Basal ganglia components have distinct computational roles in decision-making dynamics under conflict and uncertainty

PLoS Biol. 2025 Jan 23;23(1):e3002978. doi: 10.1371/journal.pbio.3002978. eCollection 2025 Jan.

Abstract

The basal ganglia (BG) play a key role in decision-making, preventing impulsive actions in some contexts while facilitating fast adaptations in others. The specific contributions of different BG structures to this nuanced behavior remain unclear, particularly under varying situations of noisy and conflicting information that necessitate ongoing adjustments in the balance between speed and accuracy. Theoretical accounts suggest that dynamic regulation of the amount of evidence required to commit to a decision (a dynamic "decision boundary") may be necessary to meet these competing demands. Through the application of novel computational modeling tools in tandem with direct neural recordings from human BG areas, we find that neural dynamics in the theta band manifest as variations in a collapsing decision boundary as a function of conflict and uncertainty. We collected intracranial recordings from patients diagnosed with either Parkinson's disease (PD) (n = 14) or dystonia (n = 3) in the subthalamic nucleus (STN), globus pallidus internus (GPi), and globus pallidus externus (GPe) during their performance of a novel perceptual discrimination task in which we independently manipulated uncertainty and conflict. To formally characterize whether these task and neural components influenced decision dynamics, we leveraged modified diffusion decision models (DDMs). Behavioral choices and response time distributions were best characterized by a modified DDM in which the decision boundary collapsed over time, but where the onset and shape of this collapse varied with conflict. Moreover, theta dynamics in BG structures modulated the onset and shape of this collapse but differentially across task conditions. In STN, theta activity was related to a prolonged decision boundary (indexed by slower collapse and therefore more deliberate choices) during high conflict situations. Conversely, rapid declines in GPe theta during low conflict conditions were related to rapidly collapsing boundaries and expedited choices, with additional complementary decision bound adjustments during high uncertainty situations. Finally, GPi theta effects were uniform across conditions, with increases in theta associated with a prolongation of decision bound collapses. Together, these findings provide a nuanced understanding of how our brain thwarts impulsive actions while nonetheless enabling behavioral adaptation amidst noisy and conflicting information.

MeSH terms

  • Adult
  • Aged
  • Basal Ganglia* / physiology
  • Conflict, Psychological*
  • Decision Making* / physiology
  • Dystonia / physiopathology
  • Female
  • Globus Pallidus / physiology
  • Humans
  • Male
  • Middle Aged
  • Parkinson Disease* / physiopathology
  • Subthalamic Nucleus / physiology
  • Theta Rhythm / physiology
  • Uncertainty

Grants and funding

This work was supported by the Swiss National Science Foundation (P500PS_214223 to NGJ; www.snsf.ch) and the National Institutes of Mental Health (1R01MH119382 to JC; T32MH126388-01 & P50MH119467 & P50MH106435-06A1 to MJF; www.nimh.nih.gov) and the Office of Naval Research Global (ONR MURI N00014-23-1-2792 to MJF; https://www.onr.navy.mil/) and the National Institutes of Health (P20GM1 03645 to WFA & S10OD025181 to the Center for Computation and Visualization at Brown University; www.nimh.nih.gov) and the Doris Duke Charitable Foundation Clinical Scientist Development Award to WFA (www.dorisduke.org) and the AANS Neurosurgery Research and Education Foundation Award to WFA (www.aans.org) and the DEARS Foundation to MJF (https://thedearfoundation.ch). None of the funders played any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.