Abstract
1. The development of motoneurone projection patterns in the chick hind limb from reversed spinal cord segments was studied from the onset of axonal outgrowth (St. 24) to the establishment of mature connectivity patterns (St. 36). Approximately the first three lumbosacral cord segments were reversed along the anterior-posterior axis at St. 15-16. 2. Projection patterns from reversed cord segments were assessed electrophysiologically by direct spinal cord and spinal nerve stimulation and anatomically by retrograde horseradish peroxidase (HRP) labelling of motoneurones in St. 30-36 embryos. In younger embryos, paths taken by reversed axons were characterized by orthograde HRP labelling of motoneurones in specific reversed cord segments. 3. Lumbosacral motoneurones formed appropriate functional connexions with individual limb muscles in spite of anterior-posterior shifts in their spinal cord position aned consequent shifts in their spinal nerve entry point into the limb bud. Reversed motoneurones supplying individual hind limb muscles formed discrete nuclei in the transverse plane of the cord. Each nucleus and the lateral motor column as a whole showed reversed topographical characteristics when compared to control embryos. These observations were made before (St. 30) and after (St. 35-36) the major period of motoneurone cell death. 4. Correct connectivity resulted from specific alterations in axonal pathways within the plexus or major nerve trunks proximal to the branching of individual muscle nerves. Further such directed outgrowth was present from the earliest times that axons could be traced into the limb which is before the onset of motoneurone cell death and muscle cleavage. 5. It is concluded that motoneurones are specified to project to individual muscles or to follow particular pathways prior to motoneurone birthdays and limb bud formation. The establishment of specific motoneurone connectivity can not be accounted for by passive or mechanical guidance models alone. Rather, motoneurones must also actively respond to cues within the limb or interact among themselves on the basis of an early central specification.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson H. Postembryonic development of the visual system of the locust, Schistocerca gregaria. II. An experimental investigation of the formation of the retina-lamina projection. J Embryol Exp Morphol. 1978 Aug;46:147–170. [PubMed] [Google Scholar]
- Chung S. H., Cooke J. Observations on the formation of the brain and of nerve connections following embryonic manipulation of the amphibian neural tube. Proc R Soc Lond B Biol Sci. 1978 Jun 5;201(1145):335–373. doi: 10.1098/rspb.1978.0050. [DOI] [PubMed] [Google Scholar]
- Cook J. E., Horder T. J. The multiple factors determining retinotopic order in the growth of optic fibres into the optic tectum. Philos Trans R Soc Lond B Biol Sci. 1977 Apr 26;278(961):261–276. doi: 10.1098/rstb.1977.0041. [DOI] [PubMed] [Google Scholar]
- Cruce W. L. The anatomical organization of hindlimb motoneurons in the lumbar spinal cord of the frog, Rana catesbiana. J Comp Neurol. 1974 Jan 1;153(1):59–76. doi: 10.1002/cne.901530106. [DOI] [PubMed] [Google Scholar]
- Ebendal T. Extracellular matrix fibrils and cell contacts in the chick embryo. Possible roles in orientation of cell migration and axon extension. Cell Tissue Res. 1977 Jan 4;175(4):439–458. doi: 10.1007/BF00222411. [DOI] [PubMed] [Google Scholar]
- HAMBURGER V. Regression versus peripheral control of differentiation in motor hypoplasia. Am J Anat. 1958 May;102(3):365–409. doi: 10.1002/aja.1001020303. [DOI] [PubMed] [Google Scholar]
- Hamburger V. Cell death in the development of the lateral motor column of the chick embryo. J Comp Neurol. 1975 Apr 15;160(4):535–546. doi: 10.1002/cne.901600408. [DOI] [PubMed] [Google Scholar]
- Hibbard E. Orientation and directed growth of Mauthners cell axons form duplicated vestibular nerve roots. Exp Neurol. 1965 Nov;13(3):289–301. doi: 10.1016/0014-4886(65)90117-2. [DOI] [PubMed] [Google Scholar]
- Hollyday M., Hamburger V. An autoradiographic study of the formation of the lateral motor column in the chick embryo. Brain Res. 1977 Aug 26;132(2):197–208. doi: 10.1016/0006-8993(77)90416-4. [DOI] [PubMed] [Google Scholar]
- Hollyday M., Hamburger V., Farris J. M. Localization of motor neuron pools supplying identified muscles in normal and supernumerary legs of chick embryo. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3582–3586. doi: 10.1073/pnas.74.8.3582. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hope R. A., Hammond B. J., Gaze R. M. The arrow model: retinotectal specificity and map formation in the goldfish visual system. Proc R Soc Lond B Biol Sci. 1976 Nov 12;194(1117):447–466. doi: 10.1098/rspb.1976.0088. [DOI] [PubMed] [Google Scholar]
- Lamb A. H. Neuronal death in the development of the somatotopic projections of the ventral horn in Xenopus. Brain Res. 1977 Sep 23;134(1):145–150. doi: 10.1016/0006-8993(77)90932-5. [DOI] [PubMed] [Google Scholar]
- Lamb A. H. The projection patterns of the ventral horn to the hind limb during development. Dev Biol. 1976 Nov;54(1):82–99. doi: 10.1016/0012-1606(76)90288-8. [DOI] [PubMed] [Google Scholar]
- Lance-Jones C., Landmesser L. Motoneurone projection patterns in embryonic chick limbs following partial deletions of the spinal cord. J Physiol. 1980 May;302:559–580. doi: 10.1113/jphysiol.1980.sp013261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lance-Jones C., Landmesser L. Motoneurone projection patterns in embryonic chick limbs following partial deletions of the spinal cord. J Physiol. 1980 May;302:559–580. doi: 10.1113/jphysiol.1980.sp013261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Landmesser L., Morris D. G. The development of functional innervation in the hind limb of the chick embryo. J Physiol. 1975 Jul;249(2):301–326. doi: 10.1113/jphysiol.1975.sp011017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Landmesser L. The development of motor projection patterns in the chick hind limb. J Physiol. 1978 Nov;284:391–414. doi: 10.1113/jphysiol.1978.sp012546. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Landmesser L. The distribution of motoneurones supplying chick hind limb muscles. J Physiol. 1978 Nov;284:371–389. doi: 10.1113/jphysiol.1978.sp012545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Letourneau P. C. Cell-to-substratum adhesion and guidance of axonal elongation. Dev Biol. 1975 May;44(1):92–101. doi: 10.1016/0012-1606(75)90379-6. [DOI] [PubMed] [Google Scholar]
- Letourneau P. C. Chemotactic response of nerve fiber elongation to nerve growth factor. Dev Biol. 1978 Sep;66(1):183–196. doi: 10.1016/0012-1606(78)90283-x. [DOI] [PubMed] [Google Scholar]
- Macagno E. R. Mechanism for the formation of synaptic projections in the arthropod visual system. Nature. 1978 Sep 28;275(5678):318–320. doi: 10.1038/275318a0. [DOI] [PubMed] [Google Scholar]
- McGrath P. A., Bennett M. R. Development of synaptic connections between different segmental motoneurones striated muscles in an axolotl limb. Dev Biol. 1979 Mar;69(1):133–145. doi: 10.1016/0012-1606(79)90280-x. [DOI] [PubMed] [Google Scholar]
- Morris D. G. Development of functional motor innervation in supernumerary hindlimbs of the chick embryo. J Neurophysiol. 1978 Nov;41(6):1450–1465. doi: 10.1152/jn.1978.41.6.1450. [DOI] [PubMed] [Google Scholar]
- NARAYANAN C. H. AN EXPERIMENTAL ANALYSIS OF PERIPHERAL NERVE PATTERN DEVELOPMENT IN THE CHICK. J Exp Zool. 1964 Jun;156:49–60. doi: 10.1002/jez.1401560105. [DOI] [PubMed] [Google Scholar]
- Pettigrew A. G., Lindeman R., Bennett M. R. Development of the segmental innervation of the chick forelimb. J Embryol Exp Morphol. 1979 Jan;49:115–137. [PubMed] [Google Scholar]
- ROMANES G. J. THE MOTOR POOLS OF THE SPINAL CORD. Prog Brain Res. 1964;11:93–119. doi: 10.1016/s0079-6123(08)64045-5. [DOI] [PubMed] [Google Scholar]
- SPERRY R. W. CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. Proc Natl Acad Sci U S A. 1963 Oct;50:703–710. doi: 10.1073/pnas.50.4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]
- SZEKELY G. Functional specificity of spinal cord segments in the control of limb movements. J Embryol Exp Morphol. 1963 Jun;11:431–444. [PubMed] [Google Scholar]
- Stirling R. V., Summerbell D. The development of functional innervation in the chick wing-bud following truncations and deletions of the proximal-distal axis. J Embryol Exp Morphol. 1977 Oct;41:189–207. [PubMed] [Google Scholar]
- Stirling R. V., Summerbell D. The segmentation of axons from the segmental nerve roots to the chick wing. Nature. 1979 Apr 12;278(5705):640–642. doi: 10.1038/278640a0. [DOI] [PubMed] [Google Scholar]
- Straznicky K. The development of the innervation and the musculature of wings innervated by thoracic nerves. Acta Biol Acad Sci Hung. 1967;18(4):437–448. [PubMed] [Google Scholar]
- Ueyama T. The topography of root fibres within the sciatic nerve trunk of the dog. J Anat. 1978 Oct;127(Pt 2):277–290. [PMC free article] [PubMed] [Google Scholar]
- von der Malsburg C., Willshaw D. J. How to label nerve cells so that they can interconnect in an ordered fashion. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5176–5178. doi: 10.1073/pnas.74.11.5176. [DOI] [PMC free article] [PubMed] [Google Scholar]