Mechanisms and function of asynchronous flight motor pattern generation
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Abstract
The vast majority of insect species and therefore overall species uses asynchronous
indirect flight as locomotion. Highly specialized muscles generate the power for the up
and down stroke of the wing and are the most energy consuming tissues in biology. In
Drosophila melanogaster a small network of five motoneurons (MNs) controls the
activity of the wing depressor muscle. The firing pattern of these five MNs is well
described, as a firing equidistantly splayed-out in time and in a preferred sequence.
The approximate firing rate of ~5 Hz is asynchronous, hence the name, to the muscle
contraction frequency of around 200 Hz. However, the mechanism that generates this
splayed firing pattern and the functional consequences are not yet fully understood.
This thesis will describe how the motor pattens are generated by a minimal central
pattern generating network (CPG) that consists of five electrically coupled MNs and
translates common, unpatterned, cholinergic, excitatory input into splayed-out
patterned firing of the MNs. For a given power demand all MNs fire at similar
frequencies but in specific sequences, thus desynchronized. Mechanistically, weak
electrical coupling together with a specific excitability class is responsible for network
desynchronization. Increasing or decreasing the expression of the gap junction protein
ShakB through genetic manipulation disrupts the splay state and increases MN firing
synchronization, leading to wingbeat frequency fluctuations during flight. Changing the
excitability class of the electrically coupled MNs using genetic manipulation of the Shab
delayed rectifier potassium channel also shifts network activity to a more synchronized
state. The functional consequence of the desynchronized splayed-out motor patterns
is to minimize fluctuations in wingbeat frequency. In vivo calcium imaging in single
muscle fibers reveals the kinetics of myoplasmic Ca2+-signals, which can be used to
link the MN firing pattern and the wingbeat frequency fluctuations: Splayed-out MN
firing minimizes fluctuations of average myoplasmic Ca2+-levels across all muscle
fibers, ultimately allowing a uniform wingbeat frequency and thus a steady power
output over time. The capability of weak electrical coupling together with the right
neuronal excitation class to desynchronize network activity has far-reaching
implications for neuronal network activity, since gap junction proteins are ubiquitously
expressed in neuronal networks throughout different species. It provides a novel
mechanism for different synchronization states in all nervous systems, from flies to
humans.