Genetic background modulates impaired excitability of inhibitory neurons in a mouse model of Dravet syndrome

Neurobiol Dis. 2015 Jan:73:106-17. doi: 10.1016/j.nbd.2014.09.017. Epub 2014 Oct 2.

Abstract

Dominant loss-of-function mutations in voltage-gated sodium channel NaV1.1 cause Dravet Syndrome, an intractable childhood-onset epilepsy. NaV1.1(+/-) Dravet Syndrome mice in C57BL/6 genetic background exhibit severe seizures, cognitive and social impairments, and premature death. Here we show that Dravet Syndrome mice in pure 129/SvJ genetic background have many fewer seizures and much less premature death than in pure C57BL/6 background. These mice also have a higher threshold for thermally induced seizures, fewer myoclonic seizures, and no cognitive impairment, similar to patients with Genetic Epilepsy with Febrile Seizures Plus. Consistent with this mild phenotype, mutation of NaV1.1 channels has much less physiological effect on neuronal excitability in 129/SvJ mice. In hippocampal slices, the excitability of CA1 Stratum Oriens interneurons is selectively impaired, while the excitability of CA1 pyramidal cells is unaffected. NaV1.1 haploinsufficiency results in increased rheobase and threshold for action potential firing and impaired ability to sustain high-frequency firing. Moreover, deletion of NaV1.1 markedly reduces the amplification and integration of synaptic events, further contributing to reduced excitability of interneurons. Excitability is less impaired in inhibitory neurons of Dravet Syndrome mice in 129/SvJ genetic background. Because specific deletion of NaV1.1 in forebrain GABAergic interneuons is sufficient to cause the symptoms of Dravet Syndrome in mice, our results support the conclusion that the milder phenotype in 129/SvJ mice is caused by lesser impairment of sodium channel function and electrical excitability in their forebrain interneurons. This mild impairment of excitability of interneurons leads to a milder disease phenotype in 129/SvJ mice, similar to Genetic Epilepsy with Febrile Seizures Plus in humans.

Keywords: Action potential threshold; Dravet Syndrome; Epilepsy; Excitatory post synaptic potential amplification; Interneuron; Na(V)1.1; Sodium channels.

Publication types

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

MeSH terms

  • Action Potentials / genetics
  • Animals
  • Animals, Newborn
  • Biophysical Phenomena / genetics
  • Conditioning, Psychological / physiology
  • Disease Models, Animal
  • Epilepsies, Myoclonic / etiology
  • Epilepsies, Myoclonic / genetics*
  • Epilepsies, Myoclonic / pathology*
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / genetics
  • Fear / psychology
  • Hippocampus / cytology
  • Hyperthermia, Induced / adverse effects
  • In Vitro Techniques
  • Lidocaine / analogs & derivatives
  • Lidocaine / pharmacology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mutation / genetics*
  • NAV1.1 Voltage-Gated Sodium Channel / genetics*
  • Neural Inhibition / genetics*
  • Neural Inhibition / physiology
  • Sodium Channel Blockers / pharmacology

Substances

  • NAV1.1 Voltage-Gated Sodium Channel
  • Scn1a protein, mouse
  • Sodium Channel Blockers
  • QX-314
  • Lidocaine