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Bilateral stimulation of the subthalamic nucleus has differential effects on reactive and proactive inhibition and conflict-induced slowing in Parkinson’s disease

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Abstract

It has been proposed that the subthalamic nucleus (STN) mediates response inhibition and conflict resolution through the fronto-basal ganglia pathways. Our aim was to compare the effects of deep brain stimulation (DBS) of the STN on reactive and proactive inhibition and conflict resolution in Parkinson’s disease using a single task. We used the conditional Stop signal reaction time task that provides the Stop signal reaction time (SSRT) as a measure of reactive inhibition, the response delay effect (RDE) as a measure of proactive inhibition and conflict-induced slowing (CIS) as a measure of conflict resolution. DBS of the STN significantly prolonged SSRT relative to stimulation off. However, while the RDE measure of proactive inhibition was not significantly altered by DBS of the STN, relative to healthy controls, RDE was significantly lower with DBS off but not DBS on. DBS of the STN did not alter the mean CIS but produced a significant differential effect on the slowest and fastest RTs on conflict trials, further prolonging the slowest RTs on the conflict trials relative to DBS off and to controls. These results are the first demonstration, using a single task in the same patient sample, that DBS of the STN produces differential effects on reactive and proactive inhibition and on conflict resolution, suggesting that these effects are likely to be mediated through the impact of STN stimulation on different fronto-basal ganglia pathways: hyperdirect, direct and indirect.

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Acknowledgments

We are grateful to all the participants. This research was supported by a PhD studentship from Fundación Caja Madrid, Spain (IO), and a Post-doctoral Career Development Fellowship from Parkinson’s UK (LW).

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Author notes

  1. Ignacio Obeso

    Present address: Reward and Decision-Making Group, Centre de Neurosciences Cognitives, Centre National pour la Recherche Scientifique, Lyon, France

  2. Leonora Wilkinson

    Present address: Brain Stimulation Unit, National Institute of Neurological Disorders and Stroke, Bethesda, MD, 20892-1430, USA

  3. Maria-Cruz Rodríguez-Oroz

    Present address: Department of Neurology, University Hospital Donostia and Neuroscience Unit, BioDonostia Research Institute, 20014 San Sebastian, Ikerbasque, Basque Foundation for Science, Bilbao, Spain

Authors and Affiliations

  1. Sobell Department of Motor Neuroscience and Movement Disorders, UCL, Institute of Neurology, The National Hospital for Neurology and Neurosurgery, 33 Queen Square, London, WC1N 3BG, UK

    Ignacio Obeso, Leonora Wilkinson & Marjan Jahanshahi

  2. Department of Neurology, Clínica Universitaria and Medical School of Navarra, Neuroscience Centre, CIMA, University of Navarra, Pamplona, Spain

    Maria-Cruz Rodríguez-Oroz & Jose A. Obeso

  3. Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Instituto Carlos III, Ministerio de Investigación y Ciencias, Madrid, Spain

    Maria-Cruz Rodríguez-Oroz & Jose A. Obeso

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  1. Ignacio Obeso
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  2. Leonora Wilkinson
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  3. Maria-Cruz Rodríguez-Oroz
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Correspondence to Marjan Jahanshahi.

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Obeso, I., Wilkinson, L., Rodríguez-Oroz, MC. et al. Bilateral stimulation of the subthalamic nucleus has differential effects on reactive and proactive inhibition and conflict-induced slowing in Parkinson’s disease. Exp Brain Res 226, 451–462 (2013). https://doi.org/10.1007/s00221-013-3457-9

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  • DOI: https://doi.org/10.1007/s00221-013-3457-9

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