Autism-Associated Shank3 Is Essential for Homeostatic Compensation in Rodent V1

Neuron. 2020 Jun 3;106(5):769-777.e4. doi: 10.1016/j.neuron.2020.02.033. Epub 2020 Mar 20.

Abstract

Mutations in Shank3 are strongly associated with autism spectrum disorders and neural circuit changes in several brain areas, but the cellular mechanisms that underlie these defects are not understood. Homeostatic forms of plasticity allow central circuits to maintain stable function during experience-dependent development, leading us to ask whether loss of Shank3 might impair homeostatic plasticity and circuit-level compensation to perturbations. We found that Shank3 loss in vitro abolished synaptic scaling and intrinsic homeostatic plasticity, deficits that could be rescued by treatment with lithium. Further, Shank3 knockout severely compromised the in vivo ability of visual cortical circuits to recover from perturbations to sensory drive. Finally, lithium treatment ameliorated a repetitive self-grooming phenotype in Shank3 knockout mice. These findings demonstrate that Shank3 loss severely impairs the ability of central circuits to harness homeostatic mechanisms to compensate for perturbations in drive, which, in turn, may render them more vulnerable to such perturbations.

Keywords: ASD; GSK3; Shank3; homeostatic plasticity; intrinsic homeostatic plasticity; lithium; synaptic scaling; visual cortex.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antimanic Agents / pharmacology
  • Autistic Disorder / genetics
  • Behavior, Animal / drug effects
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / genetics
  • Gene Knockdown Techniques
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Grooming / drug effects
  • Homeostasis / drug effects
  • Homeostasis / genetics*
  • Lithium Compounds / pharmacology
  • Mice
  • Mice, Knockout
  • Microfilament Proteins
  • Nerve Tissue Proteins / drug effects
  • Nerve Tissue Proteins / genetics*
  • Neural Pathways
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / genetics*
  • Neurons / drug effects*
  • Neurons / metabolism
  • Rats
  • Sodium Channel Blockers / pharmacology
  • Tetrodotoxin / pharmacology
  • Visual Cortex / cytology
  • Visual Cortex / drug effects*
  • Visual Cortex / metabolism

Substances

  • Antimanic Agents
  • Lithium Compounds
  • Microfilament Proteins
  • Nerve Tissue Proteins
  • Shank3 protein, mouse
  • Shank3 protein, rat
  • Sodium Channel Blockers
  • Tetrodotoxin
  • Glycogen Synthase Kinase 3