The formation of synapses in striated muscle during development

Bennett, Max R.; Pettigrew, A. G.

doi:10.1113/jphysiol.1974.sp010670

Cited by 453 publications

(186 citation statements)

References 38 publications

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“…This may imply that the L4 root sends two different axons whose conduction velocities are different (cf. Redfern, 1970;Bennett & Pettigrew, 1974). This was confirmed by a warm-cold analysis (see below).…”

Section: R9sultssupporting

confidence: 56%

“…At day 6, all the muscle fibres were polyneuronally innervated. Singly innervated fibres were first found at day 9 (about imply that the elimination starts at day 9, because the number of inputs per fibre decreased linearly from 6 to 13 days from an average of 3-2 to an average of 1-34 (see also Bennett & Pettigrew, 1974;Brown et al 1976 3 and 4 and Table 1). This may indicate that even in adults, at least 5-10 % of fibres are polyneuronally innervated (cf.…”

Section: R9sultsmentioning

confidence: 99%

“…Skeletal muscle fibres of new-born animals are innervated polyneuronally, but in a few weeks they acquire the adult type single innervation by the elimination of all nerve terminals except one (Redfern, 1970; Bugust, Lewis & Westerman, 1973;Bennett & Pettigrew, 1974;Brown, Jansen & Van Essen, 1976;Rosenthal & Taraskevich, 1977;O'Brien, Ostberg & Vrbova, 1978). The mechanism underlying the elimination is little understood and has been questioned mainly in two ways:…”

Section: Introductionmentioning

confidence: 99%

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selective elimination of motor nerve terminals in the rat soleus muscle during development.

Miyata¹,

Yoshioka²

1980

The Journal of Physiology

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SUMMARY1. The pattern of innervation and either frequency of miniature end-plate potentials (m.e.p.p.s) or acetylcholine (ACh) sensitivity was examined in individual fibres of the soleus muscle in new-born rats to elucidate the mechanism of elimination of motor nerve terminals.2. The number of motor nerve terminals innervating a muscle fibre was judged by the difference in latencies of end-plate potentials evoked by stimulation of the ventral roots L4 and L5.3. At early developmental stages, about 50 % of soleus muscle fibres were usually singly innervated by the L5 ventral root and this nerve to fibre relation did not change throughout the developmental days. In contrast to the L5 root, the L4 root innervated all the muscle fibres polyneuronally at day 6. In day 16 or older animals, the remaining half of the fibres were singly innervated by the L4 ventral nerves. Therefore, it is concluded that the elimination of motor nerve terminals in the soleus muscle occurs selectively only for the L4 ventral nerves.4. The number of polyneuronally innervated fibres was increased, to some extent, within 2 days after transaction of the spinal cord at day 12. It is suggested that the increased polyneuronal innervation following the inactivity produced by cordotomy may reflect the recovery of terminals which had lost function only a short time previously during elimination.5. Though frequency of m.e.p.p.s increased from day 6 to adult age as previously reported, there was no significant difference in the frequencies between singly and polyneuronally innervated fibres at any age. Cord transaction at day 12 caused no change in the frequency.6. ACh sensitivity observed in singly innervated fibres was similar to that in polyneuronally innervated fibres. Furthermore, cordotomy on day 12 did not induce an increase in ACh sensitivity around the end-plate. It is concluded that the elimination of terminals is not causally related to changes in ACh sensitivity.7. The possible mechanisms of selective elimination of terminals and the process of elimination are discussed.

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Section: R9sultssupporting

confidence: 56%

Section: R9sultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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selective elimination of motor nerve terminals in the rat soleus muscle during development.

Miyata¹,

Yoshioka²

1980

The Journal of Physiology

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“…Whether innervation of skeletal muscles plays a critical role in the isoform transitions observed during postnatal development is controversial. From embryological day 18 (19) up until P-14, rat Dia m innervation is polyneuronal (4,12), and, therefore, MHC isoform expression in the rat Dia m can be influenced by more than one motoneuron during the first 2 postnatal wk. Coincident with the completion of synapse elimination and the withdrawal of polyneuronal innervation, expression of MHC 2X and MHC 2B protein isoforms occurs, and their relative expression continues to increase through P-28 when the adult pattern of MHC isoform expression is fully established.…”

Section: Discussionmentioning

confidence: 99%

Mechanisms underlying myosin heavy chain expression during development of the rat diaphragm muscle

Geiger¹,

Bailey²,

Mantilla³

et al. 2006

Journal of Applied Physiology

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real-time reverse transcriptase-polymerase chain reaction; electrophoresis; myosin heavy chain gene regulation; muscle plasticity IN THE RAT DIAPHRAGM MUSCLE (Dia m ), significant changes in myosin heavy chain (MHC) isoform expression occur during the first 4 wk of postnatal development (22-24, 38, 39, 41). Most fibers express protein for the MHC Neo isoform at birth (P-0), but the relative expression of this isoform gradually decreases until it disappears by postnatal day 28 (P-28). In contrast, MHC 2X and MHC 2B protein isoforms are not expressed in the rat Dia m until at least the second postnatal week. Postnatal development of the rat Dia m is also characterized by changes in muscle contractile properties and by significant growth of muscle fibers, most notably those expressing MHC 2X and MHC 2B (15,22,36,38,42,43,45,47). Thus the relative MHC isoform composition changes during postnatal development of the Dia m , and ultimately it determines Dia m function. At the present time, very little is known about the underlying mechanisms regulating MHC phenotype expression.Previous studies of postnatal development, both in limb muscles and the Dia m , have focused exclusively on changes in the relative protein expression of the different MHC isoforms in the whole muscle (9, 11, 22-24, 30, 31, 33, 38, 39, 45). However, during postnatal development of the rat Dia m , MHC content (measured by MHC mass per half-sarcomere volume and fiber cross-sectional area) increases markedly (15). This increase varies across fiber types (classified based on MHC isoform expression). At single Dia m fibers, the developmental increase in MHC content is greater in fibers expressing MHC 2X and/or MHC 2B isoforms than in those expressing MHC Slow or MHC 2A . Thus, during postnatal development, not only do Dia m fibers increase in size but also they increase their MHC protein content. This substantial increase in total MHC protein expression across Dia m fiber types is not evident if only the relative expression of MHC isoform is examined.The period from birth to adulthood provides a unique and significant opportunity to examine the mechanisms underlying rapid muscle growth and phenotype transitions. In rat limb muscles, postnatal muscle phenotype is regulated by MHC gene expression either as a result from mechanical stretch induced by skeletal growth and/or increased muscle activity (18). At present, there is no direct information regarding the transcriptional regulation of MHC isoform expression during postnatal development of the rat Dia m .An increase in MHC protein of the rat Dia m during postnatal development could be due to transcriptional, translational, and/or posttranslational mechanisms, which may vary depending on fiber type (10). Assuming transcriptional rate remains constant, an increase in mRNA expression would result in increased protein expression. For example, patterns of MHC isoform-specific mRNA and protein expression are very similar during postnatal development in pigs (25). We hypothesized that postnatal transitions ...

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“…Two well known paradigms for these phenomena are Hebb's postulate (6) and spike-timing-dependent plasticity (STDP) (7-10). A classic model to investigate synaptic modification is the elimination of input that occurs at developing neuromuscular junctions (NMJs) as a result of competition among the motor nerve terminals (11)(12)(13)(14). Elimination of input is widespread in the developing peripheral nervous system and CNS; at the NMJ, where it was identified (13), it spans the first 2 wk of postnatal life in rodents, during which time the innervation of each muscle fiber changes from innervation by the collaterals of different motor neurons (polyneuronal innervation) to innervation by only one collateral (mononeuronal innervation).…”

mentioning

confidence: 99%

Spike timing plays a key role in synapse elimination at the neuromuscular junction

Favero

Busetto²,

Cangiano³

2012

Proc. Natl. Acad. Sci. U.S.A.

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Nerve impulse activity produces both developmental and adult plastic changes in neural networks. For development, however, its precise role and the mechanisms involved remain elusive. Using the classic model of synapse competition and elimination at newly formed neuromuscular junctions, we asked whether spike timing is the instructive signal at inputs competing for synaptic space. Using a rat strain whose soleus muscle is innervated by two nerves, we chronically evoked different temporal spike patterns in the two nerves during synapse formation in the adult. We found that asynchronous activity imposed upon the two nerves promotes synapse elimination, provided that their relative spikes are separated by 25 ms or more; remarkably, this elimination occurs even though an equal number of spikes were evoked in the competing axons. On the other hand, when spikes are separated by 20 ms or less, activity is perceived as synchronous, and elimination is prevented. Thus, in development, as in adult plasticity, precise spike timing plays an instructive role in synaptic modification.I n the adult brain, plastic changes in the strength of synaptic connections between excitable cells occur as a result of experience and contribute to shaping its architecture during development. Many of these changes are known to be tightly linked to the pattern of action potential firing. Temporal spike correlation in pre-and postsynaptic cells strengthens or weakens synapses during development (1-3) and in cellular models of learning (long-term potentiation and depression) (4, 5). Two well known paradigms for these phenomena are Hebb's postulate (6) and spike-timing-dependent plasticity (STDP) (7-10). A classic model to investigate synaptic modification is the elimination of input that occurs at developing neuromuscular junctions (NMJs) as a result of competition among the motor nerve terminals (11)(12)(13)(14). Elimination of input is widespread in the developing peripheral nervous system and CNS; at the NMJ, where it was identified (13), it spans the first 2 wk of postnatal life in rodents, during which time the innervation of each muscle fiber changes from innervation by the collaterals of different motor neurons (polyneuronal innervation) to innervation by only one collateral (mononeuronal innervation). Examples of this peculiar end result also are observed in the CNS (e.g., the innervation of Purkinje cells by climbing fibers) (15). Activity influences this process, but its precise role remains controversial. Briefly, some studies emphasize the overall neuromuscular activity, others emphasize the differences in the amount of activity in competing inputs, and still other studies emphasize activity-independent factors (16-27). (We explore this controversy in more detail in the Discussion.)Differences in activity generally have been tested by comparing active inputs with inputs completely inactivated by conduction block. However, the insight gained from these experiments is limited because all competing motor terminals are active during norma...

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The formation of synapses in striated muscle during development

Cited by 453 publications

References 38 publications

selective elimination of motor nerve terminals in the rat soleus muscle during development.

selective elimination of motor nerve terminals in the rat soleus muscle during development.

Mechanisms underlying myosin heavy chain expression during development of the rat diaphragm muscle

Spike timing plays a key role in synapse elimination at the neuromuscular junction

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