ACC neural ensemble dynamics are structured by strategy prevalence.

Medial frontal cortical areas are thought to play a critical role in the brain's ability to flexibly deploy strategies that are effective in complex settings, yet the underlying circuit computations remain unclear. Here, by examining neural ensemble activity in male rats that sample different strategies in a self-guided search for latent task structure, we observe robust tracking during strategy execution of a summary statistic for that strategy in recent behavioral history by the anterior cingulate cortex (ACC), especially by an area homologous to primate area 32D. Using the simplest summary statistic - strategy prevalence in the last 20 choices - we find that its encoding in the ACC during strategy execution is wide-scale, independent of reward delivery, and persists through a substantial ensemble reorganization that accompanies changes in global context. We further demonstrate that the tracking of reward by the ACC ensemble is also strategy-specific, but that reward prevalence is insufficient to explain the observed activity modulation during strategy execution. Our findings argue that ACC ensemble dynamics is structured by a summary statistic of recent behavioral choices, raising the possibility that ACC plays a role in estimating - through statistical learning - which actions promote the occurrence of events in the environment.

The anterior cingulate cortex directs exploration of alternative strategies.

The ability to adjust one's behavioral strategy in complex environments is at the core of cognition. Doing so efficiently requires monitoring the reliability of the ongoing strategy and, when appropriate, switching away from it to evaluate alternatives. Studies in humans and non-human primates have uncovered signals in the anterior cingulate cortex (ACC) that reflect the pressure to switch away from the ongoing strategy, whereas other ACC signals relate to the pursuit of alternatives. However, whether these signals underlie computations that actually underpin strategy switching or merely reflect tracking of related variables remains unclear. Here we provide causal evidence that the rodent ACC actively arbitrates between persisting with the ongoing behavioral strategy and temporarily switching away to re-evaluate alternatives. Furthermore, by individually perturbing distinct output pathways, we establish that the two associated computations-determining whether to switch strategy and committing to the pursuit of a specific alternative-are segregated in the ACC microcircuitry.

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 counter prediction 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 counter prediction. 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. PAPERCLIP: