The role of Ca2+ -dependent K+ - channels at the rat corticostriatal synapses revealed by paired pulse stimulation

Synapse. 2018 Feb;72(2). doi: 10.1002/syn.22017. Epub 2017 Nov 22.

Abstract

Potassium channels play an important role in modulating synaptic activity both at presynaptic and postsynaptic levels. We have shown before that presynaptically located KV and KIR channels modulate the strength of corticostriatal synapses in rat brain, but the role of other types of potassium channels at these synapses remains largely unknown. Here, we show that calcium-dependent potassium channels BK-type but not SK-type channels are located presynaptically in corticostriatal synapses. We stimulated cortical neurons in rat brain slices and recorded postsynaptic excitatory potentials (EPSP) in medium spiny neurons (MSN) in dorsal neostriatum. By using a paired pulse protocol, we induced synaptic facilitation before applying either BK- or SK-specific toxins. Thus, we found that blockage of BKCa with iberiotoxin (10 nM) reduces synaptic facilitation and increases the amplitude of the EPSP, while exposure to SK-blocker apamin (100 nM) has no effect. Additionally, we induced train action potentials on striatal MSN by current injection before and after the exposure to KCa toxins. We found that the action potential becomes broader when the MSN is exposed to iberiotoxin, although it has no impact on frequency. In contrast, exposure to apamin results in loss of afterhyperpolarization phase and an increase of spike frequency. Therefore, we concluded that postsynaptic SK channels are involved in afterhyperpolarization and modulation of spike frequency while the BK channels are involved on the late repolarization phase of the action potential. Altogether, our results show that calcium-dependent potassium channels modulate both input towards and output from the striatum.

Keywords: BK and SK potassium channels; corticostriatal afferents; paired pulse facilitation; striatum.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Apamin / pharmacology
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / metabolism*
  • Corpus Striatum / drug effects
  • Corpus Striatum / metabolism*
  • Electric Stimulation
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Large-Conductance Calcium-Activated Potassium Channels / antagonists & inhibitors
  • Large-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Male
  • Neurons / drug effects
  • Neurons / metabolism*
  • Patch-Clamp Techniques
  • Peptides / pharmacology
  • Potassium Channel Blockers / pharmacology
  • Rats, Wistar
  • Small-Conductance Calcium-Activated Potassium Channels / antagonists & inhibitors
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Synapses / drug effects
  • Synapses / metabolism*
  • Tissue Culture Techniques

Substances

  • Large-Conductance Calcium-Activated Potassium Channels
  • Peptides
  • Potassium Channel Blockers
  • Small-Conductance Calcium-Activated Potassium Channels
  • Apamin
  • iberiotoxin