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, 211 (3), 335-51

The Development of the Neural Crest in the Human

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The Development of the Neural Crest in the Human

Ronan O'Rahilly et al. J Anat.

Abstract

The first systematic account of the neural crest in the human has been prepared after an investigation of 185 serially sectioned staged embryos, aided by graphic reconstructions. As many as fourteen named topographical subdivisions of the crest were identified and eight of them give origin to ganglia (Table 2). Significant findings in the human include the following. (1) An indication of mesencephalic neural crest is discernible already at stage 9, and trigeminal, facial, and postotic components can be detected at stage 10. (2) Crest was not observed at the level of diencephalon 2. Although pre-otic crest from the neural folds is at first continuous (stage 10), crest-free zones are soon observable (stage 11) in Rh.1, 3, and 5. (3) Emigration of cranial neural crest from the neural folds at the neurosomatic junction begins before closure of the rostral neuropore, and later crest cells do not accumulate above the neural tube. (4) The trigeminal, facial, glossopharyngeal and vagal ganglia, which develop from crest that emigrates before the neural folds have fused, continue to receive contributions from the roof plate of the neural tube after fusion of the folds. (5) The nasal crest and the terminalis-vomeronasal complex are the last components of the cranial crest to appear (at stage 13) and they persist longer. (6) The optic, mesencephalic, isthmic, accessory, and hypoglossal crest do not form ganglia. Cervical ganglion 1 is separated early from the neural crest and is not a Froriep ganglion. (7) The cranial ganglia derived from neural crest show a specific relationship to individual neuromeres, and rhombomeres are better landmarks than the otic primordium, which descends during stages 9-14. (8) Epipharyngeal placodes of the pharyngeal arches contribute to cranial ganglia, although that of arch 1 is not typical. (9) The neural crest from rhombomeres 6 and 7 that migrates to pharyngeal arch 3 and from there rostrad to the truncus arteriosus at stage 12 is identified here, for the first time in the human, as the cardiac crest. (10) The hypoglossal crest provides cells that accompany those of myotomes 1-4 and form the hypoglossal cell cord at stages 13 and 14. (11) The occipital crest, which is related to somites 1-4 in the human, differs from the spinal mainly in that it does not develop ganglia. (12) The occipital and spinal portions of the crest migrate dorsoventrad and appear to traverse the sclerotomes before the differentiation into loose and dense zones in the latter. (13) Embryonic examples of synophthalmia and anencephaly are cited to emphasize the role of the neural crest in the development of cranial ganglia and the skull.

Figures

Fig. 4
Fig. 4
The neural crest at stage 12. The planes of sections of A, C, and D are shown in the key. Alum cochineal/haematoxylin and eosin. (A) Optic crest is clearly emigrating from the optic vesicle. (B) Spinal crest in the thoracic region. The roof cells of the neural tube resemble the crest cells that are visible between the tube and the dermatomyotomes. (C) The trigeminal ganglion is connected here to the surface ectoderm by cells believed to be emigrating from the latter. (D) The facial ganglion (seen here below the otic primordium) of the embryo shown in C. The cellular columns of the neural wall continue into the ganglion and a basement membrane is absent at this level.
Fig. 1
Fig. 1
The neural crest in graphic reconstructions at stages 9 to 13. Right lateral views. The embryos are drawn at decreasing magnifications. (A) Mesencephalic crest (orange) has begun to form in stage 9. (B) Neural crest from the widely open rostral neuropore (thick curved black line) in stage 10. The preotic crest (mesencephalic, trigeminal, and facial components) is emigrating from the neural folds. The postotic and occipitospinal crest is present. (C) Trigeminal (green) and facial (yellow) ganglia have appeared in stage 11. Migration of the crest (arrows) continues. The uppermost arrow indicates a frontonasal component. Migration to pharyngeal arches 1 and 2 (arrows) is from closed neural tube. Rhombomeres 1, 3, and 5 are now seen to be crest-free. (D) The cardiac and hypoglossal crest at stage 12. The cardiac crest arises from Rh. 6 and Rh. 7 and migrates to the truncus arteriosus, which it surrounds. Hypoglossal crest at this stage occupies mainly pharyngeal arch 4. Trigeminal and facial crest migrate (arrows) into arches 1 and 2 respectively. (E) Placodal activity at stage 13. Placodes of pharyngeal arches 1–4 are indicated. The hypoglossal cord reaches pharyngeal arch 2. Colours: orange, mesencephalic; green, trigeminal; yellow, facial; grey, hypoglossal; violet, cardiac; red, aortic arches.
Fig. 2
Fig. 2
Neural crest at stage 10. Alum cochineal. (A) Mesencephalic crest from the neural folds can be seen above. The crest cells are darker and more rounded than those of the mesoderm. The optic sulcus (arrow) is visible and the optic primordium is present. (B) Facial crest in stage 10 is emerging laterad from the wall of the neural groove. (C) Hypoglossal crest is migrating between the neural tube and the first somite. The planes of section are shown in the key. Figure 2B is taken from R. O’Rahilly and F. Müller, The Embryonic Human Brain, 3rd edn. Copyright ©, 2006, Wiley-Liss. Reprinted by permission of John Wiley and Sons, Inc.
Fig. 3
Fig. 3
Otic crest at stage 11. The otic pit can be seen above and also cellular strands from its edge, especially lateral to (to the left of) the facial ganglion. Azan.
Fig. 5
Fig. 5
The development of the occipitospinal neural crest, based on photomicrographs of serial sections. (A) The spinal crest at stage 12 does not extend beyond the dermatomyotomes. The main (ventrolateral) migratory pathway detectable from sections is shown by an arrow. (B) The crest at stage 13 has given rise to spinal ganglia. The myotomic plates are found laterally, and ventrally the sclerotomes show dense and loose portions. Motor fibres penetrate the loose portions. (C) The neural tube at stage 15 is covered by pia mater, believed to be derived from the neural crest (Sensenig, 1951; O’Rahilly and Müller, 1986). Dorsal and ventral roots are forming a spinal nerve. (D) Lateral view of the occipitospinal transition at stage 15. Spinal ganglia and sclerotomes are in register. No ganglia form in the occipital part. Nerve fibres of XII pass through the loose moieties of the sclerotomes, as do also the spinal nerves. Occipital and spinal sclerotomes are in register. (The dense areas will develop into the lateral parts of the basioccipital and into the neural arches of the cervical vertebrae.)
Fig. 6
Fig. 6
The postotic neural crest in stage 13 is still a continuous band. Superior and inferior ganglia of IX and X are present, as are also the cervical and some thoracic ganglia. The ventral spinal roots are included, but the hypoglossal crest is not shown. CN1, cervical nerve 1. LL, lower limb bud. TN1, thoracic nerve 1. UL, upper limb bud.
Fig. 7
Fig. 7
Cranial ganglia at stage 13 seen in a laterally situated sagittal, azan-stained section. The pharyngeal arches and the cranial ganglia show a segmental arrangement. Scale bar: 0.6 mm.
Fig. 8
Fig. 8
Placodal activity in stage 13. The planes of sections of A and B are shown in the key. The site of the epipharyngeal placodes is indicated in the key drawings here by brackets, the shorter of which marks the portion where the basement membrane is clearly interrupted. Haematoxylin and eosin. (A) Pharyngeal arch 2 containing facial crest migrating from the facial ganglion. The placode is recognizable by its much higher surface ectoderm compared with the regular ectoderm. Emigrating placodal cells can be observed where the basement membrane is interrupted. (B) Pharyngeal arch 4 with migrating vagal crest. The placode delivers cells to the crest. The future superior vagal ganglion is slightly less compact than the inferior, which adheres to the placode.
Fig. 9
Fig. 9
The relationship of spinal ganglia to sclerotomes in stage 14. Haematoxylin and eosin. In this laterally situated sagittal section the accessory nerve of one side can be seen in the upper right-hand corner. The ganglia extend over most of the medial myotomic surfaces, which are not seen here, that is, over the whole segment. The nerve fibres appear to be ‘squeezed’ through the loose rostral parts of the sclerotomes where also the blood vessels (horizontal dark streaks) are located (cf Fig. 5D). A sclerotome is outlined in the key drawing. Ao., aorta.
Fig. 10
Fig. 10
Nasal crest is arising from the tip of the nasal pit at stage 20 and migrating rostrocaudad towards the basal region of the diencephalon. Azan. From R. O’Rahilly and F. Müller, ‘The Embryonic Human Brain,’ 3rd Ed. Copyright ©, 2006, Wiley-Liss. Reprinted by permission of John Wiley and Sons, Inc.

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