How the dynamic interplay of cortico-basal ganglia-thalamic pathways shapes the time course of deliberation and commitment

Abstract

Although the cortico-basal ganglia-thalamic (CBGT) network is identified as a central circuit for decision-making, the dynamic interplay of multiple control pathways within this network in shaping decision trajectories remains poorly understood. Here we develop and apply a novel computational framework -- CLAW (Circuit Logic Assessed via Walks) -- for tracing the instantaneous flow of neural activity as it progresses through CBGT networks engaged in a virtual decision-making task. Our CLAW analysis reveals that the complex dynamics of network activity is functionally dissectible into two critical phases: deliberation and commitment. These two phases are governed by distinct contributions of underlying CBGT pathways, with indirect and pallidostriatal pathways influencing deliberation, while the direct pathway drives action commitment. We translate CBGT dynamics into the evolution of decision-related policies, based on three previously identified control ensembles (responsiveness, pliancy, and choice) that encapsulate the relationship between CBGT activity and the evidence accumulation process. Our results demonstrate two contrasting strategies for decision-making. Fast decisions, with direct pathway dominance, feature an early response in both boundary height and drift rate, leading to a rapid collapse of decision boundaries and a clear directional bias. In contrast, slow decisions, driven by indirect and pallidostriatal pathway dominance, involve delayed changes in both decision policy parameters, allowing for an extended period of deliberation before commitment to an action. These analyses provide important insights into how the CBGT circuitry can be tuned to adopt various decision strategies and how the decision-making process unfolds within each regime. Author summaryWe investigate how the cortico-basal ganglia-thalamic (CBGT) network coordinates decision-making through its interconnected pathways. Using a novel Circuit Logic Assessed via Walks (CLAW) framework, we trace instantaneous neural activity through virtual CBGT networks as they engage in forced choice decisions. This analysis uncovers two key phases of a decision: deliberation, shaped by the indirect and pallidostriatal pathways, and commitment, driven by the direct pathway. We also demonstrate that CBGT activity supports two distinct decision styles: fast decisions involve an early decision boundary collapse and strong directional preference, while slow decisions feature minimal changes during an extended deliberation phase. These findings reveal the dynamic mechanisms within the CBGT network that underlie the different decision processes and how these can be tuned to adapt decision-making across varying demands and contexts.