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.

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)