Basolateral amygdala neurons await oscillatory recruitment into valence-relevant ensembles

Impaired valence processing is a core feature of psychiatric illnesses. The ability to rapidly evaluate situations and stimuli and determine whether they have positive or negative implications, termed valence processing, is a highly adaptive brain function that is essential for survival. Despite its importance, we still lack a complete understanding of the neural computations involved. The basolateral amygdala (BLA) plays a critical role in valence processing and valence ensembles have been identified by their anatomical location within the BLA, their projection targets, their genetic identity, or some combination of these factors. In parallel, distinct BLA oscillatory states have been shown to drive divergent valence states. Despite abundant evidence separately supporting these processes, we have failed to reconcile these disparate contributions to valence processing. Here, we demonstrate that subpopulations of BLA principal neurons are recruited in response to specific frequencies of optogenetically-driven oscillations. We provide evidence showing ensemble recruitment is a product of individual neuronal sensitivities to input frequencies that can be driven by interneuron-driven oscillatory states. We also demonstrate that oscillations driven by interneuron stimulations can activate projection-specific populations and reactivate behaviorally-relevant ensembles. Together, these findings reveal a novel neural computational mechanism governing valence processing involving the ability of interneuron-driven oscillatory states to selectively recruit populations of frequency-, projection-, and valence-specific BLA neurons to evoke distinct behavioral outcomes.