Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy

Maarten H P Kole; Johannes J Letzkus; Greg J Stuart

doi:10.1016/j.neuron.2007.07.031

Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy

Neuron. 2007 Aug 16;55(4):633-47. doi: 10.1016/j.neuron.2007.07.031.

Authors

Maarten H P Kole¹, Johannes J Letzkus, Greg J Stuart

Affiliation

¹ Division of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra, ACT 0200, Australia.

PMID: 17698015
DOI: 10.1016/j.neuron.2007.07.031

Abstract

Action potentials are binary signals that transmit information via their rate and temporal pattern. In this context, the axon is thought of as a transmission line, devoid of a role in neuronal computation. Here, we show a highly localized role of axonal Kv1 potassium channels in shaping the action potential waveform in the axon initial segment (AIS) of layer 5 pyramidal neurons independent of the soma. Cell-attached recordings revealed a 10-fold increase in Kv1 channel density over the first 50 microm of the AIS. Inactivation of AIS and proximal axonal Kv1 channels, as occurs during slow subthreshold somatodendritic depolarizations, led to a distance-dependent broadening of axonal action potentials, as well as an increase in synaptic strength at proximal axonal terminals. Thus, Kv1 channels are strategically positioned to integrate slow subthreshold signals, providing control of the presynaptic action potential waveform and synaptic coupling in local cortical circuits.

MeSH terms

4-Aminopyridine / pharmacology
Action Potentials / drug effects
Action Potentials / physiology*
Action Potentials / radiation effects
Animals
Axons / drug effects
Axons / physiology*
Axons / radiation effects
Cerebral Cortex / cytology
Dose-Response Relationship, Drug
Dose-Response Relationship, Radiation
Elapid Venoms / pharmacology
Electric Stimulation / methods
Excitatory Postsynaptic Potentials / drug effects
Excitatory Postsynaptic Potentials / physiology
Excitatory Postsynaptic Potentials / radiation effects
Female
In Vitro Techniques
Lysine / analogs & derivatives
Lysine / metabolism
Male
Models, Neurological
Patch-Clamp Techniques
Potassium Channel Blockers / pharmacology
Pyramidal Cells / cytology*
Rats
Rats, Wistar
Shaker Superfamily of Potassium Channels / physiology*
Synapses / drug effects
Synapses / physiology*
Synapses / radiation effects

Substances

Elapid Venoms
Potassium Channel Blockers
Shaker Superfamily of Potassium Channels
dendrotoxin I
4-Aminopyridine
biocytin
Lysine