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Specific neuronal subpopulations within specific brain areas are responsible for learning and memory. A fear memory engages a subset of lateral amygdala neurons, but whether multiple contextual fear memories engage the same or different subsets of lateral amygdala neurons remains unclear. Here, we demonstrate the representation of multiple contextual fear memories in the amygdala with cellular and temporal resolution using a large-scale imaging method. Mice were conditioned with a footshock in 2 separate chambers. They were then re-exposed to either the same conditioning chamber twice or 2 different conditioning chambers. The activities of individual neurons related to the re-exposures were determined by the subcellular distribution of Arc/Arg3.1 RNA. Reactivation of different memories activated partially (about 50%) overlapping neurons, whereas reactivation of the same memory activated more overlapping (about 65%) neurons. These findings indicate that lateral amygdala neurons related to different fear memories are partly common, and that a small but significant neuronal population (2.7% of total lateral amygdala neurons) encodes differences in individual fear memories. Moreover, memory retrieval increased the size of the neuronal subpopulation activated during subsequent retrieval. Taken together, our findings indicate that small plastic subsets of neurons encode fear memories from individual contexts.□ The representation of multiple context fear memories was imaged in the amygdala. □ Reactivations of the different fear memories activate partially overlapping neurons. □ Reactivation of the same context fear memory activates more overlapping neurons. □ Only 2.7% of total neurons encode differences in individual fear memories. □ Memory reactivation enlarges the neuronal subpopulation related to the memory.