Region-specific mechanosensation modulates Drosophila postural control behaviour

The relation between regional morphological features derived from the bilaterian body plan and the behaviours necessary to extract utility from such structures is not well understood. Here, we use the Drosophila larva to investigate this 'form-function' problem focusing on the mapping of the regional stimuli that trigger an adaptive and evolutionarily conserved behaviour termed self-righting: a postural control system that allows the animal to restore its natural position if turned upside-down. Through the development of new methodologies that allow regionally restricted mechanical stimulation and zonal-specific neuronal optogenetics, we find that multidendritic sensory neuron inhibition in anterior areas (thoracic/anterior abdominal) has a profound effect on self-righting performance, while inhibition of posterior sensory elements (mid and posterior abdomen) produces no effects. To gain insight into how regional neuronal inhibition affects the different subcomponents of the self-righting sequence we applied a deep neural network tracking method which revealed that reduction of neural activity in anterior sensory neurons primarily increases head casting behaviour and that this, in turn, is strongly correlated with abnormally long self-righting times. Furthermore, to explore the mechanistic bases of our behavioural observations, we considered the hypothesis that the Hox genes - well known for their roles in axial developmental patterning - might play a role in the functional specification of multidendritic sensory neurons along the body axis. Molecular expression analysis of FACS-sorted neural populations, fluorescent immunolabelling and neuron-specific knockdown experiments demonstrate that normal sensory neuron expression of the Hox genes Antennapedia and Abdominal-b is necessary for self-righting in the Drosophila larva. Altogether, our work shows that region-specific mechanosensory processes mediated by multidendritic sensory neurons and instructed via Hox gene inputs are essential for self-righting, providing a link between regional structural features and an adaptive and widely evolutionarily conserved postural control behaviour.