The method of embryonic tissue transplantation was used to confirm the dual origin of avian cranial sensory ganglia, to map precise locations of the anlagen of these sensory neurons, and to identify placodal and neural crest-derived neurons within ganglia. Segments of neural crest or strips of presumptive placodal ectoderm were excised from chick embryos and replaced with homologous tissues from quail embryos, whose cells contain a heterochromatin marker. Placode-derived neurons associated with cranial nerves V, VII, IX, and X are located distal to crest-derived neurons. The generally larger, embryonic placodal neurons are found in the distal portions of both lobes of the trigeminal ganglion, and in the geniculate, petrosal and nodose ganglia. Crest-derived neurons are found in the proximal trigeminal ganglion and in the combined proximal ganglion of cranial nerves IX and X. Neurons in the vestibular and acoustic ganglia of cranial nerve VIII derive from placodal ectoderm with the exception of a few neural crest-derived neurons localized to regions within the vestibular ganglion. Schwann sheath cells and satellite cells associated with all these ganglia originate from neural crest. The ganglionic anlagen are arranged in cranial to caudal sequence from the level of the mesencephalon through the third somite. Presumptive placodal ectoderm for the VIIIth, the Vth, and the VIIth, IXth, and Xth ganglia are located in a medial to lateral fashion during early stages of development reflecting, respectively, the dorsolateral, intermediate, and epibranchial positions of these neurogenic placodes.
Avian cranial sensory ganglia are embryonically derived from neural crest and epidermal placodes. Cells from these two populations interact with each other and with other components of their environment to influence the complex structural and functional organization of the ganglia. To help understand these processes, the times of terminal mitosis of cranial sensory neuroblasts were established. Birthdate patterns within each ganglion are described with particular attention given to the structural organization of the VII-VIII ganglionic complex. Birthdate information on cranial autonomic ganglia is also included. Chick embryos ranging in age from 1 to 8 days of incubation were treated with 3H-thymidine and sacrificed on embryonic day 8, 10, or 18. Large, placode-derived neurons are generated between days 2 and 5 of incubation. Embryonically smaller, neural crest-derived cells leave the proliferative pool between days 4 and 7. Neurons of the acoustic ganglion cease their mitotic activity in an apical to basal fashion and are the only placodal neurons to form later than day 5. Of the cranial autonomic ganglia, the period of neuron production is best defined for the ciliary ganglion, where it is 2.5-5.5 days of incubation. Most later-dividing neuroblasts in the ciliary ganglion belong to the choroid cell population. Temporal patterns of neurogenesis are discussed in relationship to other aspects of sensory gangliogenesis including embryonic origin of neurons, condensation of ganglionic anlagen, cell degeneration, and cytological characteristics of mature ganglia.
The avian trigeminal ganglion, which is embryonically derived from the neural crest and epidermal placodes, consists of two topographically segregated classes of immature neurons, large and small, during the second week of incubation, and two neuronal cell types, dark and light, interspersed throughout the mature ganglion. In order to establish the times of terminal mitosis of trigeminal sensory neurons, embryos were treated with [3H]thymidine during the first week of incubation and their ganglia fixed on embryonic day 11. The embryonically large, distal, placodal-derived neurons are generated between days 2 and 5, while the small, proximal, neural crest-derived neurons are formed mostly between days 4 and 7. By comparing the locations of labeled cells in ganglia treated with isotope but fixed on day 18 of incubation with their 11-day counterparts, we have proved that there are no morphogenetic rearrangements of neurons during the final week of incubation. Thus, no unique relationship exists between the two neuron types in the mature ganglion and the two cell classes in the immature trigeminal. Therefore, both the light and the dark neurons in the mature trigeminal ganglion arise from neural crest as well as placodal primordia.
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