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Responses of a Locust Looming Sensitive Neuron, Flight Muscle Activity and Body Orientation to Changes in Object Trajectory, Background Complexity, and Flight Condition



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Survival is one of the highest priorities of any animal. Interaction in the environment with conspecifics, predators, or objects, is driven by evolution of systems that can efficiently and rapidly respond to potential collision with these stimuli. Flight introduces further complexity for a collision avoidance system, requiring an animal to compute air speed, wind speed, ground speed, as well as transverse and longitudinal image flow, all within the context of detecting an approaching object. Understanding the mechanisms underlying neural control and coordination of motor systems to produce behaviours in response to the natural environment is a main goal of neuroethology. Locusts have a tractable nervous system, and a robust, reproducible collision avoidance response to looming stimuli. This tractable system allows recording from the nerve cord and flight muscles with precision and reliability, allowing us to answer important questions regarding the neuronal control of muscle coordination and, in turn, collision avoidance behaviour during flight. In flight, a collision avoidance behaviour will most often be a turn away from the approaching stimulus. I tested the hypothesis that during loosely tethered flight, synchrony between flight muscles increases just prior to the initiation of a turn and that muscle synchronization would correlate with body orientation changes during flight steering. I found that hind and forewing flight muscle synchronization events correlated strongly with forewing flight muscle latency changes, and to pitch and roll body orientation changes in response to a lateral looming visual stimulus. These findings led me to investigate further the role of the looming-sensitive descending contralateral movement detector (DCMD) neuron in flight muscle coordination and the initiation of forewing asymmetry in rigidly tethered locusts that generate a flight-like rhythm. By conducting simultaneous recordings from the nerve cord, forewing flight muscles, and visually recording the wing positions within the same flying animal, I hypothesized that DCMD burst properties would correlate with flight muscle activity changes and the initiation of wing asymmetry associated with turning behaviour. Furthermore, I accessed the effect of manipulating background complexity of the locust’s visual environment, looming object trajectory, and the putative effect of mechanosensory feedback during flight, on DCMD burst firing rate properties. DCMD burst properties were affected by changes in background complexity and object trajectory, and most interestingly during flight. This suggests that reafferent feedback from the flight motor system modulates the DCMD signal, and therefore represents a more naturalistic representation of collision avoidance behaviour. A pivotal discovery in my study was the temporal role of bursting in collision avoidance behaviour. I found that the first burst in a DCMD spike train represents the earliest detectable neuronal event correlated with muscle activity changes and the creation of wing asymmetry. I found strong correlations across all object trajectories and background complexities, between the timing of the first bursts, flight muscle activity changes and the initiation of wing asymmetry. These findings reinforce the importance of the temporal properties of DCMD bursting in collision avoidance behaviour.



Neuroethology, Behaviour, Electrophysiology, Collision Avoidance, Flight, Flight Muscle, DCMD



Doctor of Philosophy (Ph.D.)






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