Fibre type composition of single motor units during synapse elimination in neonatal rat soleus muscle

Abstract

Skeletal motor neurones innervate the specialized 'types' of fibres comprising most mammalian muscles in a characteristic fashion: each motor neurone forms a 'motor unit' by innervating a set of fibres all of the same type. Because the type expression of adult muscle fibres is plastic and apparently controlled by their innervation, each motor neurone is thought to impose a common type differentiation on all the fibres in its motor unit. However, the situation in developing muscles cannot be this simple. Muscle fibres in neonates receive synaptic input from several motor neurones and achieve the adult, single innervation only after a period of 'synapse elimination. Despite this polyneuronal innervation, differentiated fibre types are present in neonatal muscles. This means either that the motor neurones polyneuronally innervate fibres in a random fashion and type expression is not determined by innervation or that the polyneuronal innervation is ordered in such a way that each fibre could receive unambiguous instructions for type differentiation. We have investigated these possibilities here by determining the fibre type composition of motor units in neonatal rat soleus muscle. We find that even during the time of polyneuronal innervation each motor neurone confines its innervation to largely one of two fibre types present in the muscle. Therefore, some mechanism during early development segregates the synapses of two groups of soleus motor neurones onto two separate populations of soleus muscle fibres.

Selective Fasciculation and Divergent Pathfinding Decisions of Embryonic Chick Motor Axons Projecting to Fast and Slow Muscle Regions

“…We also found that the position of motoneuron somas in the spinal cord was not clearly correlated with fast and slow specificity or subsequent axon fasciculation. These results are consistent with previous reports of selective innervation both in the chick, showing that embryonic motoneurons selectively innervate foreign muscles containing the muscle fiber type characteristic of their normal target (Rafuse et al, 1996; for adult chick, see also Feng et al, 1965;Hnik et al, 1967), and in the mammal, documenting that neonatal motor units are composed predominantly of a single muscle fiber type (for mouse, see Jansen, 1988, 1990; for rat, see Thompson et al, 1984Thompson et al, , 1987Thompson et al, , 1990; for rabbit, see Gordon and Van Essen, 1985;Soha et al, 1987;Cramer and Van Essen, 1995). Figure 9.…”

“…Recent evidence also shows that in the adult, some intrinsic differences between fiber types may still exist, setting limits to their ability to be converted by patterns of electrical activity (e.g., Dum et al, 1985;Foehring et al, 1987;Foehring and Munson, 1990;Gordon et al, 1997). Finally, neonatal studies in the rat (Thompson et al, 1984(Thompson et al, , 1990, mouse Jansen, 1988, 1990), and rabbit (Gordon and Van Essen, 1985;Soha et al, 1987;Cramer and Van Essen, 1995) have found that motor units are heavily biased toward one fiber type, providing strong evidence to support an initial period of selective recognition (for selective reinnervation during this period, see also Soileau et al, 1987).…”

“…This observation together with the lack of molecular markers for young fast and slow motoneurons has led many investigators to favor initial nonselective innervation (for review, see Jolesz and Sreter, 1981). In contrast, the fact that neonatal rodent motor units are strongly biased toward one fiber type (for mouse, see Jansen, 1988, 1990; for rat, see Thompson et al, 1984Thompson et al, , 1987Thompson et al, , 1990; and for rabbit, see Gordon and Van Essen, 1985;Soha et al, 1987;Cramer and Van Essen, 1995) favors selective innervation, as do several other experimental studies in both chick and mammal (Feng et al, 1965;Hnik et al, 1967;Hoh, 1975;Soileau et al, 1987;Vogel, 1987;Vogel and Landmesser, 1987;Rafuse et al, 1996).…”

A developmentally regulated disappearance of slow myosin in fast‐type muscles of the mouse

“…This could lead to some slow myosin-containing fibers being innervated by a slow motor neuron with the result that slow myosin is maintained into adult stages. A further possibility is that slow myosincontaining fibers and slow nerves might arise separately and then be actively matched during development [33]. These mechanisms could reconcile the different observations concerning the fate of slow myosin-containing fibers in the EDL muscles of young rats and mice: in the rat, slow motor units clearly develop and are present in the adult muscle, whereas in the mouse they often are not.…”

Histochemical profiles of fibers in the rat tibialis anterior muscle during early postnatal development.

“…Therefore, the type shift of muscle fibers from S to F immediately after the differentiation of fibers occurs while still multiply innervated. Whether the histochemical properties of muscle fibers under multiple innervation are regulated by neuronal factors of the predetermined spinal motoneurons, the functional activity, and/or neurotrophic factors has been discussed in previous studies (THOMPSON et al, 1984;GORDON and VAN ESSEN, 1985;JONES et at., 1987a, b;FLADBY and JANSEN, 1988;REDENBACH et al, 1988). Although the mechanism underlying the type shift of muscle fibers under multiple innervation is not clear, our findings suggest that collateral sprouting from type-different motoneurons which differentiate earlier causes the type shift of muscle fibers during early postnatal development, as observed by MIYATA and YOsHIOKA (1980) All muscle fibers 1 day after birth showed a uniform reaction for the enzyme, but fast-twitch (dark) and slow-twitch (light) fibers were found at 9 days.…”