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Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold

Abstract

It takes effort and time to tame one's impulses. Although medial prefrontal cortex (mPFC) is broadly implicated in effortful control over behavior, the subthalamic nucleus (STN) is specifically thought to contribute by acting as a brake on cortico-striatal function during decision conflict, buying time until the right decision can be made. Using the drift diffusion model of decision making, we found that trial-to-trial increases in mPFC activity (EEG theta power, 4–8 Hz) were related to an increased threshold for evidence accumulation (decision threshold) as a function of conflict. Deep brain stimulation of the STN in individuals with Parkinson's disease reversed this relationship, resulting in impulsive choice. In addition, intracranial recordings of the STN area revealed increased activity (2.5–5 Hz) during these same high-conflict decisions. Activity in these slow frequency bands may reflect a neural substrate for cortico–basal ganglia communication regulating decision processes.

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Figure 1: Theoretical model, task and performance.
Figure 2: DBS ON/OFF study: scalp EEG (FCz electrode) from the test phase split by high and low conflict.
Figure 3: DBS ON/OFF study: Bayesian posterior densities of decision thresholds estimated from the drift diffusion model (ordinates) and how they varied as a function of mPFC theta (abcissa).
Figure 4: Intracranial EEG from the STN for dorsal, middle and ventral leads.

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Acknowledgements

The authors express their gratitude to T. Norton and his surgical staff for their support during the intraoperative recording sessions, L. Trujillo for a review of permutation methods, E.J. Wagenmakers for consultation on Bayesian data analysis, J.J.B. Allen and E.F. Martino for laboratory resources that facilitated some data acquisition and analyses, and K. Carlisle for help with subject recruitment. This project was funded by a grant from the Michael J. Fox Foundation to M.J.F.

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Authors

Contributions

M.J.F., J.F.C. and M.X C. designed the experiments. J.F.C., C.M.F., J.S. and S.J.S. recruited and ran participants. J.F.C. and M.X C. processed the EEG data. T.V.W. and M.J.F. designed the computational models. J.F.C. and M.J.F. wrote the manuscript.

Corresponding authors

Correspondence to James F Cavanagh or Michael J Frank.

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The authors declare no competing financial interests.

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Supplementary Figures 1–7, Supplementary Tables 1–5, Supplementary Results and Supplementary Discussion (PDF 581 kb)

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Cavanagh, J., Wiecki, T., Cohen, M. et al. Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nat Neurosci 14, 1462–1467 (2011). https://doi.org/10.1038/nn.2925

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