Detachment of structurally intact nerve endings from chromatolytic neurones of rat superior cervical ganglion during the depression of synaptic transmission induced by post‐ganglionic axotomy.

Abstract

SUMMARY1. Electrophysiological studies showed that injury of post-ganglionic nerve fibres leads to severe and prolonged depression of synaptic transmission through the rat superior cervical ganglion, beginning within 24 h. This is in line with the results of previous studies in other species and upon other neurones.2. Electron microscopy after post-ganglionic axotomy revealed nerve endings of presynaptic type with all the specialized membrane-related features of a synaptic zone, but which were not apposed to any postsynaptic nervous element. These unusual profiles were interpreted as detached presynaptic nerve endings. In normal and control ganglia, such profiles formed at most 05 % of-all vesicle-containing profiles of presynaptic type; in ganglia with all major post-ganglionic branches cut the proportion rose to approximately 7 %, between 3 and 7 d post-operatively.Over this period,' the mean incidence of chromatolytic neurones was 74.6%.3. Concomitantly, the -incidence of synapses within the ganglion fell by about 75 %, reaching its lowest levels between 3 and 7 d post-operatively.There was strikingly little evidence of persistence of post-synaptic membrane specializations ('membrane thickenings') following detachment of synapses. 4. At longer survival intervals the incidence of synapses gradually increased, and that of detached nerve endings gradually decreased; recovery was well advanced by 42 d.5. The fall in the incidence of synapses was closely paralleled by a fall in the incidence of desmosome-like attachments in the ganglion; the * M.R.C. Scholar. 92 MARGARET R. MATTHEWS AND VICTORIA H. NELSON incidence of such attachments was found to be correlated to a significant degree with that of synapses.6. It is concluded that most or all of the synapses upon sympathetic neurones become physically dissociated during the chromatolytic reaction of these neurones to axotomy. The failure to persist of ultrastructurally specialized post-synaptic sites, and the loss of desmosomes (particularly marked for those involving purely post-ganglionic nervous elements) suggest that the post-ganglionic neurone is losing all its specializations for attachment. 7. Some evidence suggests that the satellite cells may effect the final separation between pre-and post-synaptic structures.

Changes in the dendritic geometry of mouse superior cervical ganglion cells following postganglionic axotomy

“…One aspect of the present observations that is not easily rationalized is the presence on some axotomized cells of fine processes that appear to be elongating rather than retracting (see Matthews and Nelson, 1975;Purves, 1975). Dendritic sprouting has also been reported in lamprey hindbrain neurons when the axons are transected close to the cell bodies (Hall and Cohen, 1983), and chronically axotomized cat spinal motoneurons respond to axotomy by developing supernumerary axons (Havton and Kellerth, 1987).…”

“…A. Johnson, unpublished observations). Perhaps the cholinergic population of superior cervical ganglion cells (thought to be about 5%; see Sjiiqvist, 1963a,b;Buckley et al, 1967;Yamauchi et al, 1973) reacts in a manner similar to the preganglionic synapse loss that follows axotomy (Matthews and Nelson, 1975;Purves, 1975).…”

Transient, axotomy‐induced changes in the membrane properties of crayfish central neurones.

“…Fig. 4B Kuno & Llinas, 1970); guinea-pig superior cervical ganglion (Purves, 1975;Matthews & Nelson, 1975); chick ciliary ganglion (Pilar & Landmesser, 1972;Brenner & Johnson, 1976;Brenner & Martin, 1976); mouse hypoglossal nucleus (Watson, 1965). However, decreased synaptic efficacy is not universal.…”

Propagation of activity-dependent synaptic depression in simple neural networks

“…Retrograde signals also flow across the synapse on a slower timescale to regulate the development, maintenance and modification of the properties of the presynaptic neuron 1,[37][38][39][40][41] . Gradual loss of synapses at the dendrites after axotomy [42][43][44] or interruption of axonal transport 45 has demonstrated the existence of slow axon-dendritic trophic interaction of the order of days to weeks which is crucial for maintaining the structural and functional integrity of synaptic inputs at the dendrites. Our results on the back propagation of synaptic depression further indicate an axon-dendritic signalling that conveys information on activity-dependent synaptic modification at the axonal terminals with a timescale of the order of minutes.…”