Legged locomotion in terrestrial animals is often essential for mating and survival, and locomotor behavior must be robust and adaptable in order to be successful. The behavioral plasticity demonstrated by animals’ ability to locomote across diverse types of terrains and to change their locomotion in a task-dependent manner highlights the flexible and modular nature of locomotor networks. The six legs of insects are under the multi-level control of local networks for each limb and limb joint in addition to over-arching central control of the local networks. These networks, consisting of pattern-generating groups of interneurons, motor neurons, and muscles, receive modifying and reinforcing feedback from sensory structures that encode motor output. Proprioceptors in the limbs monitoring their position and movement provide information to these networks that is essential for the adaptability and robustness of locomotor behavior.
In insects, proprioceptors are highly diverse, and the exact role of each type in motor control has yet to be determined. Chordotonal organs, analogous to vertebrate muscle spindles, are proprioceptive stretch receptors that span joints and encode specific parameters of relative movement between body segments. In insects, when leg chordotonal organs are disabled or manipulated, interleg coordination and walking are affected, but the simple behavior of straight walking on a flat surface can still be performed. The femoral chordotonal organ (fCO) is the largest leg proprioceptor and monitors the position and movements of the tibia relative to the femur. It has long been studied for its importance in locomotor and postural control. In Drosophila melanogaster, an ideal model organism due its genetic tractability, investigations into the composition, connectivity, and function of the fCO are still in their infancy. The fCO in Drosophila contains anatomical subgroups, and the neurons within a subgroup demonstrate similar responses to movements about the femur-tibia joint. Collectively, the experiments laid out in this dissertation provide a multi-faceted analysis of the anatomy, connectivity, and functional importance of subgroups of fCO neurons in D. melanogaster.
The dissertation is divided into four chapters, representing different aspects of this complex and intriguing system. First, I present a detailed analysis of the composition of the fCO and its connectivity within the peripheral and central nervous systems. I demonstrate that the fCO is made up of anatomically distinct groups of neurons, each with their own unique features in the legs and ventral nerve cord. Second, I investigated the neuropeptide profile of the fCO and demonstrate that some fCO neurons express a susbtance that is known to act as a neuromodulator. Third, I demonstrate the sufficiency of subsets of fCO neurons to elicit reflex responses, highlighting the role of the Drosophila fCO in postural control. Lastly, I take this a step further and look into the functional necessity of these neuronal subsets for intra- and interleg coordination during walking. The importance of the fCO in motor control in D. melanogaster has been considered rather minor, though research into the topic is very limited. In the work laid out herein, I highlight the complexity of the Drosophila fCO and its role in the determination of locomotor behavior
