Social Facilitation of Long-Lasting Memory is Mediated by CO 2 in Drosophila

How social interactions influences 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 for the influence of the social context has received little attention. In the fruitfly Drosophila melanogaster, the presence of conspecifics improves retrieval of a long-lasting olfactory memory. Here, we demonstrate that this memory is composite and involves two independent neural pathways. One is based on the expression of individual memory and depends on the α’β’ lobes outputs of the Mushroom Bodies (MBs), the memory center in the insect brain. The other one relies on the expression of group memory and requires a distinct sub-part of the MBs, the αβ lobes outputs. We show that such social facilitation increases with group size and is triggered by the CO2 released by group members. Among the 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 this CO2-dependent memory engages a serotoninergic pathway involving the Dorsal-Paired Median neurons (DPM), which reveals a new role for this pair of serotonergic neurons. Overall, we identify both the sensorial cue and the neural circuit (biVPN>αβ>DPM>αβ) governing social facilitation of memory. This study provides the first 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.