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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.

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. Still, the specific circuit computations that underpin this foundational aspect of intelligence remain unclear. Here, by examining neural ensemble activity in rats that sample different strategies in a self-guided search for latent task structure, we demonstrate a robust tracking of individual strategy prevalence in the anterior cingulate cortex (ACC), especially in an area homologous to primate area 32D. Prevalence encoding in the ACC is wide-scale, independent of reward delivery, and persists through a substantial ensemble reorganization that tags ACC representations with contextual content. 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 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 switching away from it to evaluate alternatives when appropriate. Studies in humans and non-human primates have uncovered signals in the anterior cingulate cortex (ACC) that track the pressure to switch away from the ongoing strategy, and others that 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 rodent ACC actively arbitrates between persisting with ongoing behavioral choice and switching away temporarily to re-evaluate alternatives. Furthermore, by individually perturbing distinct output pathways, we establish that the two associated computations-whether to switch away from the current choice, and the pursuit of alternatives-are segregated within ACC micro-circuitry. Competing Interest Statement The authors have declared no competing interest.