Journal of Neuroscience, Vol 6, 2889-2899, Copyright © 1986 by Society for Neuroscience
Cell death of lumbosacral motoneurons in chick, quail, and chick-quail chimera embryos: a test of the quantitative matching hypothesis of neuronal cell death
H Tanaka and LT Landmesser
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.
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