Multiple clusters of release sites formed by individual thalamic afferents onto cortical interneurons ensure reliable transmission

Neuron. 2011 Jul 14;71(1):180-94. doi: 10.1016/j.neuron.2011.05.032.

Abstract

Thalamic afferents supply the cortex with sensory information by contacting both excitatory neurons and inhibitory interneurons. Interestingly, thalamic contacts with interneurons constitute such a powerful synapse that even one afferent can fire interneurons, thereby driving feedforward inhibition. However, the spatial representation of this potent synapse on interneuron dendrites is poorly understood. Using Ca imaging and electron microscopy we show that an individual thalamic afferent forms multiple contacts with the interneuronal proximal dendritic arbor, preferentially near branch points. More contacts are correlated with larger amplitude synaptic responses. Each contact, consisting of a single bouton, can release up to seven vesicles simultaneously, resulting in graded and reliable Ca transients. Computational modeling indicates that the release of multiple vesicles at each contact minimally reduces the efficiency of the thalamic afferent in exciting the interneuron. This strategy preserves the spatial representation of thalamocortical inputs across the dendritic arbor over a wide range of release conditions.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism
  • Computer Simulation
  • Dendrites / physiology
  • Dendrites / ultrastructure
  • Electric Stimulation / methods
  • Excitatory Postsynaptic Potentials / physiology
  • Interneurons / metabolism
  • Interneurons / physiology*
  • Interneurons / ultrastructure
  • Mice
  • Mice, Inbred ICR
  • Microscopy, Electron / methods
  • Molecular Imaging / methods
  • Neural Pathways / metabolism
  • Neural Pathways / physiology
  • Neural Pathways / ultrastructure
  • Neurons, Afferent / metabolism
  • Neurons, Afferent / physiology*
  • Neurons, Afferent / ultrastructure
  • Synaptic Transmission / physiology*
  • Thalamus / metabolism
  • Thalamus / physiology*
  • Thalamus / ultrastructure

Substances

  • Calcium