Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats

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Abstract
Many visceral afferent neurons contain peptides, which have been proposed as histochemical markers for nerve pathways of particular targets or as transmitter candidates. The former possibility was investigated in the present study. Primary afferent neurons which project to the urinary bladder, distal colon or penis of rats, and the colon of cats were labelled with retrogradely transported fluorescent dyes (Fast Blue, True Blue, or Fluoro Gold). One to six weeks after dye injection into the organs, lumbosacral dorsal root ganglia were removed, treated with colchicine, and processed for immunohistochemical identification of five peptides. Dye‐labelled neurons were distributed in an organ‐specific manner in the lower lumbosacral ganglia, where colon afferent neurons were almost exclusively found in S1 ganglia, penis neurons primarily in L6, and bladder neurons at both levels. Substance P‐ (SP), calcitonin gene‐related peptide‐(CGRP), vasoactive intestinal peptide‐ (VIP), enkephalin‐ (ENK), and somatostatin‐ (SOM) immunoreactivity (IR) were detected in neurons in all lumbosacral ganglia but only some of these peptides were present in a large percentage of labelled neurons. The numbers of peptide‐containing neurons innervating each organ were CGRP > SP > VIP > ENK > SOM; however some differences were observed in the relative proportions of these neuronal populations between upper lumbar and lower lumbosacral ganglia and between different organs. The major difference seen at the upper lumbar level was amongst the SP‐IR neurons, which were common (25–30%) amongst bladder and colon afferent neurons but absent in penis neurons. At the lower lumbar‐sacral level CGRP‐IR was present in a greater proportion (70%) of colon neurons than neurons which supplied the bladder (52%) or penis (35%). VIP‐IR was found in fewer (2–12%) neurons of each group. The afferent innervation of the cat colon exhibited a similar peptide distribution but with smaller numbers of CGRP‐IR neurons (45% vs. 70%) and larger numbers of VIP‐ (18% vs. 2%) and ENK‐IR (5% vs. 0–2%) neurons. SOM‐IR was rarely found in any dye‐labelled neurons and may therefore be more important in the sensory supply of other pelvic organs or of somatic organs. In summary, these studies have revealed that primary afferent neurons supplying the urogenital organs and colon of male rats differ in their segmental distribution and also exhibit some differences in the percentage of cells containing certain peptides (SP, CGRP, and VIP).

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