Sleep Homeostatic and Waking Behavioral Phenotypes in Egr3-Deficient Mice Associated with Serotonin Receptor 5-HT2 Deficits

Sleep. 2016 Dec 1;39(12):2189-2199. doi: 10.5665/sleep.6324.

Abstract

Study objective: The expression of the immediate early gene early growth response 3 (Egr3) is a functional marker of brain activity including responses to novelty, sustained wakefulness, and sleep. We examined the role of this gene in regulating wakefulness and sleep.

Methods: Electroencephalogram/electromyogram (EEG/EMG) were recorded in Egr3-/- and wild-type (WT) mice during 24 h baseline, 6 h sleep disruption and 6 h recovery. Serotonergic signaling was assessed with 6 h EEG/EMG recordings after injections of nonselective 5-HT2 antagonist (clozapine), selective 5-HT2 antagonists (5-HT2A; MDL100907 and 5-HT2BC; SB206553) and a cocktail of both selective antagonists, administered in a randomized order to each animal.

Results: Egr3-/- mice did not exhibit abnormalities in the timing of wakefulness and slow wave sleep (SWS); however, EEG dynamics in SWS (suppressed 1-3 Hz power) and in quiet wakefulness (elevated 3-8 Hz and 15-35 Hz power) differed in comparison to WT-mice. Egr3-/- mice showed an exaggerated response to sleep disruption as measured by active wakefulness, but with a blunted increase in homeostatic sleep drive (elevated 1-4 Hz power) relative to WT-mice. Egr3-/-mice exhibit greatly reduced sedative effects of clozapine at the electroencephalographic level. In addition, clozapine induced a previously undescribed dissociated state (low amplitude, low frequency EEG and a stable, low muscle tone) lasting up to 2 h in WT-mice. Egr3-/- mice did not exhibit this phenomenon. Selective 5-HT2A antagonist, alone or in combination with selective 5-HT2BC antagonist, caused EEG slowing coincident with behavioral quiescence in WT-mice but not in Egr3-/- mice.

Conclusion: Egr3 has an essential role in regulating cortical arousal, wakefulness, and sleep, presumably by its regulation of 5-HT2 receptors.

Keywords: cortical arousal; early growth response; sedation; serotonin.

MeSH terms

  • Animals
  • Crosses, Genetic
  • Electroencephalography
  • Electromyography
  • Female
  • Homeostasis / drug effects
  • Homeostasis / genetics*
  • Homeostasis / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Phenotype*
  • Potassium Channels / genetics*
  • Receptors, Serotonin, 5-HT2 / genetics*
  • Receptors, Serotonin, 5-HT2 / physiology*
  • Serotonin Antagonists / pharmacology
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Sleep / genetics*
  • Sleep / physiology*
  • Sleep Deprivation / genetics*
  • Sleep Deprivation / physiopathology*
  • Wakefulness / genetics*
  • Wakefulness / physiology*

Substances

  • Erg3 protein, mouse
  • Potassium Channels
  • Receptors, Serotonin, 5-HT2
  • Serotonin Antagonists