Skip to main content
SpringerLink
Log in

On the development of the pyramidal tract in the rat

II. An anterograde tracer study of the outgrowth of the corticospinal fibers

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

An anterograde tracer study has been made of the developing corticospinal tract (CST) in the rat using wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP). Analysis of normal Rager stained material revealed that corticospinal axons reach upper cervical spinal cord levels at the day of birth (PO). Postnatal rats ranging in age from one (P1) to fourteen (P14) days received multiple WGA-HRP injections into the cortex of their left hemisphere and were allowed to survive for 24 h. The first labeled CST fibers caudally extend into the third thoracic spinal cord segment at P1; into the eighth thoracic segment at P3; into the first or second lumbar segment at P7 and into the second to third sacral segment at Pg. Thus the outgrowth of the leading ‘pioneer’ fibers of the CST is completed at P9 but later developing axons are continuously added even beyond P9. Quantitative analysis of the amount of label along the length of the outgrowing CST revealed a characteristic pattern of labeling varying with age. The most striking features of that pattern are: (1) the formation of two standing peaks at the level of the cervical and lumbar enlargements respectively and (2) the transient presence of a smaller running peak which moves caudally with the front of the outgrowing bundle. The standing peaks are ascribed to the branching of the axon terminals at both intumescences, whereas the running peak probably arises by the accumulation of tracer within the growth cones at the tips of the outgrowing CST axons. Factors such as the number of axons, the varying axon diameters, the branching collaterals, the presence of varicosities, the transport rate of the tracer, the uptake of the tracer at the injection site, which possibly may affect the amount of label present in both the entire bundle and in the individual axons are discussed. Current research is focused upon an analysis of the relation between the site of injection within the cortex and the pattern of labeling of the CST. A delay of two days was found between the arrival of the CST axons at a particular spinal cord level and their outgrowth into the adjacent spinal gray. However, combined HRP and electronmicroscopic experiments are necessary to determine the factors behind the maturation of the CST as well as the maturation of the spinal gray.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adams CE, Mihailoff GA, Woodward DJ (1983a) A transient component of the developing corticospinal tract arises in visual cortex. Neurosci Lett 36:243–248

    Google Scholar 

  • Adams CE, Wooward DJ, Mihailoff GA (1983b) Development of sensorimotor and visual corticopontine projections in the postnatal rat. In: Developing and regenerating vertebrate nervous systems. Liss, New York, pp 211–222

    Google Scholar 

  • Bastiani M, Pearson KG, Goodman CS (1984) From embryonic fascicles to adult tracts: organization of neuropile from a developmental perspective. J Exp Biol 112:45–64

    Google Scholar 

  • Bates CA, Killackey HP (1984) The emergence of a discretely distributed pattern of corticospinal projection neurons. Dev Brain Res 13:265–273

    Google Scholar 

  • Bernstein DR, Stelzner DJ (1983) Plasticity of the corticospinal tract following midthoracic spinal injury in the postnatal rat. J Comp Neurol 221:382–400

    Google Scholar 

  • Cabana T, Martin GF (1985) Corticospinal development in the North American opossum: evidence for a sequence in the growth of cortical axons in the spinal cord and for transient projections. Dev Brain Res 23:69–80

    Google Scholar 

  • Cancalon P (1985) Influence of temperature on various mechanisms associated with neuronal growth and nerve regeneration. Prog Neurobiol 25:27–92

    Google Scholar 

  • Carney PR, Silver J (1983) Studies on cell migration and axon guidance in the developing distal auditory system of the mouse. J Comp Neurol 215:359–369

    Google Scholar 

  • D'Amato CJ, Hicks SP (1980) Development of the motor system: effects of radiation on developing corticospinal neurons and locomotor function. Exp Neurol 70:1–23

    Google Scholar 

  • De Kort EJM, van Aanholt HTH (1983) On the development of the pyramidal tract in the rat. Neurosci Lett [Suppl] 14:85

    Google Scholar 

  • De Kort EJM, van Aanholt HTH (1984) On the development of the pyramidal tract in the rat. Acta Morphol Neerl-Scand 22:182

    Google Scholar 

  • De Kort EJM, Gribnau AAM, van Aanholt HTH, Nieuwenhuys R (1985) On the development of the pyramidal tract in the rat. I. The morphology of the growth zone. Anat Embryol 172:195–204

    Google Scholar 

  • De Myer W (1967) Ontogenesis of the rat corticospinal tract. Normal events and effects of intra-uterine neurosurgical lesions. Arch Neurol 16:203–211

    Google Scholar 

  • Donatelle JM (1977) Growth of the corticospinal tract and the development of placing reactions in the postnatal rat. J Comp Neurol 175:207–232

    Google Scholar 

  • Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88

    Google Scholar 

  • Gribnau AAM, Dederen PJWC (1984) On the development of the pyramidal tract in the rat: an anterograde WGA-HRP study. Neurosci Lett [Suppl] 18:175

    Google Scholar 

  • Hicks SP, d'Amato CJ (1975) Motor-sensory cortex-cortico-spinal system and developing locomotion and placing in rats. Am J Anat 143:1–42

    Google Scholar 

  • Hicks SP, d'Amato CJ (1980) Development of the motor system: hopping rats produced by prenatal irradiation. Exp Neurol 70:24–39

    Google Scholar 

  • Humphrey T (1960) The developmental of the pyramidal tracts in human fetuses correlated with cortical diffeentiation. In: Tower, Schadé (eds) Structure and function of the cerebral cortex. Proceedings of the Second International Meeting of Neurobiologists. Elsevier, Amsterdam London New York, pp 93–103

    Google Scholar 

  • Ivy GO, Killackey HP (1982) Ontogenetic changes in the projections of neocortical neurons. J Neurosci 2:735–743

    Google Scholar 

  • Jones EG, Schreyer DJ, Wise SP (1982) Growth and maturation of the rat corticospinal tract. Prog Brain Res 57:361–379

    Google Scholar 

  • Kalil K (1984) Developmental and regrowth of the rodent pyramidal tract. TINS 7:394–398

    Google Scholar 

  • Kalil K, Norris C (1985) Rearrangement of axon fascicles in the decussation of the pyramidal tract. Soc Neurosci 11:584 (abstr)

    Google Scholar 

  • Kalil K, Reh T (1979a) Redirection of pyramidal tract axons in neonatal hamsters: some mechanisms of axonal guidance during development. Soc Neurosci 5:629

    Google Scholar 

  • Kalil K, Reh T (1979b) Regrowth of severed axons in the neonatal central nervous system: establishment of normal connections. Science 205:1158–1161

    Google Scholar 

  • Kalil K, Reh T (1982) A light and electron microscopic study of regrowing pyramidal tract fibers. J Comp Neurol 211:265–275

    Google Scholar 

  • Katz MJ (1984) Sterotyped and variable growth of redirected Mauthner axons. Dev Biol 104:199–209

    Google Scholar 

  • Katz MJ (1985) How straight do axons grow? J Neurosci 5:589–595

    Google Scholar 

  • Katz MJ, Lasek RJ (1979) Substrate pathways which guide growing axons in Xenopus embryos. J Comp Neurol 183:817–832

    Google Scholar 

  • Katz MJ, Lasek RJ (1981) Substrate pathways demonstrated by transplanted Mauthner axons. J Comp Neurol 195:627–642

    Google Scholar 

  • Katz MJ, Lasek RJ, Nauta HJW (1980) Ontogeny of substrate pathways and the origin of the neural circuit pattern. Neuroscience 5:821–833

    Google Scholar 

  • Killackey HP (1984) Glia and the elimination of transient cortical projections. TINS 7:225–226

    Google Scholar 

  • Krayanek S, Goldberg S (1981) Oriented extracellular channels and axonal guidance in the embryonic chick retina. Dev Biol 84:41–50

    Google Scholar 

  • Lasek RJ (1980) Axonal transport: a dynamic view of neuronal structures. TINS 3:87–91

    Google Scholar 

  • Leong SK (1983) Localizing the corticospinal neurons in neonatal, developing and mature albino rat. Brain Res 265:1–9

    Google Scholar 

  • Leong SK, Shieh JY, Wong WC (1984a) Localizing spinal-cordprojecting neurons in adult albino rats. J Comp Neurol 228:1–17

    Google Scholar 

  • Leong SK, Shieh JY, Wong WC (1984b) Localizing spinal-cordprojecting neurons in neonatal and immature albino rats. J Comp Neurol 228:18–23

    Google Scholar 

  • Martin GF, Cabana T, Culberson JL, Curry JJ, Tschismada J (1980) The early development of corticobulbar and corticospinal systems. Studies using the North American Opossum. Anat Embryol 161:197–213

    Google Scholar 

  • Mesulam MM (1978) Tetramethylbenzidine for horseradish peroxidase neurohistochemistry. A non-carcinogenic blue reactionproduct with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    Google Scholar 

  • Mesulam MM, Mufson EJ (1980) The rapid anterograde transport of horseradish peroxidase. Neuroscience 5:1277–1286

    Google Scholar 

  • Nordlander RH, Singer M (1978) The role of ependyma in regeneration of the spinal cord of the urodele amphibian tail. J Comp Neurol 180:349–374

    Google Scholar 

  • Nordlander RH, Singer M (1982a) Spaces preceed axons in Xenopus embryonic spinal cord. Exp Neurol 75:221–228

    Google Scholar 

  • Nordlander RH, Singer M (1982b) Morphology and position of growth cones in the developing Xenopus spinal cord. Dev Brain Res 4:181–193

    Google Scholar 

  • O'Leary DDM, Stanfield BB (1985) Occipital cortical neurons with transient pyramidal tract axons extend and maintain collaterals to subcortical but not intracortical targets. Brain Res 336:326–333

    Google Scholar 

  • O'Leary DDM, Stanfield BB (1986) A transient pyramidal tract projection from the visual cortex in the hamster and its removal by selective collateral elimination. Dev Brain Res 27:87–99

    Google Scholar 

  • Papasozomenos SC, Autilio-Gambetti L, Gambetti P (1983) Distribution of proteins migrating with fast axonal transport. Their relationship to smooth endoplasmic reticulum. Brain Res 278:232–235

    Google Scholar 

  • Rager G, Lausmann S, Gallyas F (1979) An improved silver stain for developing nervous tissue. Stain Technol 54:193–200

    Google Scholar 

  • Reh T, Kalil K (1981) Development of the pyramidal tract in the hamster. I. A light microscopic study. J Comp Neurol 200:55–67

    Google Scholar 

  • Reh T, Kalil K (1982a) Development of the pyramidal tract in the hamster. II. An electron microscopic study. J Comp Neurol 205:77–88

    Google Scholar 

  • Reh T, Kalil K (1982b) Functional role of regrowing pyramidal tract fibers. J Comp Neurol 211:276–283

    Google Scholar 

  • Rutishauser U (1985) Influences of the neural cell adhesion molecule on axon growth and guidance. J Neurosci Res 13:123–131

    Google Scholar 

  • Schnapp BJ, Reese TS (1986) New developments in understanding rapid axonal transport. TINS 9:155–162

    Google Scholar 

  • Schreyer DJ, Jones EG (1982) Growth and target finding by axons of the corticospinal tract in prenatal and postnatal rats. Neuroscience 7:1837–1853

    Google Scholar 

  • Schreyer DJ, Jones EG (1983) Growing corticospinal axons by-pass lesions of neonatal rat spinal cord. Neuroscience 9:31–40

    Google Scholar 

  • Schreyer DJ, Jones EG (1985) Developmental pattern of the cells of origin of the corticospinal tract of the rat. Soc Neurosci 11:988 (abstr)

    Google Scholar 

  • Shook BC, Abramson BP, Chalupa LM (1984) An analysis of the transport of WGA-HRP in the cat's visual system. J Neurosci Methods 11:65–77

    Google Scholar 

  • Silver J (1984) Studies on the factors that govern directionality of axonal growth in the embryonic optic nerve and at the chiasm of mice. J Comp Neurol 223:238–251

    Google Scholar 

  • Silver J, Robb RM (1979) Studies on the development of the eye cup and optic nerve in normal mice and in mutants with congenital optic nerve aplasia. Dev Biol 68:175–190

    Google Scholar 

  • Silver J, Rutishauser U (1984) Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithetial endfeet. Dev Biol 106:485–499

    Google Scholar 

  • Silver J, Sapiro J (1981) Axonal guidance during development of the optic nerve: the role of pigmented epithelia and other extrinsic factors. J Comp Neurol 202:521–538

    Google Scholar 

  • Silver J, Sidman RL (1980) A mechanism for the guidance and topographic patterning of retinal ganglion cell axons. J Comp Neurol 189:101–111

    Google Scholar 

  • Silver JE, Lorenz SE, Wahlstein D, Coughlin J (1982) Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies in vivo, on the role of preformed glial pathways. J Comp Neurol 210:10–29

    Google Scholar 

  • Singer M, Nordlander RM, Egar M (1979) Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blueprint hypothesis of neuronal pathway patterning. J Comp Neurol 185:1–22

    Google Scholar 

  • Stanfield BB (1984) Postnatal reorganization of cortical projections: the role of collateral climination. TINS 7:37–40

    Google Scholar 

  • Stanfield BB, O'Leary DDM (1985a) Fetal occipital cortical neurones transplanted to the rostral cortex can extend and maintain a pyramidal tract axon. Nature 313:135–137

    Google Scholar 

  • Stanfield BB, O'Leary DDM (1985b) The transient corticospinal projection from the occipital cortex during the postnatal development of the rat. J Comp Neurol 238:236–248

    Google Scholar 

  • Stanfield BB, O'Leary DDM, Fricks C (1982) Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298:371–373

    Google Scholar 

  • Terashima T, Inoue K, Inoue Y, Mikoshiba K, Tsukada Y (1983) Distribution and morphology of corticospinal tract neurons in Reller mouse cortex by the retrograde HRP method. J Comp Neurol 218:314–326

    Google Scholar 

  • Valentino KL, Jones EG (1982) The early formation of the corpus callosum: a light and electron microscopic study in fetal and neonatal rats. J Neurocytol 11:583–609

    Google Scholar 

  • Wise SP, Murray EA, Coulter JD (1979a) Somatotopic organization of corticospinal and corticotrigeminal neurons in the rat. Neuroscience 4:65–78

    Google Scholar 

  • Wise SP, Fleshman JW, Jones EG (1979b) Maturation of pyramidal cell form in relation to developing afferent and efferent connections of rat somatic sensory cortex. Neuroscience 4:1275–1297

    Google Scholar 

  • Wozniak W, O'Rahilly R (1982) An electronmicroscopic study of myelination of pyramidal fibers at the level of the pyramidal decussation in the human fetus. J Hirnforsch 23:331–342

    Google Scholar 

  • Wujek JR, Lasek RJ, Gambetti P (1986) The amount of slow axonal transport is proportional to the radial dimensions of the axon. J Neurocytol 15:75–83

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Embryology, Faculty of Medicine, University of Nijmegen, Nijmegen, The Netherlands

    A. A. M. Gribnau, E. J. M. de Kort, P. J. W. C. Dederen & R. Nieuwenhuys

Authors
  1. A. A. M. Gribnau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. J. M. de Kort
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. J. W. C. Dederen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Nieuwenhuys
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gribnau, A.A.M., de Kort, E.J.M., Dederen, P.J.W.C. et al. On the development of the pyramidal tract in the rat. Anat Embryol 175, 101–110 (1986). https://doi.org/10.1007/BF00315460

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00315460

Key words

Search

Navigation