Log in

The rostrocaudal organization in the dorsal root ganglia of the rat: a consequence of plexus formation?

  • Review Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

The dorsal root ganglia (DRGs) of the rat have a rostrocaudal organization. This organization can most easily be demonstrated in fetal and neonatal rats because the spatial relationships of their DRGs are maintained better in tissue sections than those of mature rats. This review is concerned with the way in which the rostrocaudal organization of the DRGs is generated. Wheat germ agglutinin — horseradish peroxidase/horseradish peroxidase labeling of peripheral nerves of the brachial and lumbar plexuses shows that the position of the somata of the sensory neurons of the labeled nerves can be restricted to rostral or caudal halves of DRGs. Labeling of the thoracic nerve or its branches always results in labeling throughout the entire thoracic DRG. After application of the marker to forelimb nerves, it was observed that whenever a DRG is labeled only partially, its spinal nerve is correspondingly labeled partially as well. These data suggest that the rostrocaudal organization in the DRG is related to the formation of the plexuses. During development nerve fibers can be segmentally labeled, using the subdivision of the DRGs into a rostral and a caudal half to keep together as they find their way through the plexus. Application of label to forelimb skin, hindlimb skin and even thoracic skin can result in labeling of rostral or caudal halves of a DRG. A possible explanation might be that each dermatome can be divided into a skin area innervated by the rostral half of a DRG and a skin area innervated by the caudal half of the same dorsal root ganglion. In the rat, the segmental sensory innervation of muscles during development has not yet been investigated. The question of whether the segmental unit of innervation of a muscle is a whole DRG or half a DRG therefore still remains unanswered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arvidsson J, Pfaller K (1990) Central projections of C4–C8 dorsal root ganglia in the rat studied by anterograde transport of WGA-HRP. J Comp Neurol 292:349–362

    Google Scholar 

  • Baron R, Jänig W, Kollmann W (1988) Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat. J Comp Neurol 275:460–468

    Google Scholar 

  • Bolk L (1910) De segmentale innervatie van romp en ledematen by den mensch. De Erven F Bohn, Haarlem

    Google Scholar 

  • Bronner-Fraser M (1993) Mechanisms of neural crest cell migration. Bioessays 15:221–230

    Google Scholar 

  • Burton H, McFarlane JJ (1973) The organization of the seventh lumbar spinal ganglion of the cat. J Comp Neurol 149:215–232

    Google Scholar 

  • Castro-Lopes JM, Coimbra A (1991) Spinal cord projections of the rat main forelimb nerves, studied by transganglionic transport of WGA-HRP and by the disappearance of acid phosphatase. Brain Res 542:187–192

    Google Scholar 

  • Cole JP, Lesswing AL, Cole JR (1968) An analysis of the lumbosacral dermatomes in Man. Clin Orthop 61:241–247

    Google Scholar 

  • Devor M, Claman D (1980) Map** and plasticity of acid phosphatase afferents in the rat dorsal horn. Brain Res 190:17–28

    Google Scholar 

  • Dykes RW, Terzis JK (1981) Spinal nerve distributions in the upper limb: the organization of the dermatome and afferent myotome. Philos Trans R Soc Lond [Biol] 293:509–554

    Google Scholar 

  • Friede RL, Samorajski T (1968) Myelin formation in the sciatic nerve of the rat. J Neuropathol Exp Neurol 27:546–570

    Google Scholar 

  • Grant G (1993) Projection patterns of primary sensory neurons studied by transganglionic methods: somatotopy and target-related organization. Brain Res Bull 30:199–208

    Google Scholar 

  • Gray H, Williams PL, Warwick R (1980) Gray's anatomy, 36th edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Greene EC (1955) Anatomy of the rat. Hafner, New York

    Google Scholar 

  • Hollyday M (1980) Organization of motor pools in the chick lumbar lateral motor column. J Comp Neurol 194:143–170

    Google Scholar 

  • Honig MG (1982) The development of sensory projection patterns in embryonic chick hind limb. J Physiol (Lond) 330:175–202

    Google Scholar 

  • Kausz M, Réthelyi M (1985) Lamellar arrangement of neuronal somata in the dorsal root ganglion of the cat. Somatosens Res 3:193–204

    Google Scholar 

  • Keynes RJ, Stern CD (1984) Segmentation in the vertebrate nervous system. Nature 310:786–789

    CAS  PubMed  Google Scholar 

  • Kuhn RA (1953) Organization of tactile dermatomes in cat and monkey. J Neurophysiol 16:169–182

    Google Scholar 

  • La Vail JH, La Vail MM (1974) The retrograde intra-axonal transport of horseradish peroxidase in the chick visual system: a light and electron microscopic study. J Comp Neurol 157:303–358

    Google Scholar 

  • LaMotte CC, Kapadia SE, Shapiro CM (1991) Central projections of the sciatic, saphenous, median and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and Wheat Germ Agglutinin-HRP (WGA-HRP). J Comp Neurol 311:546–562

    Google Scholar 

  • Lance-Jones C (1988) The somitic level of origin of embryonic chick hindlimb muscles. Dev Biol 126:394–407

    Google Scholar 

  • McLachlan EM, Jänig W (1983) The cell bodies of origin of sympathetic and sensory axons in some skin and muscle nerves of the cat hindlimb. J Comp Neurol 214:115–130

    Google Scholar 

  • Mesulam MM (1982) Tracing neural connections with horseradish peroxidase. IBRD handbook series. Wiley, Chichester

    Google Scholar 

  • Molander C, Grant G (1985) Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by trans-ganglionic transport of WGA-HRP conjugate. J Comp Neurol 237:476–484

    CAS  PubMed  Google Scholar 

  • Molander C, Grant G (1986) Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat. Neuroscience 19:297–312

    Google Scholar 

  • Molander C, Grant G (1987) Spinal cord projections from hindlimb muscle nerves in the rat studied by transganglionic transport of horseradish peroxidase, wheat germ agglutinin conjugated horseradish peroxidase, or horseradish peroxidase with dimethylsulfoxide. J Comp Neurol 260:246–255

    Google Scholar 

  • Myles LM, Gilmour JA, Glasby MA (1992) Effects of different methods of peripheral nerve repair on the number and distribution of muscle afferent neurons in rat dorsal root ganglion. J Neurosurg 77:457–462

    Google Scholar 

  • Neuhuber WL, Zenker W (1989) Central distribution of cervical primary afferents in the rat, with emphasis on proprioceptive projections to vestibular, perihypoglossal, and upper thoracic spinal nuclei. J Comp Neurol 280:231–253

    CAS  PubMed  Google Scholar 

  • Nyberg G, Blomqvist A (1985) The somatotopic organization of forelimb cutaneous nerves in the brachial dorsal horn: an anatomical study in the cat. J Comp Neurol 242:28–39

    Google Scholar 

  • Peyronnard JM, Charron LF, Lavoie J, Messier JP (1986) Motor, sympathetic and sensory innervation of rat skeletal muscles. Brain Res 373:288–302

    Google Scholar 

  • Pfaller K, Arvidsson J (1988) Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin. J Comp Neurol 268:91–108

    Google Scholar 

  • Remak R (1855) Untersuchungen über die Entwicklung der Wirbeltiere. Reimer, Berlin

    Google Scholar 

  • Rickman M, Fawcett JW, Keynes RJ (1985) The migration of neural crest cells and the growth of motor axons through the rostral half of the chick somite. J Embryol Exp Morphol 90:431–455

    Google Scholar 

  • Rivero-Melian C, Grant G (1990) Distribution of lumbar dorsal root fibers in the lower thoracic and lumbosacral spinal cord of the rat studied with choleragenoid horseradish peroxidase conjugate. J Comp Neurol 299:470–481

    Google Scholar 

  • Romer AS (1927) The development of the thigh musculature of the chick. J Morphol Physiol 43:347–385

    Google Scholar 

  • Scott SA (1982) The development of the segmental pattern of skin sensory innervation in embryonic chick hind limb. J Physiol (Lond) 330:203–220

    Google Scholar 

  • Sherrington CS (1893) Experiments in the examination of the peripheral distribution of the fibers of the posterior roots of some spinal nerves. I. Philos Trans R Soc Lond [Biol] 184:641–763

    Google Scholar 

  • Sima A (1974) Studies on fibre size in develo** sciatic nerve and spinal roots in normal, undernourished and rehabilitated rats. Acta Physiol Scand 406:1–55

    Google Scholar 

  • Smith CL (1983) The development and postnatal organization of primary afferent projections to the rat thoracic spinal cord. J Comp Neurol 220:29–43

    Google Scholar 

  • Smith CL (1986) Sensory neurons supplying touch domes near the body midlines project bilaterally in the thoracic spinal cord of rats. J Comp Neurol 245:541–552

    Google Scholar 

  • Swett JE, Woolf CJ (1985) The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J Comp Neurol 220:66–77

    Google Scholar 

  • Teillet M, Kalcheim C, Le Douarin NM (1987) Formation of the dorsal root ganglia in the avian embryo: segmental origin and migratory behavior of neural crest progenitor cells. Dev Biol 120:329–347

    CAS  PubMed  Google Scholar 

  • Verbout AJ (1985) The development of the vertebral column. Adv Anat Embryol Cell Biol 90:1–122

    CAS  PubMed  Google Scholar 

  • Werner W, Whitsel BL (1967) Topology of dermatomal projection in the medial lemniscal system. J Physiol (Lond) 192:123–144

    Google Scholar 

  • Wessels WJT (1991) Development of the peripheral sensory innervation of the rat hindlimb and its central connections: a WGA-HRP study. Thesis, Leiden

  • Wessels WJT, Marani E (1993) A rostrocaudal somatotopic organization in the brachial dorsal root ganglia of neonatal rats. Clin Neurol Neurosurg 95: S3-S11

    Google Scholar 

  • Wessels WJT, Feirabend HKP, Marani E (1990a) Evidence for a rostrocaudal organization in dorsal root ganglia during development as demonstrated by intra-uterine WGA-HRP injections into the hindlimb of rat fetuses. Dev Brain Res 54:273–281

    Google Scholar 

  • Wessels WJT, Feirabend HKP, Marani E (1990b) Somatotopic organization in the sensory innervation of the rat hindlimb during development, using half dorsal root ganglia as subsegmental units. Eur J Morphol 28:394–403

    Google Scholar 

  • Woodbury CJ, Scott SA (1991) Somatotopic organization of hindlimb skin sensory inputs to the dorsal horn of hatchling chicks (Gallus g. domesticus). J Comp Neurol 314:237–256

    Google Scholar 

  • Woolf CJ, Fitzgerald M (1986) Somatotopic organization of cutaneous afferent terminals and dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord. J Comp Neurol 251:517–531

    Google Scholar 

  • Wortham RA (1948) The development of the muscles and tendons in the lower leg and foot of chick embryos. J Morphol 83:105–148

    Google Scholar 

  • Ygge J (1984) On the organization of the thoracic spinal ganglion and nerve in the rat. Exp Brain Res 55:395–401

    Google Scholar 

  • Ygge J (1989) Central projections of the rat radial nerve investigated with transganglionic degeneration and transganglionic transport of horseradish peroxidase. J Comp Neurol 279:199–211

    Google Scholar 

  • Ygge J, Grant G (1983) The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglionic transport of horseradish peroxidase. J Comp Neurol 216:1–9

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wessels, W.J.T., Feirabend, H.K.P. & Marani, E. The rostrocaudal organization in the dorsal root ganglia of the rat: a consequence of plexus formation?. Anat Embryol 190, 1–11 (1994). https://doi.org/10.1007/BF00185841

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00185841

Key words

Navigation