Role of the subesophageal zone in sensorimotor control of orientation in Drosophila larva

Abstract

Chemotaxis is a powerful paradigm to investigate how nervous systems represent and integrate changes in sensory signals to direct navigational decisions. In the Drosophila melanogaster larva, chemotaxis mainly consists of an alternation of distinct behavioral modes: runs and directed turns. During locomotion, turns are triggered by the integration of temporal changes in the intensity of the stimulus. Upon completion of a turning maneuver, the direction of motion is typically realigned toward the odor gradient. While the anatomy of the peripheral olfactory circuits and the locomotor system of the larva are reasonably well documented, the neural circuits connecting the sensory neurons to the motor neurons remain unknown. We combined a loss-of-function behavioral screen with optogenetics-based clonal gain-of-function manipulations to identify neurons that are necessary and sufficient for the initiation of reorientation maneuvers in odor gradients. Our results indicate that a small subset of neurons residing in the subesophageal zone controls the rate of transition from runs to turns-a premotor function compatible with previous observations made in other invertebrates. After having shown that this function pertains to the processing of inputs from different sensory modalities (olfaction, vision, thermosensation), we conclude that the subesophageal zone operates as a general premotor center that regulates the selection of different behavioral programs based on the integration of sensory stimuli. The present analysis paves the way for a systematic investigation of the neural computations underlying action selection in a miniature brain amenable to genetic manipulations.M.L. acknowledges funding from the Spanish Ministry of Science and Innovation (MICINN, BFU2008-00362, BFU2009-07757-E/BMC, and BFU2011-26208), the EMBL/CRG Systems Biology Program, and a Marie Curie Reintegration Grant (PIRG02-GA-2007-224791). J.W.T. was supported by the Howard Hughes Medical Institute. I.T. acknowledges funding from the Marie Curie FP7 Programme through FLiACT (ITN