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Human subthalamic nucleus activity during non-motor decision making.

ABSTRACT: Recent studies have implicated the subthalamic nucleus (STN) in decisions that involve inhibiting movements. Many of the decisions that we make in our daily lives, however, do not involve any motor actions. We studied non-motor decision making by recording intraoperative STN and prefrontal cortex (PFC) electrophysiology as participants perform a novel task that required them to decide whether to encode items into working memory. During all encoding trials, beta band (15-30 Hz) activity decreased in the STN and PFC, and this decrease was progressively enhanced as more items were stored into working memory. Crucially, the STN and lateral PFC beta decrease was significantly attenuated during the trials in which participants were instructed not to encode the presented stimulus. These changes were associated with increase lateral PFC-STN coherence and altered STN neuronal spiking. Our results shed light on why states of altered basal ganglia activity disrupt both motor function and cognition.

SUBMITTER: Zavala BA

PROVIDER: S-EPMC5780045 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Human subthalamic nucleus activity during non-motor decision making.

Zavala Baltazar A BA Jang Anthony I AI Zaghloul Kareem A KA

eLife 20171215

Recent studies have implicated the subthalamic nucleus (STN) in decisions that involve inhibiting movements. Many of the decisions that we make in our daily lives, however, do not involve any motor actions. We studied non-motor decision making by recording intraoperative STN and prefrontal cortex (PFC) electrophysiology as participants perform a novel task that required them to decide whether to encode items into working memory. During all encoding trials, beta band (15-30 Hz) activity decreased ...[more]

PMID: 29243587

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Project description:Adaptive behaviour entails the capacity to select actions as a function of their energy cost and expected value and the disruption of this faculty is now viewed as a possible cause of the symptoms of Parkinson's disease. Indirect evidence points to the involvement of the subthalamic nucleus-the most common target for deep brain stimulation in Parkinson's disease-in cost-benefit computation. However, this putative function appears at odds with the current view that the subthalamic nucleus is important for adjusting behaviour to conflict. Here we tested these contrasting hypotheses by recording the neuronal activity of the subthalamic nucleus of patients with Parkinson's disease during an effort-based decision task. Local field potentials were recorded from the subthalamic nucleus of 12 patients with advanced Parkinson's disease (mean age 63.8 years ± 6.8; mean disease duration 9.4 years ± 2.5) both OFF and ON levodopa while they had to decide whether to engage in an effort task based on the level of effort required and the value of the reward promised in return. The data were analysed using generalized linear mixed models and cluster-based permutation methods. Behaviourally, the probability of trial acceptance increased with the reward value and decreased with the required effort level. Dopamine replacement therapy increased the rate of acceptance for efforts associated with low rewards. When recording the subthalamic nucleus activity, we found a clear neural response to both reward and effort cues in the 1-10 Hz range. In addition these responses were informative of the subjective value of reward and level of effort rather than their actual quantities, such that they were predictive of the participant's decisions. OFF levodopa, this link with acceptance was weakened. Finally, we found that these responses did not index conflict, as they did not vary as a function of the distance from indifference in the acceptance decision. These findings show that low-frequency neuronal activity in the subthalamic nucleus may encode the information required to make cost-benefit comparisons, rather than signal conflict. The link between these neural responses and behaviour was stronger under dopamine replacement therapy. Our findings are consistent with the view that Parkinson's disease symptoms may be caused by a disruption of the processes involved in balancing the value of actions with their associated effort cost.

Project description:Even simple behaviour requires us to make decisions based on combining multiple pieces of learned and new information. Making such decisions requires both learning the optimal response to each given stimulus as well as combining probabilistic information from multiple stimuli before selecting a response. Computational theories of decision making predict that learning individual stimulus-response associations and rapid combination of information from multiple stimuli are dependent on different components of basal ganglia circuitry. In particular, learning and retention of memory, required for optimal response choice, are significantly reliant on dopamine, whereas integrating information probabilistically is critically dependent upon functioning of the glutamatergic subthalamic nucleus (computing the 'normalization term' in Bayes' theorem). Here, we test these theories by investigating 22 patients with Parkinson's disease either treated with deep brain stimulation to the subthalamic nucleus and dopaminergic therapy or managed with dopaminergic therapy alone. We use computerized tasks that probe three cognitive functions-information acquisition (learning), memory over a delay and information integration when multiple pieces of sequentially presented information have to be combined. Patients performed the tasks ON or OFF deep brain stimulation and/or ON or OFF dopaminergic therapy. Consistent with the computational theories, we show that stopping dopaminergic therapy impairs memory for probabilistic information over a delay, whereas deep brain stimulation to the region of the subthalamic nucleus disrupts decision making when multiple pieces of acquired information must be combined. Furthermore, we found that when participants needed to update their decision on the basis of the last piece of information presented in the decision-making task, patients with deep brain stimulation of the subthalamic nucleus region did not slow down appropriately to revise their plan, a pattern of behaviour that mirrors the impulsivity described clinically in some patients with subthalamic nucleus deep brain stimulation. Thus, we demonstrate distinct mechanisms for two important facets of human decision making: first, a role for dopamine in memory consolidation, and second, the critical importance of the subthalamic nucleus in successful decision making when multiple pieces of information must be combined.

Dataset Information

Human subthalamic nucleus activity during non-motor decision making.

Publications

Human subthalamic nucleus activity during non-motor decision making.

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