Responses of a Locust Looming Sensitive Neuron, Flight Muscle Activity and Body Orientation to Changes in Object Trajectory, Background Complexity, and Flight Condition
Date
2019-08-29
Authors
Journal Title
Journal ISSN
Volume Title
Publisher
ORCID
0000-0002-7905-9878
Type
Thesis
Degree Level
Doctoral
Abstract
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.
Description
Keywords
Neuroethology, Behaviour, Electrophysiology, Collision Avoidance, Flight, Flight Muscle, DCMD
Citation
Degree
Doctor of Philosophy (Ph.D.)
Department
Biology
Program
Biology