Elsevier

Neuroscience

Volume 84, Issue 1, 3 February 1998, Pages 263-280
Neuroscience

Projections of pelvic autonomic neurons within the lower bowel of the male rat: an anterograde labelling study

https://doi.org/10.1016/S0306-4522(97)89502-4Get rights and content

Abstract

The tissues of the large intestine which receive an innervation by neurons of the major pelvic ganglia were identified following in vivo and in vitro anterograde labelling with the lipophilic tracer 1,1′didodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate in the male rat. The primary target in the gut of major pelvic ganglion neurons is the myenteric plexus of the distal colon and the rectum. The serosal ganglia, on the surface of the most distal region of the rectum and the circular muscle of the distal colon and rectum were less densely innervated. The pelvic ganglia do not innervate the longitudinal muscle, submucosal blood vessels, submucosal plexus, or mucosa. The pelvic supply reaches the bowel via two groups of rectal nerves and branches of the penile nerves. All of these connections also carry the axons of viscerofugal neurons from the bowel, some of which have terminal axons in the major pelvic ganglia. Finally, the different nerves supplied different targets. In particular, while the rectal nerves carried pelvic axons supplying the myenteric plexus, circular muscle, and serosal ganglia, the penile nerves only innervated the serosal ganglia. In addition, the two groups of rectal nerves innervated slightly different regions of the bowel and provided different projection patterns. However, successful in vivo labelling was achieved in only 6/12 animals and while all in vitro experiments resulted in successful labelling, it was clear that only a proportion of pelvic projections in any given nerve were labelled.

These studies have shown that the major pelvic ganglia are primarily involved in the control of motility, but not of vascular and secretomotor functions. Thus pelvic neurons do not innervate the same range of target tissues within the bowel as the prevertebral ganglia. This study has also shown that the different pathways to the gut from the major pelvic ganglia innervate different tissues, suggesting that the autonomic innervation of the gut is not homogeneous along its length.

Section snippets

Injection of DiI into the major pelvic ganglia in vivo

To gain an overview of the MPG projections to the gut via both the RN and PenN, DiI was injected into the MPG of 12 Advit male Wistar rats (106–245 g). Rats were anaesthetized with sodium pentobarbitone (48 mg/kg, i.p.), and the MPG were injected bilaterally with approximately 100–200 nl of DiI (diluted to 3–5% in ethanol) via a glass micropipette connected to a glass syringe filled with silicon oil, as described previously.[46]Two types of DiI were used [DiI(C12)3, n=9; DiI(C18)3, n=3; see

General features of DiI labelling

All fibres labelled anterogradely from injection of DiI into the MPG or from application of DiI onto the RN or PenN were confined to the middle and distal colon and rectum, with the majority of labelled structures occurring in the rectum. The primary target of MPG fibres within the gut was the mpx. A pelvic innervation of the serosal ganglia, and the circular muscle was also observed. Projections to the spx were rare and limited (1/9 animals had sparse spx labelling). An innervation of the

Discussion

These studies have provided the first description of the tissues targeted by rat MPG neurons in the lower bowel. They show that the majority of MPG projections innervate the mpx, although some supply the serosal ganglia and circular muscle. No other gut tissues are innervated by pelvic neurons. These results were produced by both in vivo and in vitro anterograde labelling of pelvic axons. The innervation of the mpx was primarily confined to the distal colon and rectum, with only a small

Conclusions

The present study has demonstrated that the major pelvic ganglia provide their primary innervation of the intestine to the myenteric plexus and are almost exclusively involved in the control of motility. These findings differentiate pelvic from prevertebral ganglia in two ways. First, unlike the pelvic ganglia, the prevertebral ganglia control secretory function and blood flow as well as motility. Second, while both ganglia control motility, the role of the pelvic ganglia is different due to

Acknowledgements

We wish to thank Mandy Bauer and Mark Kepper for their assistance with animal handling and tissue preparation, and Dr S. Brookes for teaching us the organotypic culturing method. This work was supported by the National Health and Medical Research Council of Australia.

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