Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence

Decisions are made through the integration of external and internal inputs until a threshold is reached, triggering a response. The subthalamic nucleus (STN) has been implicated in adjusting the decision bound to prevent impulsivity during difficult decisions. We combine model-based and model-free a...

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Main Authors: Dennis London, Michael H. Pourfar, Alon Y. Mogilner
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-03-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.00270/full
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author Dennis London
Michael H. Pourfar
Alon Y. Mogilner
author_facet Dennis London
Michael H. Pourfar
Alon Y. Mogilner
author_sort Dennis London
collection DOAJ
description Decisions are made through the integration of external and internal inputs until a threshold is reached, triggering a response. The subthalamic nucleus (STN) has been implicated in adjusting the decision bound to prevent impulsivity during difficult decisions. We combine model-based and model-free approaches to test the theory that the STN raises the decision bound, a process impaired by deep brain stimulation (DBS). Eight male and female human subjects receiving treatment for Parkinson's disease with bilateral DBS of the STN performed an auditory two-alternative forced choice task. By ending trials unpredictably, we collected reaction time (RT) trials in which subjects reached their decision bound and non-RT trials in which subjects were forced to make a decision with less evidence. A decreased decision bound would cause worse performance on RT trials, and we found this to be the case on left-sided RT trials. Drift diffusion modeling showed a negative drift rate. This implies that in the absence of new evidence, the amount of evidence accumulated tends to drift toward zero. If evidence is accumulated at a constant rate this results in the evidence accumulated reaching an asymptote, the distance of which from the bound was decreased by DBS (p = 0.0079, random shuffle test), preventing subjects from controlling impulsivity. Subjects were more impulsive to bursts of stimuli associated with conflict (p < 0.001, cluster mass test). In addition, DBS lowered the decision bound specifically after error trials, decreasing the probability of switching to a non-RT trial after an error compared to correct response (28% vs. 38%, p = 0.005, Fisher exact test). The STN appears to function in decision-making by modulating the decision bound and drift rate to allow the suppression of impulsive responses.
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spelling doaj.art-f3e11360243f4e4cb406d5405d2ef9632022-12-21T23:49:36ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-03-011310.3389/fnins.2019.00270434585Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory EvidenceDennis LondonMichael H. PourfarAlon Y. MogilnerDecisions are made through the integration of external and internal inputs until a threshold is reached, triggering a response. The subthalamic nucleus (STN) has been implicated in adjusting the decision bound to prevent impulsivity during difficult decisions. We combine model-based and model-free approaches to test the theory that the STN raises the decision bound, a process impaired by deep brain stimulation (DBS). Eight male and female human subjects receiving treatment for Parkinson's disease with bilateral DBS of the STN performed an auditory two-alternative forced choice task. By ending trials unpredictably, we collected reaction time (RT) trials in which subjects reached their decision bound and non-RT trials in which subjects were forced to make a decision with less evidence. A decreased decision bound would cause worse performance on RT trials, and we found this to be the case on left-sided RT trials. Drift diffusion modeling showed a negative drift rate. This implies that in the absence of new evidence, the amount of evidence accumulated tends to drift toward zero. If evidence is accumulated at a constant rate this results in the evidence accumulated reaching an asymptote, the distance of which from the bound was decreased by DBS (p = 0.0079, random shuffle test), preventing subjects from controlling impulsivity. Subjects were more impulsive to bursts of stimuli associated with conflict (p < 0.001, cluster mass test). In addition, DBS lowered the decision bound specifically after error trials, decreasing the probability of switching to a non-RT trial after an error compared to correct response (28% vs. 38%, p = 0.005, Fisher exact test). The STN appears to function in decision-making by modulating the decision bound and drift rate to allow the suppression of impulsive responses.https://www.frontiersin.org/article/10.3389/fnins.2019.00270/fullDBSSTNParkinson's diseasedecision-makingdrift diffusion model
spellingShingle Dennis London
Michael H. Pourfar
Alon Y. Mogilner
Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence
Frontiers in Neuroscience
DBS
STN
Parkinson's disease
decision-making
drift diffusion model
title Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence
title_full Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence
title_fullStr Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence
title_full_unstemmed Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence
title_short Deep Brain Stimulation of the Subthalamic Nucleus Induces Impulsive Responses to Bursts of Sensory Evidence
title_sort deep brain stimulation of the subthalamic nucleus induces impulsive responses to bursts of sensory evidence
topic DBS
STN
Parkinson's disease
decision-making
drift diffusion model
url https://www.frontiersin.org/article/10.3389/fnins.2019.00270/full
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AT michaelhpourfar deepbrainstimulationofthesubthalamicnucleusinducesimpulsiveresponsestoburstsofsensoryevidence
AT alonymogilner deepbrainstimulationofthesubthalamicnucleusinducesimpulsiveresponsestoburstsofsensoryevidence