Astrocytic metabolic control of orexinergic activity in the lateral hypothalamus regulates sleep and wake architecture

Nat Commun. 2024 Jul 16;15(1):5979. doi: 10.1038/s41467-024-50166-7.

Abstract

Neuronal activity undergoes significant changes during vigilance states, accompanied by an accommodation of energy demands. While the astrocyte-neuron lactate shuttle has shown that lactate is the primary energy substrate for sustaining neuronal activity in multiple brain regions, its role in regulating sleep/wake architecture is not fully understood. Here we investigated the involvement of astrocytic lactate supply in maintaining consolidated wakefulness by downregulating, in a cell-specific manner, the expression of monocarboxylate transporters (MCTs) in the lateral hypothalamus of transgenic mice. Our results demonstrate that reduced expression of MCT4 in astrocytes disrupts lactate supply to wake-promoting orexin neurons, impairing wakefulness stability. Additionally, we show that MCT2-mediated lactate uptake is necessary for maintaining tonic firing of orexin neurons and stabilizing wakefulness. Our findings provide both in vivo and in vitro evidence supporting the role of astrocyte-to-orexinergic neuron lactate shuttle in regulating proper sleep/wake stability.

MeSH terms

  • Animals
  • Astrocytes* / metabolism
  • Hypothalamic Area, Lateral* / metabolism
  • Hypothalamus / metabolism
  • Lactic Acid* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic*
  • Monocarboxylic Acid Transporters* / genetics
  • Monocarboxylic Acid Transporters* / metabolism
  • Muscle Proteins
  • Neurons* / metabolism
  • Orexins* / metabolism
  • Sleep* / physiology
  • Wakefulness* / physiology

Substances

  • Orexins
  • Monocarboxylic Acid Transporters
  • Lactic Acid
  • Slc16a4 protein, mouse
  • Muscle Proteins