The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers

Thompson, Wesley J.; Kuffler, Damién P.; Jansen, J. K. S.

doi:10.1016/0306-4522(79)90088-5

Cited by 219 publications

(118 citation statements)

References 23 publications

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“…Polyneuronal innervation of muscles remains when the axonal activity is blocked with TTX [16]. Consistent with this evidence is the finding that the preferential reduction of axons or their collaterals from the incorrect brachium of the goldfish optic tract does not occur at times when misrouted axons or collaterals with normal activity are lost.…”

supporting

confidence: 70%

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Preferential loss of collaterals from goldfish retinal axons in the optic tract is delayed by tetrodotoxin

Hartlieb

Stuermer

1987

Neuroscience Letters

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Key words." Goldfish retinal axon; Regeneration; Brachium of the optic tract; Preferential loss of collaterals; Tetrodotoxin (TTX)Following optic nerve section (ONS) in goldfish, the right eye was repeatedly injected with tetrodotoxin (TTX) and the left eye with Ringer solution. At various survival periods after ONS, horseradish peroxidase (HRP) was applied to small groups of axons in dorsal or ventral retina in both eyes. Counts of labeled regenerating retinal axons show that 43 + 4.6% of regenerating axons course through the inappropriate brachium of the optic tract between 20 and 65 days after ONS. The amount of misrouted axons declines to 30 + 6.1% between 70 and 80 days after ONS. Under TTX blockade the reduction of misrouted axons is delayed but reaches 27+3.6% at 150 days after ONS.When the optic nerve is sectioned in goldfish the retinal axons regenerate. In their target, the tectum opticum, they build a projection of coarse retinotopic order at early regeneration stages which refines to near normal precision around 70 days [6,7].On their way to their target regions in tectum the regenerating axons make severe pathway mistakes [12,13,15]. One location where pathway errors can readily be quantified is the brachial bifurcation of the optic tract. In normal fish more than 99% of all axons from dorsal retina pass through the ventrolateral brachium of the optic tract and ventral axons through the dorsomedial brachium [13]. After optic nerve section roughly 20-30% of dorsal and ventral axons travel through the incorrect brachium [12,13]. According to a recent abstract [1] the amount of misrouted axons at the brachial bifurcation is 40% at early regeneration stages and then drops to 20-30% around 70 days, that is at survival periods when the tectal projection matures to near normal precision [9].When the normal impulse activity of the regenerating axons is blocked with tetrodotoxin (TTX), the refinement of the retinotopic map is inhibited [5,10]. This report addresses the question whether TTX influences the number of incorrectly routed Correspondence: C.A.O. Stuermer, Friedrich-Miescher

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supporting

confidence: 70%

“…There is ample evidence from the neuromuscular systems [16] as well as from visual projections [5,10] that the formation of precisely ordered connections is activity dependent. Polyneuronal innervation of muscles remains when the axonal activity is blocked with TTX [16].…”

mentioning

confidence: 99%

Preferential loss of collaterals from goldfish retinal axons in the optic tract is delayed by tetrodotoxin

Hartlieb

Stuermer

1987

Neuroscience Letters

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“…Also, the concept and the effects of synchronous activity as an Hebbian paradigm, as shown by us here and previously (19,28), cannot be considered equivalent to that of synchronous inactivity [complete paralysis, a paradigm not used here, powerfully stimulates polyneuronal innervation (19,28,62)], because in the latter case it is the up-regulation of the muscle sprouting signal that comes into play.…”

Section: Further Considerations On the Role Of The Timing Of Spike Acmentioning

confidence: 98%

“…The same signal is up-regulated again in adult muscle by paralysis or partial denervation, inducing nerve sprouting and polyneuronal innervation (19,58,59). In all likelihood, this upregulation is why paralysis prolongs polyneuronal innervation during postnatal development (60)(61)(62). According to the above scenario, increasing postsynaptic activity by electrical stimulation in newborn animals down-regulates the muscle signal and speeds up synapse elimination (23,26,63).…”

Section: Further Considerations On the Role Of The Timing Of Spike Acmentioning

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 role of activity in synapse elimination has been extensively studied at neuromuscular junctions between motor neurons and skeletal muscle fibers, at which initial innervation by several different motor axons is followed by synapse elimination culminating in innervation by a single motor axon (7)(8)(9)(10)(11). Reducing overall motor neuron activity delays synapse elimination (8)(9)(10), whereas increasing motor neuron activity accelerates it (12,13).…”

mentioning

confidence: 99%

Reduced gap junctional coupling leads to uncorrelated motor neuron firing and precocious neuromuscular synapse elimination

Personius

Chang

Mentis

et al. 2007

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

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During late embryonic and early postnatal life, neuromuscular junctions undergo synapse elimination that is modulated by patterns of motor neuron activity. Here, we test the hypothesis that reduced spinal neuron gap junctional coupling decreases temporally correlated motor neuron activity that, in turn, modulates neuromuscular synapse elimination, by using mutant mice lacking connexin 40 (Cx40), a developmentally regulated gap junction protein expressed in motor and other spinal neurons. In Cx40 ؊/؊ mice, electrical coupling among lumbar motor neurons, measured by whole-cell recordings, was reduced, and single motor unit recordings in awake, behaving neonates showed that temporally correlated motor neuron activity was also reduced. Immunostaining and intracellular recording showed that the neuromuscular synapse elimination was accelerated in muscles from Cx40 ؊/؊ mice compared with WT littermates. Our work shows that gap junctional coupling modulates neuronal activity patterns that, in turn, mediate synaptic competition, a process that shapes synaptic circuitry in the developing brain.

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The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers

Cited by 219 publications

References 23 publications

Preferential loss of collaterals from goldfish retinal axons in the optic tract is delayed by tetrodotoxin

Preferential loss of collaterals from goldfish retinal axons in the optic tract is delayed by tetrodotoxin

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

Reduced gap junctional coupling leads to uncorrelated motor neuron firing and precocious neuromuscular synapse elimination

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