Proximal colon distention increases Fos expression in the lumbosacral spinal cord and activates sacral parasympathetic NADPHd-positive neurons in rats

Fos expression induced by nociceptive mechanical distention of the proximal colon was examined in the lumbosacral spinal cord in freely moving rats equipped with a chronic balloon in the proximal colon. Fos protein in lumbosacral neurons was detected immunocytochemically, and colocalization with nicotinamide adenine dinucleotide phosphate diaphorase (NADPHd) activity was determined histochemically at 1 hour after distention. Distention of the proximal colon (10 ml, 30 seconds on/off for 10 minutes, about 90 mm Hg) increased the number of Fos‐positive cells in the lumbar 6 (L6) and sacral 1 and 2 (S1, S2) segments, whereas no change was observed in the L1–L5 and S3 segments compared with the sham distended group or with animals that received no treatment. In L6–S2 segments, Fos‐positive neurons were increased by two‐fold in laminae I‐VII (mainly in laminae I and outer II) and area X (surrounding the central canal) and by nine‐fold in the sacral parasympathetic nucleus. Results of time course studies indicate that the maximal increase in Fos expression observed at 1 hour after distention returns to basal levels within 4 hours. In the S1 segment, distention of the proximal colon increased the percentage of NADPHd/Fos‐positive neurons selectively in the parasympathetic nucleus by 40% compared with less than 4% in the sham distention group; the number and pattern of NADPHd‐stained cells were not modified. These results indicate that noxious distention of the proximal colon for a short duration in awake rats selectively activates neurons in the L6‐S2 segments of the dorsal horn mainly in laminae involved in nociceptive and autonomic processing. The marked activation of NADPHd‐positive neurons in the sacral parasympathetic nucleus suggests a possible role of nitric oxide in the visceroautonomic reflexes induced by distention of the proximal colon. J. Comp. Neurol. 390:311–321, 1998. © 1998 Wiley‐Liss, Inc.