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The Search for and Formation of Synapses on Zebrafish Motoneurons Across Natural Periods of Activity and Quiescence

Author
DiPietro, Joseph V.
Abstract
The work presented in this dissertation is an in-depth analysis of how a single
neuron, the primary motoneuron of zebrafish, searches for and forms
synapses across the circadian periods of activity and quiescence that occur
from day to night. Dendrites repeatedly extend and retract filopodia in a
search for synapses, the formation of which stabilizes the process, leading to
growth of the arbor. I first focused my attention on zebrafish primary neurons
during the day to explore, for the first time, the search process from the level
of individual filopodial dynamics to the distribution of dynamics across an
entire dendritic arbor. We found the magnitude of searching at individual
locations varied tremendously across locations, with filopodia extending and
retracting as much as 3 microns and averaging about 12 dynamics events per
filopodium in a given 30-minute period. An analysis of the temporal sequence
of these dynamic events showed the pattern of dynamics at individual
locations also varied tremendously. Only retractions showed a consistent
trend, tending to stabilize for some time and rarely being followed by an
extension. This shows that dendrites are not just simply extending and
stabilizing filopodia. Instead, filopodia at each individual location are engaging
in highly dynamic periods of searching, with most extensions retracting within
5 minutes. Only about 4% of extensions survive for an hour or more, possibly
representing the formation of synapses. We further find that these dynamic
locations are equally distributed across the dendrite arbor independent of their
individual dynamics and only the furthest extents of dendrite had higher than
average numbers of motile locations, suggesting the search is largely
unbiased except for those furthest regions. A comparison of how the search
differs between day and night shows surprisingly, that the magnitude of this
searching increases at night, a quiescent time, when motoneuron are much
less active. While the extensions at night are less likely to stabilize, this
increase in searching may partly account for these cells still forming synapses
at a similar rate as during the day, with only the rate of synapse removal
changing, increasing significantly at night. These results demonstrate that
during times of behavioral and activity quiescence, neurons continue to search
for and form synapses at the expense of losing others, providing potential
insight into the role these quiescent states may play in network development
and neuronal plasticity.
Date Issued
2017-08-30Subject
dendrites; motoneurons; sleep; synapses; zebrafish; Development; Neurosciences
Committee Chair
Fetcho, Joseph R.
Committee Member
Harris-Warrick, Ronald Morgan; Bass, Andrew Howard; Schaffer, Chris
Degree Discipline
Neurobiology and Behavior
Degree Name
Ph. D., Neurobiology and Behavior
Degree Level
Doctor of Philosophy
Type
dissertation or thesis