Journal of Neuroscience, Vol 9, 1806-1824, Copyright © 1989 by Society for Neuroscience
Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons
EM Callaway, JM Soha and DC Van Essen
Division of Biology, California Institute of Technology, Pasadena 91125.
We have tested whether the ability of synapses to compete for occupancy of
endplates during neuromuscular synapse elimination is affected by
differences in the spinal position or in the activity level of the parent
motor neuron. To test the role of spinal position, the relative sizes of
motor units for motor neurons from middle and extreme (rostral/caudal)
positions in the rabbit soleus motor pool were determined at 3 postnatal
ages: 4-5 d ("early" ages, when the soleus is heavily polyinnervated), 8-9
d ("intermediate"), and 11-15 d ("late," when the soleus has just reached
singly innervated state). Average motor unit sizes from extreme ventral
roots were similar to those from middle ventral roots in early-aged soleus
muscles but were significantly smaller (by 18-27%) for both intermediate
and late muscles. Thus, motor neurons from extreme positions evidently
compete less effectively for retention of synapses than those from middle
positions. To test the role of differential activity, inactive and active
synapses were pitted directly against one another by implanting Silastic
plugs laden with tetrodotoxin (TTX) into one of the spinal nerves
containing a minority of the soleus motor axons. Differential activity was
maintained during a period of extensive synapse loss, from the time of the
implant at day 4 or 5 until the intermediate age (day 8- 9). Motor unit
twitch tensions were subsequently measured to determine the relative number
of synapses retained by individual active and inactive motor neurons. The
inactivated motor units were on average significantly larger (by more than
50%) than the corresponding group from normal and control-implanted
animals. The abnormally large size of inactivated motor units persisted in
animals allowed to recover from the TTX block and examined after multiple
innervation had disappeared. Hence, the effect of the TTX block cannot be
attributed to a simple slowing of synapse elimination specifically among
the inactive motor neurons. We conclude that complete presynaptic
inactivity improves the chances of survival relative to that for normal
activity during synapse elimination in the neonatal rabbit soleus muscle.
This difference in competitive ability may contribute to the development of
an important characteristic of adult muscles, the correlation between motor
unit size and recruitment threshold.