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. 1999 Jul;195(Pt 1):137–145. doi: 10.1046/j.1469-7580.1999.19510137.x

Compartmentalisation of the developing trigeminal ganglion into maxillary and mandibular divisions does not depend on target contact

LISA SCOTT 1 , MARTIN E ATKINSON 2 ,✉
PMCID: PMC1467973  PMID: 10473301

Abstract

During development axons contact their target tissues with phenomenal accuracy but the mechanisms that control this homing behaviour remain largely elusive. A prerequisite to the study of the factors involved in hard-wiring the nervous system during neurogenesis is an accurate calendar of developmental events. We have studied the maxillary and mandibular components of the trigeminal system to determine the stages during embryogenesis when a gross somatotopic order is first established within the trigeminal ganglion and the axons projecting to the brainstem. The retrograde transganglionic fluorescent tracers DiO and DiI were injected into the maxillary and mandibular arches or their derivatives in fixed mouse embryos staged between 13 and 40 somites (E9–E11). After 1–4 wk, the distribution of the 2 tracers was determined using confocal laser scanning microscopy. The first maxillary nerve cell bodies and their developing axons were labelled at the 30 somite stage (E10). This was 2 somite stages earlier than the mesencephalic nucleus and the ganglion cell bodies of the mandibular nerve. The gross somatotopic division of cells within the trigeminal ganglion projecting to the maxillary and mandibular targets was established by the 32 somite stage (E10). This arrangement was evident as 2 groups of cell bodies occupying adjacent but separate regions of the trigeminal ganglion. The central branches of the maxillary and mandibular cell bodies entered the metencephalon as 2 distinct bundles at the same stage. The trigeminal motor nucleus was first detected at the 38 somite stage (E10.5).

Gross somatotopy in the major divisions of the trigeminal ganglion is established before outgrowing axons have contacted their peripheral target tissue at E10.5. This suggests that target tissues do not induce somatotopy.

Keywords: Neurogenesis, somatotopy, dye tracing

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Selected References

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  1. Bernardo K. L., Ma P. M., Woolsey T. A. In vitro labeling of axonal projections in the mammalian central nervous system. J Neurosci Methods. 1986 Apr;16(2):89–101. doi: 10.1016/0165-0270(86)90042-7. [DOI] [PubMed] [Google Scholar]
  2. Brown K. E., Arends J. J., Wasserstrom S. P., Zantua J. B., Jacquin M. F., Woolsey T. A. Developmental transformation of dendritic arbors in mouse whisker thalamus. Brain Res Dev Brain Res. 1995 May 26;86(1-2):335–339. doi: 10.1016/0165-3806(94)00210-q. [DOI] [PubMed] [Google Scholar]
  3. Davies A. M., Lumsden A. G. Fasciculation in the early mouse trigeminal nerve is not ordered in relation to the emerging pattern of whisker follicles. J Comp Neurol. 1986 Nov 1;253(1):13–24. doi: 10.1002/cne.902530103. [DOI] [PubMed] [Google Scholar]
  4. Davies A., Lumsden A. Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion. J Comp Neurol. 1984 Feb 10;223(1):124–137. doi: 10.1002/cne.902230110. [DOI] [PubMed] [Google Scholar]
  5. Erzurumlu R. S., Jhaveri S. Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex. Brain Res Dev Brain Res. 1990 Nov 1;56(2):229–234. doi: 10.1016/0165-3806(90)90087-f. [DOI] [PubMed] [Google Scholar]
  6. Erzurumlu R. S., Jhaveri S. Trigeminal ganglion cell processes are spatially ordered prior to the differentiation of the vibrissa pad. J Neurosci. 1992 Oct;12(10):3946–3955. doi: 10.1523/JNEUROSCI.12-10-03946.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Erzurumlu R. S., Killackey H. P. Development of order in the rat trigeminal system. J Comp Neurol. 1983 Feb 1;213(4):365–380. doi: 10.1002/cne.902130402. [DOI] [PubMed] [Google Scholar]
  8. Gregg J. M., Dixon A. D. Somatotopic organization of the trigeminal ganglion in the rat. Arch Oral Biol. 1973 Apr;18(4):487–498. doi: 10.1016/0003-9969(73)90069-1. [DOI] [PubMed] [Google Scholar]
  9. Honig M. G., Hume R. I. Dil and diO: versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends Neurosci. 1989 Sep;12(9):333-5, 340-1. [PubMed] [Google Scholar]
  10. Hunt P., Gulisano M., Cook M., Sham M. H., Faiella A., Wilkinson D., Boncinelli E., Krumlauf R. A distinct Hox code for the branchial region of the vertebrate head. Nature. 1991 Oct 31;353(6347):861–864. doi: 10.1038/353861a0. [DOI] [PubMed] [Google Scholar]
  11. Hunt P., Wilkinson D., Krumlauf R. Patterning the vertebrate head: murine Hox 2 genes mark distinct subpopulations of premigratory and migrating cranial neural crest. Development. 1991 May;112(1):43–50. doi: 10.1242/dev.112.1.43. [DOI] [PubMed] [Google Scholar]
  12. Killackey H. P., Rhoades R. W., Bennett-Clarke C. A. The formation of a cortical somatotopic map. Trends Neurosci. 1995 Sep;18(9):402–407. doi: 10.1016/0166-2236(95)93937-s. [DOI] [PubMed] [Google Scholar]
  13. Landmesser L., Honig M. G. Altered sensory projections in the chick hind limb following the early removal of motoneurons. Dev Biol. 1986 Dec;118(2):511–531. doi: 10.1016/0012-1606(86)90023-0. [DOI] [PubMed] [Google Scholar]
  14. Lumsden A., Keynes R. Segmental patterns of neuronal development in the chick hindbrain. Nature. 1989 Feb 2;337(6206):424–428. doi: 10.1038/337424a0. [DOI] [PubMed] [Google Scholar]
  15. Lumsden A., Sprawson N., Graham A. Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo. Development. 1991 Dec;113(4):1281–1291. doi: 10.1242/dev.113.4.1281. [DOI] [PubMed] [Google Scholar]
  16. Ma P. M. Barrelettes--architectonic vibrissal representations in the brainstem trigeminal complex of the mouse. II. Normal post-natal development. J Comp Neurol. 1993 Jan 15;327(3):376–397. doi: 10.1002/cne.903270306. [DOI] [PubMed] [Google Scholar]
  17. Ma P. M. The barrelettes--architectonic vibrissal representations in the brainstem trigeminal complex of the mouse. I. Normal structural organization. J Comp Neurol. 1991 Jul 8;309(2):161–199. doi: 10.1002/cne.903090202. [DOI] [PubMed] [Google Scholar]
  18. Ma P. M., Woolsey T. A. Cytoarchitectonic correlates of the vibrissae in the medullary trigeminal complex of the mouse. Brain Res. 1984 Jul 23;306(1-2):374–379. doi: 10.1016/0006-8993(84)90390-1. [DOI] [PubMed] [Google Scholar]
  19. Moody S. A., Quigg M. S., Little C. D. Extracellular matrix components of the peripheral pathway of chick trigeminal axons. J Comp Neurol. 1989 May 1;283(1):38–53. doi: 10.1002/cne.902830105. [DOI] [PubMed] [Google Scholar]
  20. Rhoades R. W., Chiaia N. L., Macdonald G. J. Topographic organization of the peripheral projections of the trigeminal ganglion in the fetal rat. Somatosens Mot Res. 1990;7(1):67–84. doi: 10.3109/08990229009144698. [DOI] [PubMed] [Google Scholar]
  21. Riggott M. J., Moody S. A. Distribution of laminin and fibronectin along peripheral trigeminal axon pathways in the developing chick. J Comp Neurol. 1987 Apr 22;258(4):580–596. doi: 10.1002/cne.902580408. [DOI] [PubMed] [Google Scholar]
  22. Scott S. A. Skin sensory innervation patterns in embryonic chick hindlimb following dorsal root ganglion reversals. J Neurobiol. 1986 Nov;17(6):649–668. doi: 10.1002/neu.480170609. [DOI] [PubMed] [Google Scholar]
  23. Senft S. L., Woolsey T. A. Growth of thalamic afferents into mouse barrel cortex. Cereb Cortex. 1991 Jul-Aug;1(4):308–335. doi: 10.1093/cercor/1.4.308. [DOI] [PubMed] [Google Scholar]
  24. Stainier D. Y., Gilbert W. Neuronal differentiation and maturation in the mouse trigeminal sensory system, in vivo and in vitro. J Comp Neurol. 1991 Sep 8;311(2):300–312. doi: 10.1002/cne.903110210. [DOI] [PubMed] [Google Scholar]
  25. Stainier D. Y., Gilbert W. Pioneer neurons in the mouse trigeminal sensory system. Proc Natl Acad Sci U S A. 1990 Feb;87(3):923–927. doi: 10.1073/pnas.87.3.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wilkinson D. G., Bhatt S., Cook M., Boncinelli E., Krumlauf R. Segmental expression of Hox-2 homoeobox-containing genes in the developing mouse hindbrain. Nature. 1989 Oct 5;341(6241):405–409. doi: 10.1038/341405a0. [DOI] [PubMed] [Google Scholar]
  27. Woolsey T. A., Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 1970 Jan 20;17(2):205–242. doi: 10.1016/0006-8993(70)90079-x. [DOI] [PubMed] [Google Scholar]

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