The interruptive effect of electric shock on odor response requires mushroom bodies in Drosophila melanogaster

Nociceptive stimulus involuntarily interrupts concurrent activities. This interruptive effect is related to the protective function of nociception that is believed to be under stringent evolutionary pressure. To determine whether such interruptive effect is conserved in invertebrate and potentially uncover underlying neural circuits, we examined Drosophila melanogaster. Electric shock (ES) is a commonly used nociceptive stimulus for nociception related research in Drosophila. Here, we showed that background noxious ES dramatically interrupted odor response behaviors in a T-maze, which is termed blocking odor response by electric shock (BOBE). The interruptive effect is not odor specific. ES could interrupt both odor avoidance and odor approach. To identify involved brain areas, we focused on the odor avoidance to 3-OCT. By spatially abolishing neurotransmission with temperature sensitive Shibire^TS1 , we found that mushroom bodies (MBs) are necessary for BOBE. Among the 3 major MB Kenyon cell (KCs) subtypes, α/β neurons and γ neurons but not α'/β' neurons are required for normal BOBE. Specifically, abolishing the neurotransmission of either α/β surface (α/β_s ), α/β core (α/β_c ) or γ dorsal (γ_d ) neurons alone is sufficient to abrogate BOBE. This pattern of MB subset requirement is distinct from that of aversive olfactory learning, indicating a specialized BOBE pathway. Consistent with this idea, BOBE was not diminished in several associative memory mutants and noxious ES interrupted both innate and learned odor avoidance. Overall, our results suggest that MB α/β and γ neurons are parts of a previously unappreciated central neural circuit that processes the interruptive effect of nociception.