The temporal course of the effects of postganglionic axotomy on the inferior mesenteric ganglion of the cat

200

119

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.

Section: Introductionmentioning

confidence: 55%

Section: Margaret R Mattheivs and Victoria H Nelsonmentioning

confidence: 94%

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.

Matthews¹,

Nelson²

1975

200

119

“…To determine neuronal geometry, (Brown & Pascoe, 1954;Acheson & Remolina, 1955;Hunt & Riker, 1966;Pilar & Landmesser, 1972;Matthews & Nelson, 1975), and of mammalian spinal motoneurones (Campbell et Kuno & Llina's 1970a, b). Downman et at.…”

Section: T(9)mentioning

confidence: 99%

“…These changes include depression of synaptic transmission (Acheson, Lee & Morison, 1942;Campbell, Mark & Gasteiger, 1949;Downman, Eccles & McIntyre, 1953;Brown & Pascoe, 1954;Acheson & Remolina, 1955; Eccles, Libet & Young, 1958;Hunt & Riker, 1966;Kuno & Llina's, 1970b;Pilar & Landmesser, 1972;Matthews & Nelson, 1975), a complex of morphological changes generally called chromatolysis (see, for example, Lieberman, 1971;Matthews & Raisman, 1972), and changes in neuronal and neuroglial metabolism (Watson, 1965(Watson, , 1968(Watson, , 1969(Watson, , 1970(Watson, , 1972. The effects of axotomy have aroused considerable interest not only because of their dramatic nature, but also because these effects raise the general question of the extent to which a neurone's properties, and even survival, are determined by appropriate peripheral terminations.…”

Section: Introductionmentioning

confidence: 99%

Functional and structural changes in mammalian sympathetic neurones following interruption of their axons.

Purves¹

1975

346

260

SUMMARYThe effects of interrupting the axons of principal neurones in the superior cervical ganglion of adult guinea-pigs were studied by means of intracellular recording, and light and electron microscopy. 5. Little or no difference was found in the electrical properties of normal neurones and neurones whose axons had been interrupted 4-7 days previously. However, the mean amplitude of spontaneously occurring synaptic potentials was reduced, and the amplitude distribution was shifted. This abnormality of the synapses which remain on affected neurones also contributes to synaptic depression.6. Counts of neurones in normal and experimental ganglia showed that approximately half the principal cells died 1-5 weeks after crushing the major efferent branches. This finding presumably explains the failure of synapse counts to return to control levels after recovery.7. If axons were prevented from growing back to their target organ by chronic ligation, surviving neurones whose axons were enclosed by the ligature did not generally recover normal synaptic function. Following ligation, most affected cells died within a month.8. Thus the integrity of a principal cell's axon is necessary for the maintenance of preganglionic synaptic contacts, and ultimately for neuronal survival. The basis of neuronal recovery from the effects of axon interruption appears to be some aspect of regeneration to the peripheral target.

“…The other possible causes noted above will be considered in approximately ascending order of probability. Local effects of intraganglionic factors such as the products of neuronal degeneration (up to 50 % or more of axotomized sympathetic neurones may die in the longer term; Acheson & Remolina, 1951;Purves, 1975;Smolen, 1983) Thoenen, 1983), and might perhaps also directly have accounted for the hypertrophy of the small cells toward some semblance of principal neurones (cf. Aloe & Levi-Montalcini, 1979); but this is unlikely in adult animals: the effects observed by these groups of investigators were confined to neonatal animals, in which synapse formation and the differentiation of neuronal precursors is still incomplete.…”

Section: Discussionmentioning

confidence: 99%

Incoming synapses and size of small granule‐containing cells in a rat sympathetic ganglion after post‐ganglionic axotomy.

Case¹,

Matthews²

1986

SUMMARY1. A quantitative ultrastructural study has been made of the reaction of the incoming synapses of small granule-containing cells after axotomy of the major post-ganglionic branches of the superior cervical ganglion of the young adult rat. These cells are intrinsic and interneurone-like in this ganglion, receiving a preganglionic input and giving outgoing synapses to principal post-ganglionic neurones.2. Unlike their outgoing synapses, which are lost after post-ganglionic axotomy (Case & Matthews, 1986), the incoming synapses of the small granule-containing cells in axotomized ganglia increased in incidence post-operatively. The increase first became clearly evident 5-7 days post-operatively and was greater, being both more sustained and progressive, after bilateral than after unilateral axotomy. After bilateral axotomy the incidence of incoming synapses rose to more than four times that of normal ganglia and was still elevated at 128 days post-operatively, but was within normal limits at 390 days.3. After a unilateral lesion, increases of similar extent and time course to those in the axotomized ganglia were seen in the incoming synapses of small granulecontaining cells in the uninjured contralateral ganglia.4. The incoming synapses of the small granule-containing cells are multifocal, i.e. show several points or active foci of synaptic specialization. The increase in synapses expressed itself both through an increased incidence of these synaptic active foci per nerve terminal and through an increase in the number of~presynaptic nerve terminal profiles associated with the cells.5. Control observations indicated that the increase in synapses was not due to surgical stress, nor was it attributable solely to post-operative ageing.6. The nerve terminals which were presynaptic to the small granule-containing cells post-operatively were all ofpreganglionic origin: no incoming synapses or presynaptic nerve terminals remained at 2 days after a preganglionic denervation of axotomized or contralateral ganglia, at whatever stage this was performed throughout the range of survival intervals.7. There was some evidence that the synapses had increased by sprouting, including terminal sprouting, of the preganglionic nerve fibres. In the shorter term * To whom correspondence should be sent.PHY 374 2 C. P. CASE AND M. R. MATTHEWS there was an increase in the proportion of small nerve terminal profiles. In the longer term the mean size of the terminal profiles increased, and very large terminals of unusual form were seen.8. After post-ganglionic axotomy, and in particular after a bilateral lesion, the small granule-containing cells became hypertrophied. The size of the small granulecontaining cells was directly correlated with both the incidence and the collective size of the preganglionic nerve terminals which innervated them. Both the small granule-containing cells and their incoming innervation thus display a considerable capacity for expansion, such as is found to be inherent also in other neuronal systems.9. These inte...