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Journal of Neuroscience, Vol 7, 1816-1832, Copyright © 1987 by Society for Neuroscience
Naturally-occurring neuron death in the ciliary ganglion of the chick embryo following removal of preganglionic input: evidence for the role of afferents in ganglion cell survival
S Furber, RW Oppenheim and D Prevette
With only a few exceptions, most investigations of the mechanisms involved
in naturally-occurring neuron death have focused on interactions between
neurons and their targets, with much less attention having been paid to the
possible role of the afferent inputs in this phenomenon. This is true of
the avian ciliary ganglion (CG), which is composed of a population of
peripheral autonomic neurons that project to smooth and striated
musculature in the eye and which receive afferents from a single source,
the accessory oculomotor nucleus (AON), which is the avian homolog of the
Edinger-Westphal nucleus. Although several lines of evidence strongly
support the important role of targets in regulating the death and survival
of CG neurons, the role of afferents has not yet been systematically
examined. Following the destruction of the AON on embryonic day (E) 4,
which is several days before the onset of normal cell death in the CG, we
have found that by the end of the normal cell death period (E14-E15),
85-90% of the CG neurons degenerate and die, compared to 50% in controls.
This is comparable to the amount of induced cell loss that occurs following
removal of the optic vesicle containing the CG targets. The neurons
surviving after deafferentation appear to be sustained by some influence
from their targets since combined deafferentation and eye removal results
in the loss of virtually all neurons in the CG. Following deafferentation
of the CG on E4, the ganglion develops normally up to about E10, after
which a precipitous loss of cells occurs. Based on several kinds of
evidence (e.g., axon counts, silver stain, retrograde labeling of the CG),
we conclude that the deafferented neurons project to and innervate their
muscular targets in the eye. Therefore, the increased cell death following
deafferentation cannot be due to the failure of deafferented neurons to
contact their targets. The deafferented neurons undergo a normal sequence
of initial ultrastructural differentiation. When they do begin to
degenerate, the type of fine structural changes they exhibit appears
indistinguishable from the degenerative changes observed in control
embryos. Neurons in deafferented ganglia were occasionally observed to
receive synaptic contacts, which we attribute to aberrant intraganglionic
connections induced by deafferentation. These contacts probably play
little, if any, role in the maintenance of neurons since, as noted above,
following combined deafferentation and target deletion virtually all
neurons degenerate and die.(ABSTRACT TRUNCATED AT 400 WORDS)
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