The effect of neuronal activity on the competitive elimination of neuromuscular junctions in tissue culture

Magchielse, T.; Meeter, E.

doi:10.1016/0165-3806(86)90210-5

Cited by 31 publications

(10 citation statements)

References 32 publications

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“…No explanation for the last behavior, termed anti-Hebbian (Nelson et al, 1993) and for the discrepancy between the two sets of results has been established (Jansen and Fladby, 1990); nor can we offer one here. The most direct conflict between our findings and previous data are the accelerated synapse elimination induced by nerve electrical stimulation in soleus muscles of newborn rats (O'Brien et al, 1978;Thompson, 1983) or in culture (Magchielse and Meeter, 1986;Nelson et al, 1993), particularly of a fast pattern (Thompson, 1983). Two factors, both probably operative, can explain this discrepancy.…”

Section: Discussioncontrasting

confidence: 57%

“…ACh hypersensitivity is suppressed by activity (Lømo and Westgaard, 1975) and documented by Thompson (1983) in his preparation and, as argued by him, may help explain why stimulation speeds up elimination in the newborn rat. This may also apply to similar effects of stimulation in culture (Magchielse and Meeter, 1986;Nelson et al, 1993): although not tested, ACh hypersensitivity may well be present in the myofibers because of a likely low level of spontaneous activity of innervating neurons. In our reinnervated adult soleus, ACh hypersensitivity is essentially gone by 15 d, along with other extrajunctional membrane changes induced by denervation, and no f urther inhibitory effect of stimulation on this parameter and associated production of "innervation factor" can occur.…”

Section: Discussionmentioning

confidence: 99%

“…Action potential activity strongly controls this process. Synapse elimination is in fact suppressed by block of activity (Benoit and Changeux, 1975;Thompson et al, 1979;Brown et al, 1981), whereas it is accelerated by its increase induced by electrical stimulation (O'Brien et al, 1978;Thompson, 1983;Magchielse and Meeter, 1986;Nelson et al, 1993).…”

Section: Abstract: Synapse Elimination; Synchronous Activity; Synaptmentioning

confidence: 99%

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Hebbian Mechanisms Revealed by Electrical Stimulation at Developing Rat Neuromuscular Junctions

et al. 2000

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Synapse competition and elimination are widespread developmental processes, first demonstrated at neonatal neuromuscular junctions. Action potential activity was long shown to exert a powerful influence, but mechanisms and contribution relative to other factors are still not well understood. Here we show that replacement of natural motoneuronal discharge with synchronous activity suppresses elimination of polyneuronal innervation of myofibers. This requires the simultaneous chronic conduction block (tetrodotoxin) and distal electrical stimulation of motor axons during ectopic synaptogenesis in denervated adult soleus muscle. If in fact chronic stimulation is applied without central block of motor axons, the time course of synapse elimination is as fast as in control muscles undergoing natural activity. Our findings follow the prediction of Hebb's postulate and imply that asynchronous activity drives developmental synapse elimination in muscle. They further suggest that motoneurons could become transiently synchronized during development and regeneration, helping to establish the initial polyneuronal innervation.

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Section: Discussioncontrasting

confidence: 57%

Section: Discussionmentioning

confidence: 99%

Section: Abstract: Synapse Elimination; Synchronous Activity; Synaptmentioning

confidence: 99%

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Hebbian Mechanisms Revealed by Electrical Stimulation at Developing Rat Neuromuscular Junctions

et al. 2000

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“…An in vitro system, in which more active synapses are preferentially retained during elimination, has been described by Magchielse and Meeter (1986). In their system, chick ciliary Activity=2A Activity=A Activity=A (parasympathetic) neurons were made to innervate skeletal muscle fibers polyneuronally, but the multiple inputs were distributed across spatially separated endplates.…”

Section: Activitymentioning

confidence: 99%

“…One of these studies involved differential activity during normal neuromuscular development (Ridge and Betz, 1984); 3 involved reinnervation of adult muscle Taxt, 1983, 1984;Ribchester, 1988b); and the last involved a tissue culture preparation (Magchielse and Meeter, 1986).…”

Section: Activitymentioning

confidence: 99%

Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons

1989

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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–s15 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.

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Reorganization of Synaptic Inputs to Developing Skeletal Muscle Fibres

Vrbová

J³

2007

Ciba Foundation Symposium 138 ‐ Plasticity of the Neuromuscular System

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The effect of neuronal activity on the competitive elimination of neuromuscular junctions in tissue culture

Cited by 31 publications

References 32 publications

Hebbian Mechanisms Revealed by Electrical Stimulation at Developing Rat Neuromuscular Junctions

Hebbian Mechanisms Revealed by Electrical Stimulation at Developing Rat Neuromuscular Junctions

Differential loss of neuromuscular connections according to activity level and spinal position of neonatal rabbit soleus motor neurons

Reorganization of Synaptic Inputs to Developing Skeletal Muscle Fibres

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