Elsevier

Neuroscience

Volume 103, Issue 4, 4 April 2001, Pages 1059-1071
Neuroscience

Long-term changes in the distribution of galanin in dorsal root ganglia after sciatic or spinal nerve transection in rats

https://doi.org/10.1016/S0306-4522(01)00025-2Get rights and content

Abstract

The neuropeptide galanin is upregulated in primary afferent and sympathetic neurones and might be involved in the development of sympathetic perineuronal baskets (“rings”) following nerve injury. Galanin, calcitonin gene-related peptide and tyrosine hydroxylase have been examined immunohistochemically in dorsal root ganglia and associated roots at times up to one year after transection of either sciatic or L5 spinal nerves in adult rats. Small diameter somata containing calcitonin gene-related peptide (with or without galanin) were reduced in number, whereas galanin (and, at later times, calcitonin gene-related peptide) appeared in medium to large diameter cells after both types of lesion. Galanin also appeared in axons in grey rami and somata in lumbar paravertebral ganglia. Within dorsal root ganglia, galanin-positive axons formed perineuronal rings of two types: (i) smooth coiled axons surrounded small (<30 μm diameter) somata from which they probably arose; these were rare after 12 weeks, particularly after a spinal nerve lesion; and (ii) varicose terminals encircled medium to large galanin-positive somata; some arose from brightly immunofluorescent somata nearby and took nearly a year to disappear. About 30% of varicose galanin-positive rings had associated calcitonin gene-related peptide-positive terminals (partly colocalized) whereas nearly 45% had associated tyrosine hydroxylase-positive terminals (partly colocalized). Synaptophysin was present in swollen axons and in some varicosities of all types.

We conclude that, after peripheral nerve lesions, varicose perineuronal rings around large diameter dorsal root ganglion cells may be formed by axotomized primary afferent neurones (some containing calcitonin gene-related peptide) and sympathetic neurones, both of which contain upregulated galanin. Exocytosis from the varicosities may modify the excitability of mechanosensitive somata. Small galanin-positive somata disappear over several months after both lesions as calcitonin gene-related peptide reappears in medium to large neurones.

Section snippets

Experimental procedures

Female Wistar rats (Biological Resources Centre, UNSW; six to eight weeks of age at operation; 124–177 g) were used in this study. Under anaesthesia with i.p. ketamine 60 mg/kg plus xylazine 10 mg/kg, either the left sciatic nerve, or the ventral ramus of the left L5 spinal nerve, was ligated and cut peripherally. In four animals, Fast Blue (FB) was applied to the cut axons at the time of the sciatic lesion. Two (n=2), six (n=1), eight (n=3), 9–10 (n=6), 12 (n=2), 30 (n=2), 49 (n=1) and 55 (n=1)

Results

There were no detectable differences between naive control tissue and that from the side contralateral to the injury and both will be referred to as control.

Discussion

The present results confirm that GAL is upregulated in DRG somata after axotomy7 but also provide information about the long-term changes in GAL expression after both sciatic and spinal nerve lesions. This is the first report that GAL+ axons sprout within the DRGs containing neurones that project into damaged peripheral nerves. Previously, sprouting noradrenergic4., 20., 24. and SP/CGRP-containing19 axons and perineuronal rings have been described following various forms of nerve injury. The

Acknowledgements

This work was supported by grants from the National Health & Medical Research Council of Australia and by the Motor Accidents Authority of New South Wales. Drs Janet Keast and James Brock provided helpful comments on an earlier version of the manuscript.

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