Astrocytes Modulate a Specific Paraventricular Thalamus→Prefrontal Cortex Projection to Enhance Consciousness Recovery from Anesthesia

J Neurosci. 2024 Aug 21;44(34):e1808232024. doi: 10.1523/JNEUROSCI.1808-23.2024.

Abstract

Current anesthetic theory is mostly based on neurons and/or neuronal circuits. A role for astrocytes also has been shown in promoting recovery from volatile anesthesia, while the exact modulatory mechanism and/or the molecular target in astrocytes is still unknown. In this study by animal models in male mice and electrophysiological recordings in vivo and in vitro, we found that activating astrocytes of the paraventricular thalamus (PVT) and/or knocking down PVT astrocytic Kir4.1 promoted the consciousness recovery from sevoflurane anesthesia. Single-cell RNA sequencing of the PVT reveals two distinct cellular subtypes of glutamatergic neurons: PVT GRM and PVT ChAT neurons. Patch-clamp recording results proved astrocytic Kir4.1-mediated modulation of sevoflurane on the PVT mainly worked on PVT ChAT neurons, which projected mainly to the mPFC. In summary, our findings support the novel conception that there is a specific PVT→prefrontal cortex projection involved in consciousness recovery from sevoflurane anesthesia, which is mediated by the inhibition of sevoflurane on PVT astrocytic Kir4.1 conductance.

Keywords: Kir41 channel; anesthesia; astrocyte; consciousness; paraventricular thalamus.

MeSH terms

  • Anesthesia Recovery Period
  • Anesthetics, Inhalation / pharmacology
  • Animals
  • Astrocytes* / drug effects
  • Astrocytes* / metabolism
  • Astrocytes* / physiology
  • Consciousness* / drug effects
  • Consciousness* / physiology
  • Frontal Lobe / drug effects
  • Frontal Lobe / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Midline Thalamic Nuclei* / cytology
  • Midline Thalamic Nuclei* / drug effects
  • Midline Thalamic Nuclei* / physiology
  • Neural Pathways / drug effects
  • Neural Pathways / physiology
  • Neurons / drug effects
  • Neurons / physiology
  • Potassium Channels, Inwardly Rectifying* / metabolism
  • Prefrontal Cortex / drug effects
  • Prefrontal Cortex / physiology
  • Sevoflurane* / pharmacology

Substances

  • Sevoflurane
  • Potassium Channels, Inwardly Rectifying
  • Kcnj10 (channel)
  • Anesthetics, Inhalation