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  • Review Article
  • Published:

Information processing in the axon

Key Points

  • Axons have traditionally been regarded as simple cables for the stable transmission of action potentials. But recent data indicate that the functional capacity of axons is much more extensive and complex.

  • Propagation of action potentials along axons is influenced by various voltage-gated conductances. Axons contain sodium and potassium channels, as well as at least two types of cationic channel that are activated by hyperpolarization or G protein-dependent receptors. These axonal channels might participate in modifying the width and/or amplitude of action potentials.

  • The variability of axonal morphology also affects the propagation of action potentials. Length, diameter, degree of arborization and number of varicosities (synaptic boutons) vary greatly between different axons. Boutons and branch points reduce the conduction velocity of action potentials.

  • Selective failure of action-potential propagation in axons regulates communication with postsynaptic neurons. The likelihood of failure depends on morphology, the frequency of axon stimulation and/or activation of presynaptic A-type potassium channels.

  • Action potentials can be 'reflected' in axons. Reflection occurs when delayed action potentials establish a local potential that propagates backwards. The net result is a spike that travels in both directions.

  • Interactions between axons also influence conduction of action potentials. All of these factors increase the computational capacity of axons and affect the dynamics of synaptic coupling.

Abstract

Axons link distant brain regions and are generally regarded as reliable transmission cables in which stable propagation occurs once an action potential has been generated. However, recent experimental and theoretical data indicate that the functional capabilities of axons are much more diverse than traditionally thought. Beyond axonal propagation, intrinsic voltage-gated conductances together with the intrinsic geometrical properties of the axon determine complex phenomena such as branch-point failures and reflected propagation. This review considers recent evidence for the role of these forms of axonal computation in the short-term dynamics of neural communication.

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Figure 1: Shaping of the action potential in the axon.
Figure 2: The role of sodium channel inactivation in short-term synaptic depression.
Figure 3: Branch points and varicosities.
Figure 4: Axonal propagation and spike timing.
Figure 5: Propagation failures.
Figure 6: Mechanisms of propagation failures induced by repetitive stimulation.
Figure 7: Gating of action-potential propagation by the potassium current IA.
Figure 8: Reflection of action potentials.
Figure 9: Axo-axonic coupling of hippocampal pyramidal neurons.

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Acknowledgements

This study was supported by Centre National de la Recherche Scientifique, Ministry of Research ('Actions Incitatives Jeunes Chercheurs' 5169), Institut National de la Santé et de la Recherche Médicale (Programme 'Avenir'), and Fondation pour la Recherche Médicale. I thank G. Rougon for her support, S. Binzcak, T. Freund, P. Somogyi, E. Carlier, S. Boudkkazi & N. Ankri for helpful discussions, and M. Seagar for his constant support and constructive criticisms on the manuscript.

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DATABASE

LocusLink

Kv1.1

Kv1.2

Kv1.4

Kv3.1

Kv3.4

TRPC1

TRPC5

Glossary

GAP JUNCTIONS

Morphological equivalent of electrical synapses. They are composed of two pairs of six connexins that form two apposed hemichannels constituting a pore between two neurons.

TETRODOTOXIN

A neurotoxin derived from the Fugu, or puffer fish, which specifically and reversibly blocks voltage-gated sodium channels.

PAIRED-PULSE FACILITATION

If two stimuli are delivered in close succession to an axon, the postsynaptic response to the second stimulus is often larger than to the first one. This phenomenon is referred to as paired-pulse facilitation, and is thought to depend on the accumulation of Ca2+ that ensues after successive stimuli.

RILUZOLE

2-amino-6-trifluoromethoxy-benzothiazole). A voltage-dependent sodium channel blocker that is used as an anticonvulsant.

OUABAIN

Extracted from the seed of the Strophantus, a tropical creeper, ouabain is a cardiotonic that blocks sodium channel electrogenic pumps.

ELECTRICAL SYNAPSE

Specialized sites where gap-junction channels bridge the membrane of adjacent neurons and provide a low-resistance pathway for ions and small molecules, thereby permitting direct transmission of electrical signals.

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Debanne, D. Information processing in the axon. Nat Rev Neurosci 5, 304–316 (2004). https://doi.org/10.1038/nrn1397

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