Vagal nerve stimulation blocks interleukin 6-dependent synaptic hyperexcitability induced by lipopolysaccharide-induced acute stress in the rodent prefrontal cortex

Brain Behav Immun. 2015 Jan:43:149-58. doi: 10.1016/j.bbi.2014.07.020. Epub 2014 Aug 13.

Abstract

The ratio between synaptic inhibition and excitation (sI/E) is a critical factor in the pathophysiology of neuropsychiatric disease. We recently described a stress-induced interleukin-6 dependent mechanism leading to a decrease in sI/E in the rodent temporal cortex. The aim of the present study was to determine whether a similar mechanism takes place in the prefrontal cortex, and to elaborate strategies to prevent or attenuate it. We used aseptic inflammation (single acute injections of lipopolysaccharide, LPS, 10mg/kg) as stress model, and patch-clamp recording on a prefrontal cortical slice preparation from wild-type rat and mice, as well as from transgenic mice in which the inhibitor of IL-6 trans-signaling sgp130Fc was produced in a brain-specific fashion (sgp130Fc mice). The anti-inflammatory reflex was activated either by vagal nerve stimulation or peripheral administration of the nicotinic α7 receptor agonist PHA543613. We found that the IL-6-dependent reduction in prefrontal cortex synaptic inhibition was blocked in sgp130Fc mice, or - in wild-type animals - upon application sgp130Fc. Similar results were obtained by activating the "anti-inflammatory reflex" - a neural circuit regulating peripheral immune response - by stimulation of the vagal nerve or through peripheral administration of the α7 nicotinic receptor agonist PHA543613. Our results indicate that the prefrontal cortex is an important potential target of IL-6 mediated trans-signaling, and suggest a potential new avenue in the treatment of a large class of hyperexcitable neuropsychiatric conditions, including epilepsy, schizophrenic psychoses, anxiety disorders, autism spectrum disorders, and depression.

Keywords: Anti-inflammatory reflex; GABA; Interleukin 6; Lipopolysaccharide; Vagal nerve stimulation.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Inflammation / metabolism
  • Inflammation / physiopathology
  • Interleukin-6 / metabolism*
  • Lipopolysaccharides / pharmacology*
  • Mice
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology
  • Prefrontal Cortex / drug effects
  • Prefrontal Cortex / metabolism
  • Prefrontal Cortex / physiopathology*
  • Rats
  • Rats, Sprague-Dawley
  • Stress, Physiological / drug effects
  • Stress, Physiological / physiology*
  • Synapses / metabolism
  • Synapses / physiology*
  • Vagus Nerve Stimulation*

Substances

  • Interleukin-6
  • Lipopolysaccharides