Cell death of lumbosacral motoneurons in chick, quail, and chick-quail chimera embryos: a test of the quantitative matching hypothesis of neuronal cell death

Abstract

The quantitative matching hypothesis of neuronal cell death was tested for the chick hindlimb by determining the relationship between myotube number at the onset of motoneuron cell death and the number of motoneurons that survive in chicks, quail, and chick-quail chimeras. Hindlimb buds, which differ in size between the 2 species, were exchanged at stages 16 1/2-19, myosin ATPase-stained myotubes in selected thigh muscles were counted during the cell death period (stages 30-34), and lumbosacral motoneurons were counted following the cell death period (stage 38). No quail motoneurons were rescued when quail cords innervated chick limbs. When chick cords innervated quail limbs, the number of surviving motoneurons was significantly decreased but not to quail values. We consider that this occurred because chicks develop more slowly than quail, and we found that transplanted chick limbs were developmentally younger than the contralateral quail limb at the onset of motoneuron cell death and contained fewer myotubes. Similarly, transplanted quail limbs contained more myotubes at the onset of cell death than normal stage 30 quail limbs. An excellent correlation was obtained during normal development of both species between the number of myotube clusters at the onset of cell death and the number of surviving motoneurons. This correlation was also observed for chick-quail chimeras, and when the data points were plotted for control chick, control quail, chick host-quail limb, and quail host-chick limb, the correlation coefficient was 0.996. This strongly suggests that some parameter closely related to myotube number limits the number of motoneurons that will survive. A proposal consistent with our observations is that motoneuron survival is dependent on the uptake of a myotube-derived trophic factor that can only be taken up at synaptic sites and that the number of such sites is limited and directly related to myotube number. In conclusion, our observations strongly support a quantitative-matching component in the process of neuronal cell death. However, since we were unable to rescue any neurons, we cannot exclude the possibility that some proportion of neurons normally dies for reasons other than peripheral competition.

Neurovascular Anatomy of the Embryonic Quail Hindlimb

“…The posterior cardinal vein is formed at the level of the hindlimb by E3, as is the main artery of the early hindlimb, the ischiadic artery, as an offshoot of the dorsal aorta. Our data suggest that eight spinal segments, versus seven as reported by others (Tanaka and Landmesser, 1986a;Tyrrell et al, 1990), contribute to innervation of the quail hindlimb. Lumbosacral neurites reach the plexus region by E3.5 (HH21 & 22), pause for $24 hr, and then enter the hindlimb along with the ischiadic and crural arteries through shared foramina in the pelvic anlage.…”

“…The present study found that eight spinal segments, as opposed to seven as reported by Tanaka and Landmesser (1986a) and Tyrrell et al (1990), contribute to the innervation of the quail hindlimb. During E4.0 (HH24) LS spinal nerves 1-8 continue to extend axons in distinct bundles towards the plexus region at the base of the hindlimb (Fig.…”

Motoneurons Derived from Embryonic Stem Cells Express Transcription Factors and Develop Phenotypes Characteristic of Medial Motor Column Neurons

“…The temporal pattern of eGFP ϩ cell death was remarkably similar to the normal time course in naturally occurring cell death (Hamburger, 1975;Tanaka and Landmesser, 1986). However, the extent of cell death was greater than the usual 50% loss in motoneurons.…”

Stereological Estimate of the Total Number of Neurons in Spinal Segment D9 of the Red-Eared Turtle

“…Assuming a similar number of segmental motoneurons in segments S1 and S2, we estimate the total number of hindlimb motoneurons in the lumbar enlargement of the turtle to be at least 10,000. This is much lower than the estimated 60,000 lumbar motoneurons in humans (Tomlinson and Irving, 1977), but surprisingly similar to the number of hindlimb motoneurons in chicks (Hamburger, 1975;Laing, 1982;Tanaka and Landmesser, 1986). In contrast, the number of lumbar motoneurons is Ͻ2000 in adult bull frogs (Farel et al, 1992) and only 3500 in rodents (Oppenheim, 1986).…”