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The subthalamic nucleus contributes causally to perceptual decision-making in monkeys.

ABSTRACT: The subthalamic nucleus (STN) plays critical roles in the motor and cognitive function of the basal ganglia (BG), but the exact nature of these roles is not fully understood, especially in the context of decision-making based on uncertain evidence. Guided by theoretical predictions of specific STN contributions, we used single-unit recording and electrical microstimulation in the STN of healthy monkeys to assess its causal, computational roles in visual-saccadic decisions based on noisy evidence. The recordings identified subpopulations of STN neurons with distinct task-related activity patterns that related to different theoretically predicted functions. Microstimulation caused changes in behavioral choices and response times that reflected multiple contributions to an "accumulate-to-bound"-like decision process, including modulation of decision bounds and evidence accumulation, and to non-perceptual processes. These results provide new insights into the multiple ways that the STN can support higher brain function.

SUBMITTER: Rogers K

PROVIDER: S-EPMC11030388 | biostudies-literature | 2024 Apr

REPOSITORIES: biostudies-literature

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The subthalamic nucleus contributes causally to perceptual decision-making in monkeys.

Rogers Kathryn K Gold Joshua I JI Ding Long L

bioRxiv : the preprint server for biology 20240724

The subthalamic nucleus (STN) plays critical roles in the motor and cognitive function of the basal ganglia (BG), but the exact nature of these roles is not fully understood, especially in the context of decision-making based on uncertain evidence. Guided by theoretical predictions of specific STN contributions, we used single-unit recording and electrical microstimulation in the STN of healthy monkeys to assess its causal, computational roles in visual-saccadic decisions based on noisy evidence ...[more]

PMID: 38645039

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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.

Project description:The ability to make decisions based on external information, prior knowledge, and evidence is a crucial aspect of cognition and may determine the success and survival of an organism. Despite extensive work on decision-making mechanisms/models, understanding the effects of alertness on neural and cognitive processes remain limited. Here we use EEG and behavioral modeling to characterize cognitive and neural dynamics of perceptual decision-making in awake/low alertness periods in humans (14 male, 18 female) and characterize the compensatory mechanisms as alertness decreases. Well-rested human participants, changing between full-wakefulness and low alertness, performed an auditory tone-localization task, and its behavioral dynamics were quantified with psychophysics, signal detection theory, and drift-diffusion modeling, revealing slower reaction times, inattention to the left side of space, and a lower rate of evidence accumulation in periods of low alertness. Unconstrained multivariate pattern analysis (decoding) showed a ∼280 ms delayed onset driven by low alertness of the neural signatures differentiating between left and right decision, with a spatial reconfiguration from centroparietal to lateral frontal regions 150-360 ms. To understand the neural compensatory mechanisms with decreasing alertness, we connected the evidence-accumulation behavioral parameter to the neural activity, showing in the early periods (125-325 ms) a shift in the associated patterns from right parietal regions in awake, to right frontoparietal during low alertness. This change in the neurobehavioral dynamics for central accumulation-related cognitive processes defines a clear reconfiguration of the brain networks' regions and dynamics needed for the implementation of decision-making, revealing mechanisms of resilience of cognition when challenged by decreased alertness.SIGNIFICANCE STATEMENT Most living organisms make multiple daily decisions, and these require a degree of evidence from both the environment and the internal milieu. Such decisions are usually studied under sequential sampling models and involve making a behavioral choice based on sensory encoding, central accumulation, and motor implementation processes. Since there is little research on how decreasing alertness affects such cognitive processes, this study has looked at the cognitive and neural dynamics of perceptual decision-making in people while fully awake and in drowsy periods. Using computational modeling of behavior and neural dynamics on human participants performing an auditory tone-localization task, we reveal how low alertness modulates evidence accumulation-related processes and its corresponding compensatory neural signatures.

Dataset Information

The subthalamic nucleus contributes causally to perceptual decision-making in monkeys.

Publications

The subthalamic nucleus contributes causally to perceptual decision-making in monkeys.

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