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The segmental precision of the motor projection to the intercostal muscles in the developing chicken embryo

A differential labelling study using fluorescent tracers

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Abstract

Each skeletal muscle in the vertebrate is innervated by a group of motoneurons called a motoneuron pool. Retrograde labelling of single motoneuron pools has suggested that the arrangement of motoneuron pools innervating different limb muscles does not change during the embryonic period when more than 50% of the motoneurons die. In this study we retrogradely labelled neighbouring intercostal motoneuron pools differentially with latex microspheres or dextran amines coupled to fluorescent dyes. We then mapped the positions of the differentially labelled motoneurons in whole-mount preparations using a computer-aided drawing system. While the intercostal motoneuron pools are clearly segregated even at early stages, there is some intermingling at the rostral and caudal ends. We used a logistic regression to determine the extent of segmental overlap, and to facilitate a quantitative comparison of the overlap at different stages. Statistical analysis shows that the overlap (expressed as the percentage of the length of the overlapping motoneuron pools) decreases modestly during the period of motoneuron death. Computer simulations suggest that this decrease does not result from random motoneuron death alone; one alternative possibility is selective death of motoneurons in the overlap zone. Occasional “rogue” motoneurons, that is, motoneurons of one pool that scatter into the neighbouring pool, are still present at the end of the period of cell death, representing a potential source of “noise” in the establishment of segmental patterns of connectivity.

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References

  • Eide AL, Glover JC (1995) The development of the longitudinal projection patterns of lumbar primary sensory afferents in the chicken embryo. J Comp Neurol (in press)

  • Euler C von (1983) On the origin and pattern control of breathing rhythmicity in mammals. Symp Soc Exp Biol 37:469–485

    Google Scholar 

  • Farel PB, Bemelmans SE (1980) Retrograde labelling of migrating spinal motoneurons in bullfrog larvae. Neurosci Lett 18:133–136

    Google Scholar 

  • Forehand CJ, Ezerman EB, Rubin E, Glover JC (1994) Segmental patterning of rat and chicken sympathetic preganglionic neurons: correlation between soma position and axon projection pathway. J Neurosci 14:231–241

    Google Scholar 

  • Frank E, Westerfield M (1983) Development of sensory-motor synapses in the spinal cord of the frog. J Physiol (Lond) 343:593–610

    Google Scholar 

  • Gimlich RL, Braun J (1985) Improved fluorescent compounds for tracing cell lineage. Dev Biol 109:509–514

    Google Scholar 

  • Glover JC (1995) Retrograde and anterograde axonal tracing with fluorescent dextran-amines in the embryonic nervous system. Neurosci Protocols (in press)

  • Glover JC, Petursdottir G, Jansen JKS (1986) Fluorescent dextranamines used as axonal tracers in the nervous system of the chicken embryo. J Neurosci Methods 18:243–254

    Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    Google Scholar 

  • Hamburger V, Oppenheim RW (1982) Naturally occurring neuronal death in vertebrates. Neurosci Comment 1:39–55

    Google Scholar 

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

    Google Scholar 

  • Hollyday M (1983) Development of motor innervation of chick limbs. In: Fallon J, Caplan A (eds) Limb development and regeneration, part A. Liss, New York, pp 183–193

    Google Scholar 

  • Honig MG, Hume RI (1986) Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J Cell Biol 103:171–187

    Google Scholar 

  • Hosner DW, Lemeshow S (1989) Applied logistic regression. Wiley, New York

    Google Scholar 

  • Illert M, Fritz N, Aschoff A, Hollander H (1982) Fluorescent compounds as retrograde tracers compared with horseradish peroxidase (HRP). II. A parametric study in the peripheral motor system of the cat. J Neurosci Methods 6:199–218

    Google Scholar 

  • Katz LC, Burkhalter A, Dreyer WD (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498–500

    Google Scholar 

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

    Google Scholar 

  • Laing NG (1982) Timing of motoneuron death in the brachial and lumbar regions of the chick embryo. Dev Brain Res 5:181–186

    Google Scholar 

  • Landmesser L (1978a) The distribution of motoneurons supplying chick hind limb muscles. J Physiol (Lond) 284:371–389

    Google Scholar 

  • Landmesser L (1978b) The development of motor projection patterns in the chick hind limb. J Physiol (Lond) 284:391–414

    Google Scholar 

  • Laskowski MB, Sanes JR (1987) Topographic mapping of motor pools onto skeletal muscles. J Neurosci 7:252–260

    Google Scholar 

  • Mendelson B, Frank E (1991) Specific monosynaptic sensory-motor connections form in the absence of patterned neural activity and motoneuronal cell death. J Neurosci 11:1390–1403

    Google Scholar 

  • O'Brien MK, Oppenheim RW (1990) Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: anatomical aspects. J Neurobiol 21:313–340

    Google Scholar 

  • Oppenheim RW (1981) Neuronal death and some related regressive phenomena during neurogenesis: a selective historical review and progress report. In: Cowan WM (ed) Studies in developmental neurobiology: essays in honor of Victor Hamburger. Oxford University Press, New York, pp 74–133

    Google Scholar 

  • Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453–501

    Google Scholar 

  • Smith CL, Hollyday M (1983) The development and postnatal organization of motor nuclei in the rat thoracic spinal cord. J Comp Neurol 220:16–28

    Google Scholar 

  • Stern CD, Sisodya SM, Keynes RJ (1986) Interactions between neurites and somite cells: inhibition and stimulation of nerve growth in the chick embryo. I Embryol Exp Morphol 91:209–226

    Google Scholar 

  • Stirling RV, Summerbell D (1991) Developmental changes in the arrangement of motor pools in the chick spinal cord mapped using fluorescent beads. Soc Neurosci Abstr 17:1124

    Google Scholar 

  • Stirling RV, Summerbell D (1992) Developmental changes in the motor pools to intercostal muscles in the chick spinal cord mapped using fluorescent beads. Neurosci Lett [Suppl] 42:S19

    Google Scholar 

  • Summerbell D, Stirling RV (1981) The innervation of dorsoventrally reversed chick wings: evidence that motor axons do not actively seek out their appropriate targets. J Embryol Exp Morphol 61:233–247

    Google Scholar 

  • Summerbell D, Stirling RV (1982) Development of the pattern of innervation of the chick limb. Am Zool 22:173–184

    Google Scholar 

  • Tsering C (1992) Demonstration of segmental arrangement of thoracic spinal motor neurons using lipophilic dyes. Dev Neurosci 14:308

    Google Scholar 

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Stirling, R.V., Liestøl, K., Summerbell, D. et al. The segmental precision of the motor projection to the intercostal muscles in the developing chicken embryo. Anat Embryol 191, 397–406 (1995). https://doi.org/10.1007/BF00304425

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  • DOI: https://doi.org/10.1007/BF00304425

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