Somatic membrane potential and Kv1 channels control spike repolarization in cortical axon collaterals and presynaptic boutons

J Neurosci. 2011 Oct 26;31(43):15490-8. doi: 10.1523/JNEUROSCI.2752-11.2011.

Abstract

The shape of action potentials invading presynaptic terminals, which can vary significantly from spike waveforms recorded at the soma, may critically influence the probability of synaptic neurotransmitter release. Revealing the conductances that determine spike shape in presynaptic boutons is important for understanding how changes in the electrochemical context in which a spike is generated, such as subthreshold depolarization spreading from the soma, can modulate synaptic strength. Utilizing recent improvements in the signal-to-noise ratio of voltage-sensitive dye imaging in mouse brain slices, we demonstrate that intracortical axon collaterals and en passant presynaptic terminals of layer 5 pyramidal cells exhibit a high density of Kv1 subunit-containing ion channels, which generate a slowly inactivating K(+) current critically important for spike repolarization in these compartments. Blockade of the current by low doses of 4-aminopyridine or α-dendrotoxin dramatically slows the falling phase of action potentials in axon collaterals and presynaptic boutons. Furthermore, subthreshold depolarization of the soma broadened action potentials in collaterals bearing presynaptic boutons, an effect abolished by blocking Kv1 channels with α-dendrotoxin. These results indicate that action potential-induced synaptic transmission may operate through a mix of analog-digital transmission owing to the properties of Kv1 channels in axon collaterals and presynaptic boutons.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • 4-Aminopyridine / pharmacology
  • Animals
  • Axons / drug effects
  • Axons / physiology*
  • Biophysical Phenomena / drug effects
  • Biophysical Phenomena / physiology
  • Computer Simulation
  • Crystallins / genetics
  • Dose-Response Relationship, Drug
  • Elapid Venoms / pharmacology
  • Electric Stimulation
  • Female
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • In Vitro Techniques
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology*
  • Mice
  • Mice, Transgenic
  • Models, Neurological
  • Nerve Net / drug effects
  • Nerve Net / physiology
  • Neurons / drug effects
  • Neurons / physiology*
  • Patch-Clamp Techniques / methods
  • Potassium Channel Blockers / pharmacology
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / physiology*
  • Shaker Superfamily of Potassium Channels / metabolism*
  • Somatosensory Cortex / cytology*
  • Styrenes / metabolism
  • Tetraethylammonium / pharmacology

Substances

  • Crystallins
  • Elapid Venoms
  • JPW 3028
  • Potassium Channel Blockers
  • Shaker Superfamily of Potassium Channels
  • Styrenes
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • crystallin mu
  • Tetraethylammonium
  • dendrotoxin
  • 4-Aminopyridine