Novel neurosteroid hypnotic blocks T-type calcium channel-dependent rebound burst firing and suppresses long-term potentiation in the rat subiculum

Br J Anaesth. 2019 May;122(5):643-651. doi: 10.1016/j.bja.2019.01.029. Epub 2019 Feb 28.

Abstract

Background: Hypnotics and general anaesthetics impair memory by altering hippocampal synaptic plasticity. We recently reported on a neurosteroid analogue with potent hypnotic activity [(3β,5β,17β)-3-hydroxyandrostane-17-carbonitrile; 3β-OH], which does not cause developmental neurotoxicity in rat pups. Here, we investigated the effects of 3β-OH on neuronal excitability in the subiculum, the major output structure of the hippocampal formation, and synaptic plasticity at two key hippocampal synapses in juvenile rats.

Methods: Biophysical properties of isolated T-type calcium currents (T-currents) in the rat subiculum were investigated using acute slice preparations. Subicular T-type calcium channel (T-channel) subtype mRNA expression was compared using qRT-PCR. Using electrophysiological recordings, we examined the effects of 3β-OH and an endogenous neuroactive steroid, allopregnanolone (Allo), on T-currents and burst firing properties of subicular neurones, and on the long-term potentiation (LTP) in CA3-CA1 and CA1-subiculum pathways.

Results: Biophysical and molecular studies confirmed that CaV3.1 channels represent the dominant T-channel isoform in the subiculum of juvenile rats. 3β-OH and Allo inhibited rebound burst firing by decreasing the amplitude of T-currents in a voltage-dependent manner with similar potency, with 30-80% inhibition. Both neurosteroids suppressed LTP at the CA1-subiculum, but not at the CA3-CA1 Schaffer collateral synapse.

Conclusions: Neurosteroid effects on T-channels modulate hippocampal output and provide possible molecular mechanisms for the amnestic action of the novel hypnotic 3β-OH. Effects on T-channels in the subiculum provide a novel target for amnestic effects of hypnotics.

Keywords: T-type calcium channels; amnesia; general anaesthetic; hippocampus; neurosteroid; subiculum; synaptic plasticity.

MeSH terms

  • Androstanols / pharmacology*
  • Animals
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, T-Type / biosynthesis
  • Calcium Channels, T-Type / drug effects*
  • Calcium Channels, T-Type / genetics
  • Female
  • Gene Expression Regulation / drug effects
  • Hippocampus / drug effects*
  • Hippocampus / physiology
  • Hypnotics and Sedatives / pharmacology*
  • Long-Term Potentiation / drug effects*
  • Long-Term Potentiation / physiology
  • Male
  • Neuronal Plasticity / drug effects*
  • Nitriles / pharmacology*
  • RNA, Messenger / genetics
  • Rats, Sprague-Dawley

Substances

  • 3-hydroxyandrostane-17-carbonitrile
  • Androstanols
  • Calcium Channel Blockers
  • Calcium Channels, T-Type
  • Hypnotics and Sedatives
  • Nitriles
  • RNA, Messenger