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Am J Physiol Regul Integr Comp Physiol ; 308(1): R18-27, 2015 Jan 01.
Article in English | MEDLINE | ID: mdl-25411361

ABSTRACT

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. In this study, we used the conditioned place preference and standard tests for anxiety- and depression-like behaviors. DSS rats developed anxiety- and depression-like behaviors 10 to 20 days after the start of inflammation. Single-fiber recordings showed an increase in the frequency of spontaneous activity in L6-S1 dorsal root ganglion (DRG) roots. Prolonged desensitization of transient receptor potential vanilloid 1 (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 intracolonic 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 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 transient receptor potential ankyrin 1 and TRPV1 channels and downregulated that of Kv1.1 and Kv1.4 channels. Ulcerative colitis-like inflammation in rats induces anxiety- and depression-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.


Subject(s)
Abdominal Pain/etiology , Anxiety/etiology , Behavior, Animal , Colitis, Ulcerative/complications , Colon/innervation , Depression/etiology , Abdominal Pain/drug therapy , Abdominal Pain/metabolism , Abdominal Pain/physiopathology , Abdominal Pain/psychology , Action Potentials , Anesthetics, Local/pharmacology , Animals , Anxiety/metabolism , Anxiety/physiopathology , Anxiety/prevention & control , Anxiety/psychology , Colitis, Ulcerative/chemically induced , Colitis, Ulcerative/drug therapy , Colitis, Ulcerative/metabolism , Colitis, Ulcerative/physiopathology , Colitis, Ulcerative/psychology , Conditioning, Psychological , Depression/metabolism , Depression/physiopathology , Depression/prevention & control , Depression/psychology , Dextran Sulfate , Disease Models, Animal , Diterpenes/pharmacology , Ganglia, Spinal/drug effects , Ganglia, Spinal/metabolism , Ganglia, Spinal/physiopathology , Kv1.1 Potassium Channel/genetics , Kv1.1 Potassium Channel/metabolism , Kv1.4 Potassium Channel/genetics , Kv1.4 Potassium Channel/metabolism , Lidocaine/pharmacology , RNA, Messenger/metabolism , Rats , TRPV Cation Channels/agonists , TRPV Cation Channels/genetics , TRPV Cation Channels/metabolism , Time Factors
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