Multi-regional control of amygdalar dynamics reliably reflects fear memory age

The basolateral amygdala (BLA) is crucial for the encoding and expression of fear memory, yet it remains unexplored how neural activity in this region is dynamically influenced by distributed circuits across the brain to facilitate expression of fear memory of different ages. Using longitudinal multisite electrophysiological recordings in male mice, we find that the recall of older contextual fear memory is accompanied by weaker, yet more rhythmic, BLA gamma activity which is distally entrained by theta oscillations in both the hippocampal CA1 and the anterior cingulate cortex. Computational modeling with Light Gradient Boosting Machine using extracted oscillatory features from these three regions, as well as with Transformer using raw local field potentials, accurately classified remote from recent memory recall primarily based on BLA gamma and CA1 theta. These results demonstrate in a non-biased manner that multi-regional control of BLA activity serves as reliable neural signatures for memory age-dependent recall mechanisms.