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The effects of unilateral versus bilateral subthalamic nucleus deep brain stimulation on prosaccades and antisaccades in Parkinson’s disease

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Abstract

Unilateral deep brain stimulation (DBS) of the subthalamic nucleus (STN) in patients with Parkinson’s disease improves skeletomotor function assessed clinically, and bilateral STN DBS improves motor function to a significantly greater extent. It is unknown whether unilateral STN DBS improves oculomotor function and whether bilateral STN DBS improves it to a greater extent. Further, it has also been shown that bilateral, but not unilateral, STN DBS is associated with some impaired cognitive-motor functions. The current study compared the effect of unilateral and bilateral STN DBS on sensorimotor and cognitive aspects of oculomotor control. Patients performed prosaccade and antisaccade tasks during no stimulation, unilateral stimulation, and bilateral stimulation. There were three sets of findings. First, for the prosaccade task, unilateral STN DBS had no effect on prosaccade latency and it reduced prosaccade gain; bilateral STN DBS reduced prosaccade latency and increased prosaccade gain. Second, for the antisaccade task, neither unilateral nor bilateral stimulation had an effect on antisaccade latency, unilateral STN DBS increased antisaccade gain, and bilateral STN DBS increased antisaccade gain to a greater extent. Third, bilateral STN DBS induced an increase in prosaccade errors in the antisaccade task. These findings suggest that while bilateral STN DBS benefits spatiotemporal aspects of oculomotor control, it may not be as beneficial for more complex cognitive aspects of oculomotor control. Our findings are discussed considering the strategic role the STN plays in modulating information in the basal ganglia oculomotor circuit.

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Abbreviations

BOTH:

Bilateral stimulation condition

DBS:

Deep brain stimulation

DLPFC:

Dorsolateral prefrontal cortex

LEFT:

Left unilateral stimulation on condition

MDS-UPDRS:

Movement Disorder Society-Unified Parkinson’s Disease Rating Scale

OFF:

Stimulators off condition

PD:

Parkinson’s disease

RIGHT:

Right unilateral stimulation on condition

SNr:

Substantia nigra pars reticulata

STN:

Subthalamic nucleus

UNI:

Unilateral stimulation

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Acknowledgements

This study was supported by NIH (R56NS040902). The sponsors were not involved in the design, conduct, collection, management, analysis, and/or interpretation of the study results and preparation, review, or approval of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of NIH.

Funding

LCG has no financial disclosures. FJD received grant support from NIH. JAS received grant support from NIH and has consulted to Takeda Pharmaceuticals. DEV received grant support from the NIH, Tyler’s Hope Foundation, Bachmann Straus Foundation, and is Co-Founder and Manager of Neuroimaging Solutions. HP received grant support from NIH, NSF, and ONR. LVM received grant support from NIH, Michael J. Fox, PDF, and contracts for clinical trials from Boston Scientific, Medtronic, Adamas, Osmotica, USWorldMeds. DMC received grant support from NIH and Michael J. Fox, and receives lecture, honoraria, and reviewer fees from NIH.

Author contributions

LCG was responsible for study concept and design, acquisition of data, analysis and interpretation of the data, statistical analysis, drafting the manuscript, and administrative, technical, or material support. FJD was responsible for study concept and design, obtaining funding, acquisition of data, analysis and interpretation of the data, statistical analysis, drafting the manuscript, and administrative, technical, or material support. JAS was responsible for study concept and design, analysis and interpretation of the data, critical revision of the manuscript for important intellectual content, and administrative, technical, or material support. DEV and HP were responsible for study concept and design, obtaining funding, interpretation of the data, critical revision of the manuscript for important intellectual content, and administrative, technical, or material support. LVM was responsible for patient recruitment, study concept and design, obtaining funding, study supervision, interpretation of the data, critical revision of the manuscript for important intellectual content, and administrative, technical, or material support. DMC was responsible for study concept and design, obtaining funding, interpretation of the data, critical revision of the manuscript for important intellectual content, study supervision, and administrative, technical, or material support.

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Authors and Affiliations

  1. Department of Kinesiology and Nutrition, University of Illinois, 901 West Roosevelt, Chicago, IL, 60612, USA

    Lisa C. Goelz

  2. Department of Physical Therapy and Human Movement Sciences, Northwestern University, Chicago, IL, USA

    Lisa C. Goelz, Fabian J. David & Daniel M. Corcos

  3. Department of Psychiatry and Behavioral Neuroscience, University of Cincinnati, Cincinnati, OH, USA

    John A. Sweeney

  4. Departments of Applied Physiology and Kinesiology, Biomedical Engineering, and Neurology, University of Florida, Gainesville, FL, USA

    David E. Vaillancourt

  5. Institute for Neural Computation, University of California, San Diego, CA, USA

    Howard Poizner

  6. Department of Neurological Sciences, Section of Parkinson Disease and Movement Disorders, Rush University Medical Center, Chicago, IL, USA

    Leonard Verhagen Metman

  7. Department of Neurological Sciences, Rush University Medical Center, Chicago, IL, USA

    Daniel M. Corcos

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  1. Lisa C. Goelz
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  2. Fabian J. David
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Correspondence to Lisa C. Goelz.

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Goelz, L.C., David, F.J., Sweeney, J.A. et al. The effects of unilateral versus bilateral subthalamic nucleus deep brain stimulation on prosaccades and antisaccades in Parkinson’s disease. Exp Brain Res 235, 615–626 (2017). https://doi.org/10.1007/s00221-016-4830-2

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