Cross-Organ Sensitization of Lumbosacral Spinal Neurons Receiving Urinary Bladder Input in Rats With Inflamed Colon

Abstract

Clinical studies show that patients with irritable bowel syndrome and colonic diseases frequently experience sensory and motor dysfunctions of the urinary bladder. The aim of this study was to investigate the spinal neuronal mechanisms responsible for potential cross talk between these visceral organs. Colonic inflammation was induced by dextran sulfate sodium (5%) in drinking water for 7-12 days (n = 12); another group of rats without dextran sulfate sodium (n = 12) was used as control. Extracellular potentials of single L6 to S2 spinal neurons were recorded in pentobarbital-anesthetized and paralyzed rats with dextran sulfate sodium-induced colitis or normal colon. Urinary bladder distention (0.5-2.0 mL; 20 seconds) was produced with saline inflation, and colorectal distention was induced by inflation of an air balloon (80 mm Hg; 20 seconds). A total of 58 of 153 (38%) and 55 of 152 (36%) spinal neurons responded to urinary bladder distention in dextran sulfate sodium-treated and control animals, respectively. The mean background activity of neurons excited by urinary bladder distention in rats with dextran sulfate sodium-induced colitis was significantly higher than in the control group. The threshold volume for excitatory responses to urinary bladder distention in rats with inflamed colon (0.024 +/- 0.09 mL; n = 30) was significantly lower than for control rats (0.062 +/- 0.016 mL; n = 31; P < .05). The stimulus-response curves of excitatory responses to graded urinary bladder distention were significantly increased for both viscerovisceral (urinary bladder distention and colorectal distention) convergent neurons and urinary bladder distention-receptive neurons in rats with colitis compared with control animals. Acute colitis sensitized lumbosacral spinal neurons receiving input from the urinary bladder. Thus, spinal neuronal hyperexcitability may be involved in central cross-organ sensitization of visceral nociception between the colon and urinary bladder.