Remodelling of connections in pelvic ganglia after hypogastric nerve crush

Abstract

Pelvic ganglia innervate the urogenital organs and contain both sympathetic and parasympathetic neurons. Previous studies have shown that within days of cutting either the lumbar or sacral preganglionic axons that innervate pelvic ganglia, many axon collaterals grow and appear to form specific connections with denervated pelvic neurons. Here we have examined the longer term consequences of partial deafferentation by studying pelvic ganglia up to 7 weeks after hypogastric nerve (HGN) crush, a lesion which also allows faster regeneration of spinal axons. Noradrenergic neurons were denervated by HGN crush, as demonstrated by loss of varicosities immunostained for the synaptic proteins, synaptophysin and synapsin. A week after HGN crush, axon collaterals grew from parasympathetic pelvic ganglion neurons, shown by the presence of numerous varicose fibers immunostained for vasoactive intestinal peptide (VIP). These VIP fibers were poorly stained or unstained for synaptophysin, even after 7 weeks. At early post-operative times the VIP fibers grew irregularly; however, with longer post-operative times they appeared to target particular VIP-negative, noradrenergic neurons. Our results also indicate that some lumbar preganglionic axons regenerated during the post-operative period, although this only affected a minority of sympathetic neurons. These reinnervated sympathetic neurons were not associated with VIP fibers, suggesting that the new intrinsic connections may have precluded regeneration or targeting of preganglionic axons. Together these results demonstrate that there is considerable remodelling within pelvic ganglia after partial deafferentation. This occurs under conditions where spinal preganglionic axons can regenerate. New intra-ganglionic connectivity may be permanent and may impact on this regeneration.