Pharmacological modulation of the voltage-gated neuronal Kv7/KCNQ/M-channel alters the intrinsic excitability and synaptic responses of pyramidal neurons in rat prefrontal cortex slices

Acta Pharmacol Sin. 2017 Sep;38(9):1248-1256. doi: 10.1038/aps.2017.72. Epub 2017 Jun 12.

Abstract

The prefrontal cortex (PFC) critical for higher cognition is implicated in neuropsychiatric diseases, such as Alzheimer's disease, depression and schizophrenia. The voltage-activated Kv7/KCNQ/M-channel or M-current modulates the neuronal excitability that defines the fundamental mechanism of brain function. However, whether M-current functions to regulate the excitability of PFC neurons remains elusive. In this study, we recorded the native M-current from PFC layer V pyramidal neurons in rat brain slices and showed that it modulated the intrinsic excitability and synaptic responses of PFC pyramidal neurons. Application of a specific M-channel blocker XE991 (40 μmol/L) or opener retigabine (10 μmol/L) resulted in inhibition or activation of M-current, respectively. In the current-clamp recordings, inhibition of M-current was evidenced by the increased average spike frequency and the reduced first inter-spike interval (ISI), spike onset latency and fast afterhyperpolarization (fAHP), whereas activation of M-current caused opposite responses. Furthermore, inhibition of M-current significantly increased the amplitude of excitatory postsynaptic potentials (EPSPs) and depolarized the resting membrane potential (RMP) without affecting the miniature EPSC (mEPSC) frequency. These data demonstrate that voltage-gated neuronal Kv7/KCNQ/M-current modulates the excitability and synaptic transmission of PFC neurons, suggesting that pharmacological modulation of M-current in the PFC may exert beneficial effects on cognitive deficits implicated in the pathophysiology of neuropsychiatric disorders.

MeSH terms

  • Animals
  • Anthracenes / chemistry
  • Anthracenes / pharmacology*
  • Dose-Response Relationship, Drug
  • KCNQ Potassium Channels / antagonists & inhibitors*
  • KCNQ Potassium Channels / metabolism
  • Male
  • Potassium Channel Blockers / chemistry
  • Potassium Channel Blockers / pharmacology*
  • Prefrontal Cortex / drug effects*
  • Prefrontal Cortex / metabolism
  • Pyramidal Cells / drug effects*
  • Pyramidal Cells / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Structure-Activity Relationship
  • Synaptic Transmission / drug effects*

Substances

  • 10,10-bis(4-pyridinylmethyl)-9(10H)-anthracenone
  • Anthracenes
  • KCNQ Potassium Channels
  • Potassium Channel Blockers