Behavioral Variability through Stochastic Choice and Its Gating by Anterior Cingulate Cortex

Behavioral choices that ignore prior experience promote exploration and unpredictability but are seemingly at odds with the brain’s tendency to use experience to optimize behavioral choice. Indeed, when faced with virtual competitors, primates resort to strategic counterprediction rather than to stochastic choice. Here, we show that rats also use history- and model-based strategies when faced with similar competitors but can switch to a “stochastic” mode when challenged with a competitor that they cannot defeat by counterprediction. In this mode, outcomes associated with an animal’s actions are ignored, and normal engagement of anterior cingulate cortex (ACC) is suppressed. Using circuit perturbations in transgenic rats, we demonstrate that switching between strategic and stochastic behavioral modes is controlled by locus coeruleus input into ACC. Our findings suggest that, under conditions of uncertainty about environmental rules, changes in noradrenergic input alter ACC output and prevent erroneous beliefs from guiding decisions, thus enabling behavioral variation.