Late UP-state bias in cortico-amygdalar coordination

Neocortical slow oscillations temporally organize neuronal activity across distributed brain regions, but the coordination of basolateral amygdala (BLA) activity with these oscillations remains unclear. We investigated BLA neuronal activity relative to neocortical slow oscillations in male mice, primarily under urethane anesthesia. These oscillations are characterized by rhythmic alternation between active (UP) and inactive (DOWN) states at 0.3-3 Hz. Using unit recordings and calcium imaging, we found that BLA neuronal activity was sparse but preferentially associated with the later phase of the neocortical UP state, while calcium activity showed local spatial organization with greater synchronization among nearby neurons. Medial prefrontal cortical neurons projecting to the BLA were more likely to continue firing into the late phase of the UP state than other prefrontal neurons. Deep whole-cell recordings revealed transient depolarizations in BLA neurons preferentially during the late phase of UP states. Both the probability and timing of these depolarizations varied with UP-state duration, and voltage-clamp recordings revealed temporally anticorrelated changes in excitatory and inhibitory conductances. Thus, these findings define a temporally structured and probabilistic mode of neocortex-BLA coordination during slow oscillations.Significance Statement Neocortical slow oscillations organize long-range neuronal coordination during sleep-like states, but their temporal relationship with basolateral amygdala (BLA) activity remains poorly understood. We show that BLA neuronal activity is sparse and probabilistically biased toward the late phase of neocortical UP states rather than uniformly distributed throughout the UP period. BLA activity is further characterized by temporally anticorrelated changes in excitatory and inhibitory conductances and locally organized calcium activity. In addition, BLA-projecting medial prefrontal cortical neurons are more likely to continue firing into the late phase of UP states. These results establish a physiological framework for understanding the temporal organization of neocortex-BLA coordination during slow oscillatory brain states.