Temporal patterns of neurogenesis in avian cranial sensory and autonomic ganglia

Abstract

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.

Cell proliferation and cell death in the developing chick inner ear: Spatial and temporal patterns

“…1E-G, 2-6). The location of the proliferating cells was not uniform, as noted previously from thymidine-labeling studies (D'Amico-Martel, 1982). From stages 21 to 26, the ventral part of the vestibular ganglion displayed a higher number of BrdUϩ cells compared with the dorsal part.…”

“…When the ganglion first arises, it forms a complex with the neurons forming the proximal part of cranial ganglion VII (the facial root ganglion). After the auditory and vestibular parts of the ganglion separate, the vestibular ganglion and the proximal facial root ganglion remain adjacent and difficult to distinguish in standard histological sections (D'Amico-Martel, 1982). We outlined this proximal-VII/VIII ganglionic complex with a dashed line in Figures 2-6.…”

“…The early cell death on embryonic days 4 and 5, whereas modest in terms of total number of cells, occurs shortly after the first peripheral fibers penetrate the otic epithelium (Whitehead and Morest, 1985). This is a time when many ganglion neurons have not yet completed their final mitotic division; ganglion cells are born between embryonic days 2 and 5 in the vestibular ganglion and 4 and 7 in the auditory ganglion (D'Amico-Martel, 1982). We speculate that this early period of programmed cell death might be used to eliminate inappropriate cells, such as non-ganglion cells that had become trapped in the ganglion as it was forming, or ganglion cells that failed to develop normally.…”

“…Enlargement and morphogenesis of the otocyst is likely to depend on cellular division, growth, migration, differentiation, and apoptosis. Several previous studies on proliferation in the ear focused on terminal division, or birthdates, of various cell types (Ruben, 1967;D'Amico-Martel, 1982;Katayama and Corwin, 1989). Others attempted to understand the molecular control of proliferation in the otocyst; nerve growth factor (NGF), insulin-like growthfactors (IGFs), cyclin-dependent kinase inhibitors, retinoic acid, and proto-oncogenes have all been implicated (Bernd and Represa, 1989;Von Bartheld et al, 1991;León et al, 1995;Chen and Segil, 1999;Sanz et al, 1999).…”

Class III ?-tubulin expression in sensory and nonsensory regions of the developing avian inner ear

“…At least two neuronal cell types are generated by the otic epithelium: the neurons of the acoustic-vestibular ganglion (AVG) which migrate from the otic epithelium to the ganglion (D'Amico-Martel and Noden, 1983), and sensory hair cells. The sensory hair cells appear to be generated within the otic epithelium after the ganglion cell precursors migrate (D'Amico-Martel, 1982;Katayama and Corwin, 1989). We do not know, however, whether the cells migrating to the AVG originate from the same regions in which sensory hair cells subsequently develop.…”