Serotonin neurons in the dorsal raphe mediate the anticataplectic action of orexin neurons by reducing amygdala activity

Proc Natl Acad Sci U S A. 2017 Apr 25;114(17):E3526-E3535. doi: 10.1073/pnas.1614552114. Epub 2017 Apr 10.

Abstract

Narcolepsy is a sleep disorder caused by the loss of orexin (hypocretin)-producing neurons and marked by excessive daytime sleepiness and a sudden weakening of muscle tone, or cataplexy, often triggered by strong emotions. In a mouse model for narcolepsy, we previously demonstrated that serotonin neurons of the dorsal raphe nucleus (DRN) mediate the suppression of cataplexy-like episodes (CLEs) by orexin neurons. Using an optogenetic tool, in this paper we show that the acute activation of DRN serotonin neuron terminals in the amygdala, but not in nuclei involved in regulating rapid eye-movement sleep and atonia, suppressed CLEs. Not only did stimulating serotonin nerve terminals reduce amygdala activity, but the chemogenetic inhibition of the amygdala using designer receptors exclusively activated by designer drugs also drastically decreased CLEs, whereas chemogenetic activation increased them. Moreover, the optogenetic inhibition of serotonin nerve terminals in the amygdala blocked the anticataplectic effects of orexin signaling in DRN serotonin neurons. Taken together, the results suggest that DRN serotonin neurons, as a downstream target of orexin neurons, inhibit cataplexy by reducing the activity of amygdala as a center for emotional processing.

Keywords: amygdala; narcolepsy; orexin; serotonin; sleep.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala* / metabolism
  • Amygdala* / pathology
  • Amygdala* / physiopathology
  • Animals
  • Catalepsy* / genetics
  • Catalepsy* / metabolism
  • Catalepsy* / pathology
  • Catalepsy* / physiopathology
  • Dorsal Raphe Nucleus* / metabolism
  • Dorsal Raphe Nucleus* / pathology
  • Dorsal Raphe Nucleus* / physiopathology
  • Eye Movements
  • Male
  • Mice
  • Mice, Knockout
  • Serotonergic Neurons / metabolism*
  • Serotonergic Neurons / pathology
  • Serotonin / metabolism
  • Signal Transduction*

Substances

  • Serotonin