The formation of synapses in reinnervated and cross‐reinnervated adult avian muscle

Abstract

SUMMARY1. A study has been made of the formation of synapses in spontaneously reinnervated and cross-reinnervated anterior latissimus dorsi (ALD) and posterior latissimus dorsi (PLD) muscles of adult fowls.2. Denervated ALD and PLD muscle fibres have a uniform and high sensitivity to iontophoretically applied acetylcholine (ACh). During early reinnervation the sensitivity distribution to ACh of the ALD muscle fibres begins to return to normal before synaptic potentials can be evoked. The normal ACh sensitivity distribution of PLD muscle fibres is also restored after reinnervation. After cross-reinnervation of the ALD and PLD muscles the ACh sensitivity distribution of many of the muscle fibres is again restored to normal.3. Reinnervating and cross-reinnervating ALD nerve terminals showed a greater than normal degree of facilitation of transmitter release when a test impulse was applied at various intervals after a conditioning impulse. Cross-reinnervating PLD nerve terminals showed facilitation of transmitter release rather than the normal depression in a conditioningtest impulse sequence.4. The distribution of nerve terminals over the surface of spontaneously reinnervated and cross-reinnervated ALD and PLD muscle fibres has been determined from an examination of the sensitivity distribution to applied ACh, the graded versus all-or-none nature of the evoked potential and the distribution of cholinesterase stained synapses.5. The results suggest that the innervation pattern of individual ALD and PLD muscle fibres is restored both after spontaneous reinnervation and cross-reinnervation.

The formation of synapses in mammalian sympathetic ganglia reinnervated with preganglionic or somatic nerves

“…The presence of structures resembling the axon growth cones described in the developing central nervous system (Bodian, 1966) suggests that the somatic axons persist in an active state within the ganglion but are unable to form synapses on the denervated ganglion cells. Together with the paucity of synapses formed in cross-reinnervated avian striated muscles (Bennett, Pettigrew & Taylor, 1973), and mammalian striated muscle crossreinnervated with preganglionic axons (Bennett, McLachlan & Taylor, 1973b), these observations suggest that the mechanism of selectivity of synapse formation is located at the synaptic site on the effector. I am very grateful to M. R. Bennett for his advice and criticism of the manuscript.…”

“…Few synapses are formed in muscles reinnervated with either somatic or autonomic nerves, which normally supply multiply innervated effectors, while those which are formed also occur at the old synaptic sites (Landmesser, 1972;Bennett, Pettigrew & Taylor, 1973;Bennett, McLachlan & Taylor, 1973b). These observations suggest that the mechanism of selectivity in the innervation of a muscle occurs at the synaptic sites themselves.…”

“…Polyneuronal reinnervation of sympathetic motorneurones was detected at later stages following regeneration of preganglionic axons, but never in cross-reinnervated cells. Axons which normally focally innervate avian fast muscle fibres form a multiple and distributed innervation on slow muscle fibres (Bennett, Pettigrew & Taylor, 1973); because of the scarcity of observations, it is not possible to conclude whether or not this is true for mammalian cells.…”

“…Electrophysiological studies of denervated ganglion cells revealed no modifications of the specific membrane parameters, membrane potential or threshold. Hyperexcitability to injected acetylcholine (Simeone, Cannon & Rosenblueth, 1938) seems likely to be a consequence of the outgrowth of receptors over the surface of the neuron ; whether these extrajunctional receptors disappear following reinnervation as do those in striated muscle (McArdle & Albuquerque, 1972;Bennett, Pettigrew & Taylor, 1973), or change their properties depending on the type of reinnervating nerve (Landmesser, 1972), remains to be determined. The invariance of both structural and electrical parameters measured in this 234 REINNERVATION OF MAMMALIAN GANGLIA 23 study, together with the absence of changes in fine structure (see also Hunt & Nelson, 1965;Ha'mori, Lang & Simon, 1968;Ceccarelli et al 1971), implies that preganglionic terminals play little part in the maintenance of these properties of autonomic motorneurones.…”

“…Reinnervation of adult striated muscles with their own nerves leads to extensive restoration of synapses at the original synaptic sites on the muscle fibres (Miledi, 1960;Bennett, Pettigrew & Taylor, 1973; Bennett, McLachlan & Taylor, 1973a). Few synapses are formed in muscles reinnervated with either somatic or autonomic nerves, which normally supply multiply innervated effectors, while those which are formed also occur at the old synaptic sites (Landmesser, 1972;Bennett, Pettigrew & Taylor, 1973;Bennett, McLachlan & Taylor, 1973b).…”