The human subthalamic nucleus and globus pallidus internus differentially encode reward during action control

Abstract

The subthalamic nucleus (STN) and globus pallidus internus (GPi) have recently been shown to encode reward, but few studies have been performed in humans. We investigated STN and GPi encoding of reward and loss (i.e., valence) in humans with Parkinson's disease. To test the hypothesis that STN and GPi neurons would change their firing rate in response to reward- and loss-related stimuli, we recorded the activity of individual neurons while participants performed a behavioral task. In the task, action choices were associated with potential rewarding, punitive, or neutral outcomes. We found that STN and GPi neurons encode valence-related information during action control, but the proportion of valence-responsive neurons was greater in the STN compared to the GPi. In the STN, reward-related stimuli mobilized a greater proportion of neurons than loss-related stimuli. We also found surprising limbic overlap with the sensorimotor regions in both the STN and GPi, and this overlap was greater than has been previously reported. These findings may help to explain alterations in limbic function that have been observed following deep brain stimulation therapy of the STN and GPi. Hum Brain Mapp 38:1952-1964, 2017. © 2017 Wiley Periodicals, Inc.

Programming for Stimulation-Induced Transient Nonmotor Psychiatric Symptoms after Bilateral Subthalamic Nucleus Deep Brain Stimulation for Parkinson’s Disease

“…However, recent studies show their active contacts located in the dorsolateral (sensorimotor) area of STN [14] which also induces STPS. Because of this reason, the limbic and sensorimotor regions of the STN overlap were greater than what has been previously reported [15]. In this study, we also found that the active contacts which induced STPS were located at a medial and inferior part of the STN in seven (07) patients.…”

Impulsivity in Parkinson’s disease is associated with altered subthalamic but not globus pallidus internus activity

“…The details of the behavioural paradigm and performance criteria have been described previously 13. In brief, a unique visual stimulus was associated with each of the following scenarios: reward for action (Go for Reward), reward for inaction (No Go for Reward), punishment for action (No Go to Avoid Loss) and punishment for inaction (No Go for Reward).…”

“…During task performance, single unit activity was recorded in either the STN or GPi, using target localisation, data acquisition and recording protocols previously described 13. Recordings from 100 STN neurons (35 from ICD+ patients and 65 from ICD− patients) and 100 GPi neurons (36 from ICD+ patients and 64 from ICD− patients) met these criteria.…”

“…Recordings from 100 STN neurons (35 from ICD+ patients and 65 from ICD− patients) and 100 GPi neurons (36 from ICD+ patients and 64 from ICD− patients) met these criteria. Neuronal responsiveness (ie, significant change in firing rate from baseline in response to a stimulus) was determined via a previously described method 13. Proportions of responsive neurons were compared using χ 2  statistics, and firing rate changes were compared using two-way repeated measures analysis of variance and χ 2 statistics.…”

Non-motor Characterization of the Basal Ganglia: Evidence From Human and Non-human Primate Electrophysiology

“…Furthermore, it is important to note that investigations of response inhibition and high-conflict decision-making presented here are typically limited to studies of immediate actions and depend on the temporal sequence of the paradigm employed. For instance, a study of single units in humans showed that nucleus accumbens activity predicts future financial decisions that occur on average just 2 s later (Patel et al, 2012 ), however other studies use paradigms in which total trial duration may be <2 s (Rossi et al, 2017 ). From study to study, results cannot generally be applied to decisions occurring at different time scales (Zavala et al, 2015 ).…”