Postnatal emergence of mature release properties in terminals of rat fast‐ and slow‐twitch muscles

Abstract

Motor nerve terminals in adult mammalian slow-twitch muscles have lower levels of spontaneous and evoked neurotransmitter release than terminals in fast-twitch muscles. These reflect adaptive differences, allowing terminals in slow (postural) muscles to sustain release during the prolonged firing trains experienced in vivo. Here we ask whether these differences in terminal release properties in Sprague-Dawley rat extensor digitorum longus (EDL, fast) and soleus (slow) muscles reflect their early cytodifferentiation in the embryo or whether they might be adaptations to their distinct mature activity patterns, which emerge around two weeks postnatally. We find that the mature pattern of differences in release arise through co-ordinated increases in presynaptically dependent release properties (quantal content, spontaneous release frequency and evoked potential amplitude), beginning at three weeks, which are particularly substantial in EDL. In contrast, other synaptic properties are either consistently greater in the same muscle throughout development (evoked potential kinetics, muscle fibre diameter) or display no systematic muscle type-dependent differences (terminal area, input resistance, spontaneous release amplitude). Thus, the emergence of adaptive differences in terminal release properties correlates with the differentiation of locomotor activity patterns in postnatal rat hindlimb muscles.

Retrograde influence of muscle fibers on their innervation revealed by a novel marker for slow motoneurons

“…However, although there is evidence for metabolic heterogeneity among embryonic motoneurons (Huizar et al, 1975;Sheard et al, 1997), there is no direct evidence on when type-specific properties are acquired, and at least some diversification continues until the end of the first postnatal month, after motor patterns are established (Bewick et al, 2004). Our results indicate that one characteristic difference between fast and slow motoneurons -the restriction of SV2A expression to the latter -occurs during the first postnatal week.…”

Increased Neurotransmitter Release at the Neuromuscular Junction in a Mouse Model of Polyglutamine Disease

“…To minimize errors in the quantal content estimation, we have corrected the effect of nonlinear summation on EPP amplitude as previously described (McLachlan and Martin, 1981) using a correction factor ( f ϭ 0.8) (see Materials and Methods). The introduction of that factor improves overcorrection introduced by older methods (Martin, 1955), and it has been used in different mouse neuromuscular preparations (Plomp et al, 1992;Wood and Slater, 1997;Bullens et al, 2002;Bewick et al, 2004;Chen et al, 2010). Current-clamp measurements of quantal content could be relatively inaccurate if compared with absolute quantal content values obtained with voltage-clamp recordings as previously described in other preparations (Wood and Slater, 1997).…”

Tissue inhibitor of metalloproteinase‐2 (TIMP‐2) regulates neuromuscular junction development via a β1 integrin‐mediated mechanism

“…Motor nerve terminals and the muscle fibers they innervate are physiologically adapted to the distinct functional demands they experience. The development of fast motor nerve terminal characteristics (Bewick et al, 2004) and fast-twitch muscle fibers (DiMario and Stockdale, 1997;Wigmore and Evans, 2002) emerges during the second postnatal week as pups progress from sedentary sucklings to active weight-bearing locomotion.…”