Spike-timing dependent inhibitory plasticity to learn a selective gating of backpropagating action potentials

Eur J Neurosci. 2017 Apr;45(8):1032-1043. doi: 10.1111/ejn.13326. Epub 2016 Aug 2.


Inhibition is known to influence the forward-directed flow of information within neurons. However, also regulation of backward-directed signals, such as backpropagating action potentials (bAPs), can enrich the functional repertoire of local circuits. Inhibitory control of bAP spread, for example, can provide a switch for the plasticity of excitatory synapses. Although such a mechanism is possible, it requires a precise timing of inhibition to annihilate bAPs without impairment of forward-directed excitatory information flow. Here, we propose a specific learning rule for inhibitory synapses to automatically generate the correct timing to gate bAPs in pyramidal cells when embedded in a local circuit of feedforward inhibition. Based on computational modeling of multi-compartmental neurons with physiological properties, we demonstrate that a learning rule with anti-Hebbian shape can establish the required temporal precision. In contrast to classical spike-timing dependent plasticity of excitatory synapses, the proposed inhibitory learning mechanism does not necessarily require the definition of an upper bound of synaptic weights because of its tendency to self-terminate once annihilation of bAPs has been reached. Our study provides a functional context in which one of the many time-dependent learning rules that have been observed experimentally - specifically, a learning rule with anti-Hebbian shape - is assigned a relevant role for inhibitory synapses. Moreover, the described mechanism is compatible with an upregulation of excitatory plasticity by disinhibition.

Keywords: dendritic inhibition; dendritic signaling; feedforward circuit; metaplasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology*
  • Animals
  • Cerebral Cortex / cytology
  • Cerebral Cortex / physiology
  • Computer Simulation
  • Excitatory Postsynaptic Potentials / physiology
  • Models, Neurological*
  • Neural Inhibition / physiology*
  • Neural Pathways / cytology
  • Neural Pathways / physiology
  • Neuronal Plasticity / physiology*
  • Neurons / cytology
  • Neurons / physiology*
  • Pyramidal Cells / physiology
  • Time Factors