Formation and elimination of foreign synapses on adult salamander muscle

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.

Section: Discussionmentioning

confidence: 99%

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

Miyata¹,

Yoshioka²

1980

“…Only those neurones whose axons would be expected to regenerate ipsilateral to the cell body of the g.i.s (contralateral g.i.s, ipsilateral d.c.s and r.a.s) were tested. Similarly, the dendritic trees of l.c.s span the ipsilateral half of the spinal cord (Ringham, 1975;Rovainen, 1974a (Mark, Marotte & Mart, 1972), 'silent synapses' do not seem to occur at the vertebrate neuromuscular junction (Dennis & Yip, 1978). A mismatched axon might release a transmitter to which the post-synaptic receptors could not respond.…”

Section: Selectivity Of Synapse Formation By Regenerating Lamprey Axonsmentioning

confidence: 99%

“…In a few examples this appears to involve a degree of selective reinnervation of the post-synaptic targets. Examples include reinnervation of the neuromuscular junction of fish, amphibia, and mammals (Sperry & Arora, 1965 (however, see Scherer, 1986); Dennis & Yip, 1978;Wigston & Sanes, 1985), regeneration of sensory input onto spinal motor neurones in the bull-frog (Sah & Frank, 1984), reinnervation of autonomic ganglia in mammals (NjA, & Purves, 1977;Purves, Thompson & Yip, 1981), and the restoration of correct retinotectal projections in fish and amphibia (Attardi & Sperry, 1963;Fujisawa, 1981). Specificity has been suggested by some observations on synaptic regeneration of identified invertebrate neurones, both in vivo (Jansen & Nicholls, 1972) and in vitro (Fuchs, Nicholls & Ready, 1981).…”

Section: Introductionmentioning

confidence: 99%

Specificity of synaptic regeneration in the spinal cord of the larval sea lamprey.

Mackler

Selzer

1987

SUMMARY1. Pairs of central neurones in large larval sea lampreys were impaled with micro-electrodes and studied for synaptic connexions in both unoperated control animals and animals which had recovered from complete spinal transection. Two identified classes of neurones served as post-synaptic targets: giant interneurones (g.i.s) and lateral cells (l.c.s). Several identified neurone types were tested as potential sources of presynaptic input.2. When synaptic potentials had short, fixed latencies they also persisted during activation of the presynaptic cell at 3 3-33 3 Hz and were not eliminated after addition of lamprey saline containing high (20 mM) Ca2+. These presumably represented monosynaptic connexions. Variable-latency responses were eliminated by faster rates of stimulation of the presynaptic cell and were mediated via polysynaptic pathways.3. In control animals, g.i.s received monosynaptic input from more caudal g.i.s in fourteen of thirty-two tested cell pairs. These excitatory post-synaptic potentials (e.p.s.p.s) were composite electrochemical responses. The amplitudes of the earlier electrical component averaged 1-66 + 0-24 mV -(mean+ s.E. of mean) and the amplitude of the later chemical component averaged 0-79 ± 0 05 mV.4. In operated larvae, eight of forty-seven g.i.-g.i. pairs separated by the transection scar were connected by monosynaptic composite e.p.s.p.s. In these pairs the electrical component averaged 0-84 + 0-17 mV (P < 0 05 vs. control) and the chemical component averaged 1 56 + 0 40 mV. The average conduction velocity between these cells was less than that in control g.i.-g.i. pairs (0-93 + 0-11 vs. 1-61 + 0-25 m/s; P<0-01).5. The l.c.s showed monosynaptic e.p.s.p.s after activation of a subset of the bulbar Muller neurones (B2<) in seven of twelve pairs. In behaviourally recovered larvae three of twenty-two similar pairs separated by the transection scar were also connected via monosynaptic e.p.s.p.s. The average conduction velocity between these experimental neurones was also less than that in control bulbar-l.c. pairs (1-03+0-03vs. 1-58+0-09 m/s; P < 0-001).6. Several types of neurones were either infrequently linked or never connected to g.i.s or to l.c.s in control larvae. In animals which had recovered from a spinal S. A. MACKLER AND M. E. SELZER transection, no synaptic connexions were found from such neurones on to g.i.s or l.c.s respectively, in 124 tested cell pairs. In addition, dorsal cells (intraspinal primary sensory neurones) received no synaptic input upon stimulation of the spinal cord before or after transection.7. These findings indicate that regenerating spinal axons in the larval sea lamprey form functioning synapses directly onto neurones positioned within 8 mm distal to the healed transection scar. These axons appear to exhibit selectivity in their choice of synaptic targets.

“…Mark (1969) proposed that specificity of reinnervation could result from a process of competition in which transmission at inappropriate neuromuscular junctions might be suppressed when reinnervation of the muscle by its correct nerve occurred. Direct (Cass, Sutton & Mark, 1973;Bennett & Raftos, 1977; Dennis & Yip, 1978;Wigston, 1980). Although suppression of transmission at inappropriate neuromuscular junctions has been consistently observed in urodeles, it is generally accepted that this is a slow process and that individual muscle fibres may remain innervated by both foreign and original nerves for some time before transmission at the foreign synapses finally fails (Dennis & Yip, 1978;Bennett, McGrath & Davey, 1979;Wigston, 1980).…”

Section: Introductionmentioning

confidence: 99%

Selective reinnervation of skeletal muscle in the newt Triturus cristatus.

Holder¹,

Mills²,

Tonge³

1982

SUMMARY1. A study was made ofthe effectiveness ofsynapses formed by foreign and original nerves during reinnerv -,tion of skeletal muscle of the newt Triturus cri8tatu-8. The extensor cranialis nerve (e.c.n.) of the forelimb was implanted into the humeroantebrachialis muscle (biceps) which was denervated by cutting or crushing the forelimb flexor nerve (f.f.n.).2. Although biceps became innervated by the implanted nerve, neuromuscular transmission was abnormal. The ratio ofthe tensions developed by biceps during single and repetitive (50 Hz) stimulation of e.c.n. was lower than either that obtained in normal biceps or during stimulation of f.f.n. after it had regenerated. Similarly, the mean quantal content of e.p.p.s evoked in biceps during stimulation of e.c.n. were lower (m = 17 1) than those evoked in normal muscles (m = 74 6) or during stimulation of the regenerated f.f.n. (m = 40 4).3. Although the implanted e.c.n. had innervated biceps, after 2-3 months a sprout had grown out of the side of the nerve to reinnervate the extensor digitorum communis muscle (e.d.c.) of the forearm. The mean quantal content of e.p.p.s evoked in this muscle by stimulation of e.c.n. (m = 32 2) was higher than that of those e.p.p.s evoked by stimulation of the same nerve in biceps (m = 17'1). 4. The results suggest that the synapses formed when a muscle is innervated by an inappropriate nerve are less effective than those formed when reinnervation by the correct nerve occurs. This may account for the tendency of the inappropriate synapses to regress following reinnervation by the correct nerve. In addition however, in the newt there seem to exist mechanisms which ensure that regenerating nerves reinnervate their correct muscles.