Vagotomy attenuates brain cytokines and sleep induced by peripherally administered tumor necrosis factor-α and lipopolysaccharide in mice

Sleep. 2013 Aug 1;36(8):1227-38, 1238A. doi: 10.5665/sleep.2892.

Abstract

Study objective: Systemic tumor necrosis factor-α (TNF-α) is linked to sleep and sleep altering pathologies in humans. Evidence from animals indicates that systemic and brain TNF-α have a role in regulating sleep. In animals, TNF-α or lipopolysaccharide (LPS) enhance brain pro-inflammatory cytokine expression and sleep after central or peripheral administration. Vagotomy blocks enhanced sleep induced by systemic TNF-α and LPS in rats, suggesting that vagal afferent stimulation by TNF-α enhances pro-inflammatory cytokines in sleep-related brain areas. However, the effects of systemic TNF-α on brain cytokine expression and mouse sleep remain unknown.

Design: We investigated the role of vagal afferents on brain cytokines and sleep after systemically applied TNF-α or LPS in mice.

Measurements and results: Spontaneous sleep was similar in vagotomized and sham-operated controls. Vagotomy attenuated TNF-α- and LPS-enhanced non-rapid eye movement sleep (NREMS); these effects were more evident after lower doses of these substances. Vagotomy did not affect rapid eye movement sleep responses to these substances. NREMS electroencephalogram delta power (0.5-4 Hz range) was suppressed after peripheral TNF-α or LPS injections, although vagotomy did not affect these responses. Compared to sham-operated controls, vagotomy did not affect liver cytokines. However, vagotomy attenuated interleukin-1 beta (IL-1β) and TNF-α mRNA brain levels after TNF-α, but not after LPS, compared to the sham-operated controls.

Conclusions: We conclude that vagal afferents mediate peripheral TNF-α-induced brain TNF-α and IL-1β mRNA expressions to affect sleep. We also conclude that vagal afferents alter sleep induced by peripheral pro-inflammatory stimuli in mice similar to those occurring in other species.

Keywords: EEG; Vagotomy; interleukin-1β; lipopolysaccharide; mouse; sleep; tumor necrosis factor-α; vagal afferents.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain Chemistry / drug effects
  • Brain Chemistry / physiology*
  • Cytokines / analysis*
  • Cytokines / physiology
  • Dose-Response Relationship, Drug
  • Gene Expression / drug effects
  • Gene Expression / physiology
  • Lipopolysaccharides / pharmacology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Polysomnography
  • Sleep / drug effects*
  • Sleep / physiology
  • Sleep Stages / drug effects
  • Sleep Stages / physiology
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Tumor Necrosis Factor-alpha / physiology
  • Vagotomy* / methods
  • Vagus Nerve / physiology

Substances

  • Cytokines
  • Lipopolysaccharides
  • Tumor Necrosis Factor-alpha