Subthalamic Nucleus Deep Brain Stimulation Alters Prefrontal Correlates of Emotion Induction

doi:10.1111/ner.12537

Neuromodulation: Technology at the Neural Interface

Volume 20, Issue 3, April 2017, Pages 233-237

https://doi.org/10.1111/ner.12537 Get rights and content

Objectives

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) improves motor symptoms in advanced Parkinson’s disease. STN DBS may also affect emotion, possibly by impacting a parallel limbic cortico-striatal circuit. The objective of this study was to investigate changes in prefrontal cortical activity related to DBS during an emotion induction task.

Materials and Methods

We used near infrared spectroscopy to monitor prefrontal cortex hemodynamic changes during an emotion induction task. Seven DBS patients were tested sequentially in the stimulation-on and stimulation-off states while on dopaminergic medication. Patients watched a series of positive, negative, and neutral videos. The general linear model was used to compare prefrontal oxygenated hemoglobin concentration between DBS states.

Results

Deep brain stimulation was correlated with prefrontal oxygenated hemoglobin changes relative to the stimulation off state in response to both positive and negative videos. These changes were specific to emotional stimuli and were not seen during neutral stimuli.

Conclusions

These results suggest that STN stimulation influences the prefrontal cortical representation of positive and negative emotion induction.

Section snippets

INTRODUCTION

Deep brain stimulation (DBS) of the bilateral subthalamic nuclei (STN) is an effective and accepted treatment for advanced Parkinson’s disease (PD) (1). However, a growing body of evidence demonstrates clinically significant emotional disturbances following DBS surgery (2). In addition to improving motor symptoms of Parkinson’s disease, STN DBS may alter emotion processing, impairing emotion recognition (3., 4., 5.), altering emotion induction (6., 7., 8.), and affect mood and depression

Participants

Participants were recruited from a randomized controlled study of DBS in early PD (FDA Investigational Device Exemption G050016, ClinicalTrials.gov NCT00282152) and had been implanted with bilateral STN DBS (17). Participants in this study had been treated with medication for between six months and four years at the time of the study and were classified as Hoehn and Yahr stage II off medication. The Vanderbilt Institutional Review Board approved our study (071210). Participants provided written

Participants

There were seven participants, one woman, and six men. Demographic and clinical variables are presented in Table 1.

Neuropsychological tests were within normal ranges (Table 1). In particular, BDI-II scores fell within the minimal depression range of 0–13. The Profile of Mood States total mood disturbance score was 60.7 in the DBSon condition and 66.7 in the DBSoff condition (p = 0.43, student’s t-test), suggesting that there was no difference in mood state prior to emotion induction task in the

DISCUSSION

We show that STN stimulation alters prefrontal hemodynamics during an emotion induction task but not during emotionally neutral stimuli. These findings suggest that STN DBS alters limbic circuits and prefrontal activity specifically during emotion induction.

These findings support a role for the STN in limbic circuitry. The STN has sensorimotor, associative, and limbic subdivisions whose borders are not sharply demarcated (11). The STN is a subcentimeter structure, and spread of current from

CONCLUSION

In this study, we show that STN stimulation is correlated with unique patterns of changes in prefrontal metabolism in PD patients during an emotion induction task. This finding has important implications for the changes in emotion recognition and experience reported in PD patients treated with STN DBS. Additional study may help to further describe the mechanism of these findings.

Authorship Statements

Dr. Bick designed and conducted the study. She was responsible for data collection, analysis, and interpretation, and drafted the paper. Dr. Folley participated in study design and data analysis. Dr. Mayer participated in data collection and analysis. Dr. Park assisted with study design and provided expertise in the collection and analysis of NIRS data. Dr. Charles assisted with patient recruitment, study oversight, and manuscript preparation. Dr. Camalier contributed to data analysis and

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For more information on author guidelines, an explanation of our peer review process, and conflict of interest informed consent policies, please go to http://www.wiley.com/WileyCDA/Section/id-301854.html

Source(s) of financial support: The study was funded by a National Institutes of Health R21 grant (grant number R21NS070136-02). Funding from NIH grants RO1 EB006136 and RO1 NS095291 09 also contributed to the project.

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Invasive Brain StimulationSubthalamic Nucleus Deep Brain Stimulation Alters Prefrontal Correlates of Emotion Induction

Objectives

Materials and Methods

Results

Conclusions

Section snippets

INTRODUCTION

Participants

Participants

DISCUSSION

CONCLUSION

Authorship Statements

Parkinsonism Relat Disord

Neuropsychologia

Neuropsychologia

Neuropsychologia

Brain Res Brain Res Rev

Parkinsonism Relat Disord

Neuroimage

Biol Psychiatry

Neurosci Lett

Neuropsychologia

Neuropsychologia

Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease

N Engl J Med

Subthalamic nucleus stimulation induces deficits in decoding emotional facial expressions in Parkinson’s disease

J Neurol Neurosurg Psychiatry

Deep brain stimulation of the subthalamic nucleus enhances emotional processing in Parkinson disease

Arch Gen Psychiatry

Effect on mood of subthalamic DBS for Parkinson’s disease: a consecutive series of 24 patients

Neurology

Pallidal versus subthalamic deep-brain stimulation for Parkinson’s disease

N Engl J Med

Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior

Proc Natl Acad Sci U S A

Invasive Brain Stimulation
Subthalamic Nucleus Deep Brain Stimulation Alters Prefrontal Correlates of Emotion Induction