Social facilitation of long-lasting memory is mediated by CO₂ in Drosophila

How social interactions influence cognition is a fundamental question, yet rarely addressed at the neurobiological level. It is well established that the presence of conspecifics affects learning and memory performance, but the neural basis of this process has only recently begun to be investigated. In the fruit fly Drosophila melanogaster, the presence of other flies improves retrieval of a long-lasting olfactory memory. Here, we demonstrate that this is a composite memory composed of two distinct elements. One is an individual memory that depends on outputs from the α'β' Kenyon cells (KCs) of the mushroom bodies (MBs), the memory center in the insect brain. The other is a group memory requiring output from the αβ KCs, a distinct sub-part of the MBs. We show that social facilitation of memory increases with group size and is triggered by CO₂ released by group members. Among the different known neurons carrying CO₂ information in the brain, we establish that the bilateral ventral projection neuron (biVPN), which projects onto the MBs, is necessary for social facilitation. Moreover, we demonstrate that CO₂-evoked memory engages a serotoninergic pathway involving the dorsal-paired medial (DPM) neurons, revealing a new role for this pair of serotonergic neurons. Overall, we identified both the sensorial cue and the neural circuit (biVPN>αβ>DPM>αβ) governing social facilitation of memory in flies. This study provides demonstration that being in a group recruits the expression of a cryptic memory and that variations in CO₂ concentration can affect cognitive processes in insects.