Hippocampal NR2B-containing NMDA receptors enhance long-term potentiation in rats with chronic visceral pain

Brain Res. 2014 Jun 27:1570:43-53. doi: 10.1016/j.brainres.2014.05.001. Epub 2014 May 10.

Abstract

Pain and learning memory have striking similarities in synaptic plasticity. Activation of the N-methyl-D-aspartic acid receptors 2B subunits (NR2B-NMDAs) is responsible for the hippocampal LTP in memory formation. In our previous studies, we found the significant enhancement of CA1 hippocampal long-term potentiation (LTP) induced by high-frequency stimulation (HFS) in rats with chronic visceral pain. However, it is unclear whether the NR2B-NMDAs are required for the LTP in chronic visceral pain. In this study, a rat model with irritable bowel syndrome (IBS) was established by colorectal distention (CRD). The sensitivity of visceral pain and HFS-induced LTP at SC-CA1 synapses were significantly enhanced in IBS-like rats (p<0.05). In addition, hippocampal NR2B protein levels significantly increased in IBS-like rats (p<0.05). To test whether NR2B-NMDAs are responsible for the LTP, effects of Ro 25-6981, a selective antagonist of NR2B-NMDAs, on field potential in CA1 region were investigated in vitro. Our results demonstrated that Ro 25-6981 dose-dependently inhibited the facilitation of CA1 LTP in IBS-like rats. The plausible activation mechanism of hippocampal NR2B-NMDAs in the LTP enhancement was further explored. Western blot data indicated that expression of tyrosine phosphorylated NR2B protein in hippocampus significantly enhanced in IBS-like rats. Accordingly, genistein, a specific inhibitor of tyrosine kinases, dose-dependently blocked the facilitation of hippocampal LTP in IBS-like rats. Furthermore, EMG data revealed that intra-hippocampal injection of Ro 25-6981 dose-dependently attenuated the visceral hypersensitivity. In conclusion, hippocampal NR2B-NMDAs are responsible for the facilitation of CA1 LTP via tyrosine phosphorylation, which leads to visceral hypersensitivity.

Keywords: Chronic visceral pain; Hippocampus; Irritable bowel syndrome; Long-term potentiation; N-methyl-d-aspartic acid receptor 2B subunit; Tyrosine kinase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CA1 Region, Hippocampal / drug effects
  • CA1 Region, Hippocampal / physiopathology
  • Chronic Pain / drug therapy
  • Chronic Pain / physiopathology*
  • Disease Models, Animal
  • Excitatory Amino Acid Antagonists / pharmacology
  • Genistein / pharmacology
  • Hippocampus / drug effects
  • Hippocampus / physiopathology*
  • Hyperalgesia / drug therapy
  • Hyperalgesia / physiopathology
  • Irritable Bowel Syndrome / drug therapy
  • Irritable Bowel Syndrome / physiopathology*
  • Long-Term Potentiation / drug effects
  • Long-Term Potentiation / physiology*
  • Male
  • Phenols / pharmacology
  • Piperidines / pharmacology
  • Protein Kinase Inhibitors / pharmacology
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Protein-Tyrosine Kinases / metabolism
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Synapses / drug effects
  • Synapses / physiology
  • Visceral Pain / drug therapy
  • Visceral Pain / physiopathology*

Substances

  • Excitatory Amino Acid Antagonists
  • NR2B NMDA receptor
  • Phenols
  • Piperidines
  • Protein Kinase Inhibitors
  • Receptors, N-Methyl-D-Aspartate
  • Ro 25-6981
  • Genistein
  • Protein-Tyrosine Kinases