Increased Excitation-Inhibition Ratio Stabilizes Synapse and Circuit Excitability in Four Autism Mouse Models

Neuron. 2019 Feb 20;101(4):648-661.e4. doi: 10.1016/j.neuron.2018.12.026. Epub 2019 Jan 21.

Abstract

Distinct genetic forms of autism are hypothesized to share a common increase in excitation-inhibition (E-I) ratio in cerebral cortex, causing hyperexcitability and excess spiking. We provide a systematic test of this hypothesis across 4 mouse models (Fmr1-/y, Cntnap2-/-, 16p11.2del/+, Tsc2+/-), focusing on somatosensory cortex. All autism mutants showed reduced feedforward inhibition in layer 2/3 coupled with more modest, variable reduction in feedforward excitation, driving a common increase in E-I conductance ratio. Despite this, feedforward spiking, synaptic depolarization, and spontaneous spiking were largely normal. Modeling revealed that E and I conductance changes in each mutant were quantitatively matched to yield stable, not increased, synaptic depolarization for cells near spike threshold. Correspondingly, whisker-evoked spiking was not increased in vivo despite detectably reduced inhibition. Thus, elevated E-I ratio is a common circuit phenotype but appears to reflect homeostatic stabilization of synaptic drive rather than driving network hyperexcitability in autism.

Keywords: E-I ratio; Fragile X; autism; cerebral cortex; circuit excitability; excitation; homeostasis; inhibition; somatosensory cortex.

Publication types

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

MeSH terms

  • Animals
  • Autistic Disorder / genetics
  • Autistic Disorder / physiopathology*
  • Chromosomes, Human, Pair 16 / genetics
  • Evoked Potentials, Somatosensory*
  • Excitatory Postsynaptic Potentials*
  • Fragile X Mental Retardation Protein / genetics
  • Humans
  • Inhibitory Postsynaptic Potentials*
  • Male
  • Membrane Proteins / genetics
  • Mice
  • Mice, Inbred C57BL
  • Nerve Tissue Proteins / genetics
  • Somatosensory Cortex / physiology
  • Somatosensory Cortex / physiopathology*
  • Tuberous Sclerosis Complex 2 Protein / genetics

Substances

  • CNTNAP2 protein, mouse
  • Fmr1 protein, mouse
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Tsc2 protein, mouse
  • Tuberous Sclerosis Complex 2 Protein
  • Fragile X Mental Retardation Protein