The Role of the Basal Ganglia in the Human Cognitive Architecture: A Dynamic Causal Modeling Comparison Across Tasks and Individuals

Abstract

Researchers agree input from the basal ganglia (BG) to the prefrontal cortex (PFC) plays an important role in cognition, but they disagree on its computational properties. Theoretical models characterize the majority of BG input as either direct (directly transmitting information to the PFC), or modulatory (indirectly influencing PFC activity through the gating of signals from other cortical areas). To determine the computational nature of these BG-PFC inputs in cognition, we tested three alternative connectivity configurations (Direct, Modulatory, and Mixed) within a large-scale cognitive architecture. This architecture, the Common Model of Cognition, has been independently validated using fMRI data from the Human Connectome Project (HCP). The Direct model reflected the standard CMC configuration, featuring a bidirectional, direct connection between the BG and PFC modules. The Modulatory model removed this direct link, instead incorporating a unidirectional connection from the PFC to the BG and two modulatory pathways from the BG to the PFC that passed through other cortical modules. The Mixed model included both direct and modulatory connections. Using fMRI data from 200 HCP participants performing six cognitive tasks and one resting-state session, we applied Dynamic Causal Modeling (DCM) to estimate and compare the influence of these different BG-PFC connectivity patterns. Here, we show that for each of the six cognitive tasks and resting state, the Mixed model consistently outperformed the Direct and Modulatory models. The next best model depended on the specific cognitive task, suggesting the ability for the BG to flexibly adapt to various task demands. Taken together, the current data provide evidence for a likely set of core computations that the BG uses to differentially regulate cortical activity. Author SummaryThis study aimed to understand the nature of regulatory input from the basal ganglia to the prefrontal cortex in cognition using a neuro-computational approach. Three model architectures of basal ganglia connectivity were tested using fMRI data from 200 individuals during cognitive tasks and resting state sessions. Our findings indicate that the Mixed architecture, in which the basal ganglia can affect the prefrontal cortex both directly and indirectly, outperformed the Direct and Modulatory architectures across various cognitive tasks and resting state sessions. The results suggest that the basal ganglia likely uses a set of core computations to regulate cortical activity, which is present during task and task-free behavior.