehle, T., Galazky, I. et al. Deep brain stimulation of the subthalamic nucleus modulates reward processing and action selection in Parkinson patients. J Neurol 262, 1541–1547 (2015). https://doi.org/10.1007/s00415-015-7749-9

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    • DOI: https://doi.org/10.1007/s00415-015-7749-9

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