Composition of newly forming motor units in prenatal rat intercostal muscle.
We have examined the composition of rat intercostal motor units during the period of late gestation, when most muscle fibres are formed, in order to see the pattern of the contacts initially made between single motoneurons and myotubes. At this early stage, the muscle contains two types of myotubes, primary and secondary myotubes, and a major aim was to see whether individual motoneurons preferentially made contact with a particular myotube type. The technique used to define myotubes contacted by a single motoneuron was anterograde labelling of the neuron, followed by electron microscopic detection of labelled terminals and their postsynaptic targets. We find that prenatal motor units are inhomogeneous with respect to their primary/secondary myotube composition. Most individual motoneurons show many permutations of contact with primary myotubes, secondary myotubes, and undifferentiated cells, including single nerve terminals which contact both primary and secondary myotubes. Our results are interpreted in terms of changes to the composition of both the muscle and of the motor units during the final 5 days of gestation. We demonstrate that motoneurons necessarily make their initial contacts on primary myotubes, but that these are surprisingly sparse. As secondary myotubes appear and become innervated, motor units are at first all similar and all heterogeneous. However, primary myotubes are represented more often in motor units than in the muscle as a whole. This probably reflects the relative densities of polyinnervation of primary vs. secondary myotubes. By embryonic day 20, motor units have become divergent in composition, with some dominated by primary myotubes and others by secondaries. We propose that motoneurons initially establish contacts at random on either myotube type, but then begin to express preference for one type or the other and reorganise their periphery. Refining of motor unit composition towards homogeneity in the postnatal period probably involves other elements, such as mutability of muscle fibre and/or motoneuron characteristics as a function of usage and muscle position, perhaps influenced by sensory feedback mechanisms.
Sheard
P W
PW
Department of Physiology, University of Otago Medical School, Dunedin, New Zealand.
Duxson
M J
MJ
D000345:Affinity Labels; D000818:Animals; D007366:Intercostal Muscles / Q000166:cytology* / Q000196:embryology / Q000648:ultrastructure; D008239:Lysine / Q000031:analogs & derivatives; D008854:Microscopy, Electron; D009045:Motor Endplate / Q000166:cytology / Q000648:ultrastructure; D009046:Motor Neurons / Q000145:classification / Q000166:cytology* / Q000648:ultrastructure; D018485:Muscle Fibers, Skeletal / Q000145:classification / Q000166:cytology / Q000648:ultrastructure; D051381:Rats
D000345:Affinity Labels; C013411:biocytin; D008239:Lysine