Basal ganglia output guides decision-making by state destabilization

Abstract

To execute learned behavior, the nervous system can undergo an activity-state transition between the current and the learned activity states. Here, using adult zebrafish, we show that their basal ganglia output induces such state transitions for goal-directed behavior. After learning the Go/No-go task in virtual reality, the striatal indirect pathway responds to negative values of a conditioned cue and the absence of sensory feedback by different neuronal populations. The pallidal output pathway integrates these negative value signals and then broadcasts the integrated signal to the Dc area in the pallium (fish cortex). Optogenetics and mathematical modeling suggested that this pallidal output activity uniformly destabilizes ongoing Dc activity states, thereby facilitating behavioral state transitions toward the behavioral state with the minimum pallidal output activity. This mechanism explains how pallidal output activity guides goal-directed behavior beyond potential barriers between activity states underlying different behavioral states.