Genesis of anxiety, depression, and ongoing abdominal discomfort in ulcerative colitis-like colon inflammation

  • Chen J
  • Winston J
  • Fu Y
 et al. 
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Abstract

Background and aims: Psychological disorders are prevalent in patients with inflammatory bowel disease; the underlying mechanisms remain unknown. We tested the hypothesis that ulcerative colitis-like inflammation induced by dextran sodium sulfate (DSS) exacerbates the ongoing spontaneous activity in colon-projecting afferent neurons that induces abdominal discomfort and anxiety- and depressive-like behaviors in rats. Methods: We used the conditioned place preference and standard tests for anxiety- and depressive-like behaviors. Results: DSS-rats developed anxiety- and depressive-like behaviors 10 to 20 days after the start of inflammation. Single fiber recordings showed increase in the frequency of spontaneous activity in L6-S1 DRG roots. Prolonged desensitization of TRPV1 expressing colonic afferents by resiniferatoxin (RTX) suppressed the spontaneous activity as well as the anxiety- and depressive-like behaviors. Reduction in spontaneous activity in colon afferents by intra-colonic administration of lidocaine produced robust conditioned place preference (CPP) in DSS- rats, but not in control rats. Patch clamp studies demonstrated a significant decrease in the resting membrane potential, lower rheobase and the sensitization of colon-projecting L6-S1 DRG neurons to generate trains of action potentials in response to current injection in DSS rats. DSS inflammation upregulated the mRNA levels of TRPA1 and TRPV1 channels and downregulated that of Kv1.1 and Kv1.4 channels. Conclusions: Ulcerative colitis-like inflammation in rats induces anxiety- and depressive-like behaviors as well as ongoing abdominal discomfort by exacerbating the spontaneous activity in the colon-projecting afferent neurons. Alterations in the expression of voltage- and ligand-gated channels are associated with the induction of mood disorders following colon inflammation.

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Authors

  • J. Chen

  • J. H. Winston

  • Y. Fu

  • J. Guptarak

  • K. L. Jensen

  • X.-Z. Shi

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