Segmental patterns of neuronal development in the chick hindbrain

Abstract

Identification of specific neuronal populations and their projections in the developing hindbrain reveals a segmental organization in which pairs of metameric epithelial units cooperate to generate the repeating sequence of cranial branchiomotor nerves. Neurogenesis also follows a two-segment repeat, suggesting parallels with insect pattern formation.

Constructing the hindbrain: Insights from the zebrafish

“…Hindbrain neuroanatomy corresponds with morphological segmentation ( Fig. 3; Hanneman et al, 1988;Lumsden and Keynes, 1989;Trevarrow et al, 1990). This correspondence, although true of many neuronal types, is most dramatically illustrated by the individually identified reticulospinal interneurons of the zebrafish.…”

“…3A; Mendelson, 1986a,b;Metcalfe et al, 1986). In the chick, several lines of evidence point toward a two-segment periodicity within the hindbrain: the branchiomotor nerves that innervate the pharyngeal arches exit the hindbrain from even-numbered rhombomeres (Lumsden and Keynes, 1989); the timing of neuronal differentiation is delayed in odd-numbered rhombomeres (Lumsden and Keynes, 1989); cranial neural crest cells that contribute to the pharyngeal arches migrate from evennumbered rhombomeres ; and, finally, even-and odd-numbered rhombomeres exhibit different cell adhesive properties (Guthrie and Lumsden, 1991;Guthrie et al, 1993;Wizenmann and Lumsden, 1997). Many of these observations have also been made in the zebrafish, where cranial motor nerves sim- Hanneman et al, 1988), the rhombomeres are visible as a series of bulges along the anterior-posterior extent of the hindbrain (anterior to the left).…”

Turning heads: Development of vertebrate branchiomotor neurons

“…During development, the cranial motor ax-ons exit the brainstem through specific cranial nerves (nIII to nXII; see below). While axons of all somatomotor neurons, except nIV, exit the brain ventrally from the basal plate of the neural tube, all subtypes of visceromotor and branchiomotor axons exit the brainstem dorsally from the alar plate (Lumsden and Keynes, 1989).…”

“…The spinal accessory motor axons exit through cranial nerve XI and innervate neck muscles (Kandel et al, 2000). The homologues of these motor neurons are found in other vertebrates and innervate different but homologous muscles (Lumsden and Keynes, 1989;Gilland and Baker, 1993;Kontges and Lumsden, 1996;Schilling and Kimmel, 1997). For example, in zebrafish, the trigeminal and facial motor neurons innervate muscles in the jaw and jaw-support structures, respectively, while the glossopharyngeal and vagal motor neurons innervate gill muscles (Hatta et al, 1990;Schilling and Kimmel, 1997;Higashijima et al, 2000).…”

Significance of the cranial neural crest

“…The neuronal cells that are formed within these placodes then move internally to the site of ganglion formation wherein they differentiate and send out axons toward their central and peripheral targets. Importantly, these ganglia innervate the hindbrain at specific axial levels (Lumsden and Keynes, 1989). The ax-ons of the trigeminal ganglion enter the hindbrain at rhombomere 2, those of the geniculate and vestibuloaccoustic, which is derived from the otic placode, at rhombomere 4, and the axons of the petrosal and the nodose ganglia at rhombomeres 6 and 7.…”