CaV3.1 isoform of T-type calcium channels supports excitability of rat and mouse ventral tegmental area neurons

Neuropharmacology. 2018 Jun:135:343-354. doi: 10.1016/j.neuropharm.2018.03.028. Epub 2018 Mar 23.

Abstract

Recent data have implicated voltage-gated calcium channels in the regulation of the excitability of neurons within the mesolimbic reward system. While the attention of most research has centered on high voltage L-type calcium channel activity, the presence and role of the low voltage-gated T-type calcium channel (T-channels) has not been well explored. Hence, we investigated T-channel properties in the neurons of the ventral tegmental area (VTA) utilizing wild-type (WT) rats and mice, CaV3.1 knock-out (KO) mice, and TH-eGFP knock-in (KI) rats in acute horizontal brain slices of adolescent animals. In voltage-clamp experiments, we first assessed T-channel activity in WT rats with characteristic properties of voltage-dependent activation and inactivation, as well as characteristic crisscrossing patterns of macroscopic current kinetics. T-current kinetics were similar in WT mice and WT rats but T-currents were abolished in CaV3.1 KO mice. In ensuing current-clamp experiments, we observed the presence of hyperpolarization-induced rebound burst firing in a subset of neurons in WT rats, as well as dopaminergic and non-dopaminergic neurons in TH-eGFP KI rats. Following the application of a pan-selective T-channel blocker TTA-P2, rebound bursting was significantly inhibited in all tested cells. In a behavioral assessment, the acute locomotor increase induced by a MK-801 (Dizocilpine) injection in WT mice was abolished in CaV3.1 KO mice, suggesting a tangible role for 3.1 T-type channels in drug response. We conclude that pharmacological targeting of CaV3.1 isoform of T-channels may be a novel approach for the treatment of disorders of mesolimbic reward system.

Keywords: Burst firing; Dopamine; Low-voltage-activated; Rebound spiking; T-type calcium channel; TTA-P2; Ventral tegmental area.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, T-Type / genetics
  • Calcium Channels, T-Type / metabolism*
  • Dizocilpine Maleate / pharmacology
  • Dopamine / metabolism
  • Excitatory Amino Acid Antagonists / pharmacology
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Motor Activity / drug effects
  • Motor Activity / physiology
  • Neurons / drug effects
  • Neurons / metabolism*
  • Rats, Sprague-Dawley
  • Rats, Transgenic
  • Tissue Culture Techniques
  • Ventral Tegmental Area / drug effects
  • Ventral Tegmental Area / metabolism*

Substances

  • Cacna1g protein, mouse
  • Cacna1g protein, rat
  • Calcium Channel Blockers
  • Calcium Channels, T-Type
  • Excitatory Amino Acid Antagonists
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Dizocilpine Maleate
  • Dopamine