Excessive Astrocytic GABA Causes Cortical Hypometabolism and Impedes Functional Recovery after Subcortical Stroke

Cell Rep. 2020 Jul 7;32(1):107861. doi: 10.1016/j.celrep.2020.107861.

Abstract

Glucose hypometabolism in cortical structures after functional disconnection is frequently reported in patients with white matter diseases such as subcortical stroke. However, the molecular and cellular mechanisms have been poorly elucidated. Here we show, in an animal model of internal capsular infarct, that GABA-synthesizing reactive astrocytes in distant cortical areas cause glucose hypometabolism via tonic inhibition of neighboring neurons. We find that reversal of aberrant astrocytic GABA synthesis, by pharmacological inhibition and astrocyte-specific gene silencing of MAO-B, reverses the reduction in cortical glucose metabolism. Moreover, induction of aberrant astrocytic GABA synthesis by cortical injection of putrescine or adenovirus recapitulates cortical hypometabolism. Furthermore, MAO-B inhibition causes a remarkable recovery from post-stroke motor deficits when combined with a rehabilitation regimen. Collectively, our data indicate that cortical glucose hypometabolism in subcortical stroke is caused by aberrant astrocytic GABA and MAO-B inhibition and that attenuating cortical hypometabolism can be a therapeutic approach in subcortical stroke.

Keywords: GABA; PET imaging; astrocyte; diaschisis; internal capsule; monoamine oxidase B; reactive astrocyte; rehabilitation; stroke.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism*
  • Astrocytes / pathology
  • Cerebral Cortex / metabolism*
  • Cerebral Cortex / physiopathology*
  • Cerebral Cortex / ultrastructure
  • Glucose / metabolism
  • Male
  • Models, Biological
  • Monoamine Oxidase / metabolism
  • Monoamine Oxidase Inhibitors / pharmacology
  • Motor Activity / drug effects
  • Pyramidal Cells / metabolism
  • Rats, Sprague-Dawley
  • Recovery of Function* / drug effects
  • Stroke / metabolism*
  • Stroke / physiopathology*
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Monoamine Oxidase Inhibitors
  • gamma-Aminobutyric Acid
  • Monoamine Oxidase
  • Glucose