View Program - 63rd Annual Drosophila Research Conference

The brain coordinates the movements that constitute behavior, but how descending neurons (DNs) convey the myriad of commands required to activate the motor neurons of the limbs in the right order and combinations to produce those movements is not well understood. Here, we used fly anterior grooming to address this question. Anterior grooming consists of two basic movements, head sweeps and front leg rubbing. The analysis of the anterior grooming structure by Automatic behavior Recognition System (ABRS) showed that head sweeps and front leg rubbing are normally coupled, but alternate for the efficient dust removal. Using the optogenetic activation, we identified 3 different groups of command-like DNs that can induce front leg rubbing (DNg11), or head sweeps (aDN), or the alternation of both (DNg12). This demonstrates that there are multiple control modes for anterior grooming at the level of descending neurons, which DNs can evoke either the whole alternation program or the specific subroutines. Head sweeps and front leg rubbing both use the front legs and so are mutual exclusive. Parallel optogenetic activation of DNg11 and aDN resulted in normal alternation between head sweeps and front leg rubbing, and DNg12 itself can induce both movements. These results demonstrate that the VNC can resolve conflicting descending drives. Using FlyWire to reconstruct neurons in a whole-brain electron microscope dataset (EM), we identified a novel inhibitory circuit connecting head sensory neurons to DNg11 that command front leg rubbing. This suggests that decisions between actions can also be made in the brain. Lastly, we explored descending control of limb coordination in these movements by unilateral activation of DNs. Interestingly, unilateral activation of DNg12 or aDN1 induced single-side head sweeps, while unilateral activation of DNg11 induced bilateral front leg rubbing. Our results suggests that left and right leg movements can be decoupled in head sweeps but not in front leg rubbing. Using EM, we found a neural circuit in the brain indirectly connecting the left and right DNg11, which can potentially explain how unilateral activation can result in bilateral execution. Taken together, these results demonstrate that distinct descending neurons can orchestrate the complex alternation between the movements that make up anterior grooming.

Descending neurons coordinate anterior grooming behavior in Drosophila