Neural Correlates of Decision Thresholds in the Human Subthalamic Nucleus

Abstract

If humans are faced with difficult choices when making decisions, the ability to slow down responses becomes critical in order to avoid suboptimal choices. Current models of decision making assume that the subthalamic nucleus (STN) mediates this function by elevating decision thresholds, thereby requiring more evidence to be accumulated before responding [1Bogacz R. Gurney K. The basal ganglia and cortex implement optimal decision making between alternative actions.Neural Comput. 2007; 19: 442-477Crossref PubMed Scopus (282) Google Scholar, 2Cavanagh J.F. Wiecki T.V. Cohen M.X. Figueroa C.M. Samanta J. Sherman S.J. Frank M.J. Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold.Nat. Neurosci. 2011; 14: 1462-1467Crossref PubMed Scopus (407) Google Scholar, 3Frank M.J. Gagne C. Nyhus E. Masters S. Wiecki T.V. Cavanagh J.F. Badre D. fMRI and EEG predictors of dynamic decision parameters during human reinforcement learning.J. Neurosci. 2015; 35: 485-494Crossref PubMed Scopus (149) Google Scholar, 4Frank M.J. Samanta J. Moustafa A.A. Sherman S.J. Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism.Science. 2007; 318: 1309-1312Crossref PubMed Scopus (809) Google Scholar, 5Green N. Bogacz R. Huebl J. Beyer A.K. Kühn A.A. Heekeren H.R. Reduction of influence of task difficulty on perceptual decision making by STN deep brain stimulation.Curr. Biol. 2013; 23: 1681-1684Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar, 6Mansfield E.L. Karayanidis F. Jamadar S. Heathcote A. Forstmann B.U. Adjustments of response threshold during task switching: a model-based functional magnetic resonance imaging study.J. Neurosci. 2011; 31: 14688-14692Crossref PubMed Scopus (77) Google Scholar, 7Richard Ridderinkhof K. Forstmann B.U. Wylie S.A. Burle B. van den Wildenberg W.P.M. Neurocognitive mechanisms of action control: resisting the call of the Sirens.Wiley Interdiscip. Rev. Cogn. Sci. 2011; 2: 174-192Crossref PubMed Scopus (159) Google Scholar, 8Wei W. Rubin J.E. Wang X.J. Role of the indirect pathway of the basal ganglia in perceptual decision making.J. Neurosci. 2015; 35: 4052-4064Crossref PubMed Scopus (48) Google Scholar, 9Wiecki T.V. Frank M.J. A computational model of inhibitory control in frontal cortex and basal ganglia.Psychol. Rev. 2013; 120: 329-355Crossref PubMed Scopus (235) Google Scholar]. However, direct electrophysiological evidence for the exact role of STN during adjustment of decision thresholds is lacking. Here, we show that trial-by-trial variations in STN low-frequency oscillatory activity predict adjustments of decision thresholds before subjects make a response. The relationship between STN activity and decision thresholds critically depends on the subjects’ level of cautiousness. While increased oscillatory activity of the STN predicts elevated decision thresholds during high levels of cautiousness, it predicts decreased decision thresholds during low levels of cautiousness. This context-dependent relationship may be mediated by increased influence of the medial prefrontal cortex (mPFC)-STN pathway on decision thresholds during high cautiousness. Subjects who exhibit a stronger increase in phase alignment of low-frequency oscillatory activity in mPFC and STN before making a response have higher decision thresholds and commit fewer erroneous responses. Together, our results demonstrate that STN low-frequency oscillatory activity and corresponding mPFC-STN coupling are involved in determining how much evidence subjects accumulate before making a decision. This finding might explain why deep-brain stimulation of the STN can impair subjects’ ability to slow down responses and can induce impulsive suboptimal decisions.