GIRK1-Mediated Inwardly Rectifying Potassium Current Is a Candidate Mechanism Behind Purkinje Cell Excitability, Plasticity, and Neuromodulation

Cerebellum. 2020 Dec;19(6):751-761. doi: 10.1007/s12311-020-01158-y.

Abstract

G-protein-coupled inwardly rectifying potassium (GIRK) channels contribute to the resting membrane potential of many neurons and play an important role in controlling neuronal excitability. Although previous studies have revealed a high expression of GIRK subunits in the cerebellum, their functional role has never been clearly described. Using patch-clamp recordings in mice cerebellar slices, we examined the properties of the GIRK currents in Purkinje cells (PCs) and investigated the effects of a selective agonist of GIRK1-containing channels, ML297 (ML), on PC firing and synaptic plasticity. We demonstrated that GIRK channel activation decreases the PC excitability by inhibiting both sodium and calcium spikes and, in addition, modulates the complex spike response evoked by climbing fiber stimulation. Our results indicate that GIRK channels have also a marked effect on synaptic plasticity of the parallel fiber-PC synapse, as the application of ML297 increased the expression of LTP while preventing LTD. We, therefore, propose that the recruitment of GIRK channels represents a crucial mechanism by which neuromodulators can control synaptic strength and membrane conductance for proper refinement of the neural network involved in memory storage and higher cognitive functions.

Keywords: Cerebellum; GIRK; Neuromodulation; Purkinje cell; Synaptic plasticity.

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Animals, Newborn
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology*
  • Female
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / agonists
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels / physiology*
  • Male
  • Mice
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Neurotransmitter Agents / pharmacology*
  • Phenylurea Compounds / pharmacology
  • Purkinje Cells / drug effects
  • Purkinje Cells / physiology*
  • Pyrazoles / pharmacology

Substances

  • CID 56642816
  • G Protein-Coupled Inwardly-Rectifying Potassium Channels
  • Neurotransmitter Agents
  • Phenylurea Compounds
  • Pyrazoles