Auditory Golgi cells are interconnected predominantly by electrical synapses

J Neurophysiol. 2016 Aug 1;116(2):540-51. doi: 10.1152/jn.01108.2015. Epub 2016 Apr 27.

Abstract

The mossy fiber-granule cell-parallel fiber system conveys proprioceptive and corollary discharge information to principal cells in cerebellum-like systems. In the dorsal cochlear nucleus (DCN), Golgi cells inhibit granule cells and thus regulate information transfer along the mossy fiber-granule cell-parallel fiber pathway. Whereas excitatory synaptic inputs to Golgi cells are well understood, inhibitory and electrical synaptic inputs to Golgi cells have not been examined. Using paired recordings in a mouse brain slice preparation, we find that Golgi cells of the cochlear nucleus reliably form electrical synapses onto one another. Golgi cells were only rarely electrically coupled to superficial stellate cells, which form a separate network of electrically coupled interneurons in the DCN. Spikelets had a biphasic effect on the excitability of postjunctional Golgi cells, with a brief excitatory phase and a prolonged inhibitory phase due to the propagation of the prejunctional afterhyperpolarization through gap junctions. Golgi cells and stellate cells made weak inhibitory chemical synapses onto Golgi cells with low probability. Electrical synapses are therefore the predominant form of synaptic communication between auditory Golgi cells. We propose that electrical synapses between Golgi cells may function to regulate the synchrony of Golgi cell firing when electrically coupled Golgi cells receive temporally correlated excitatory synaptic input.

Keywords: auditory system; brain stem; cerebellum; inhibition.

Publication types

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

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Anesthetics, Local / pharmacology
  • Animals
  • Animals, Newborn
  • Cesium / pharmacology
  • Chlorides / pharmacology
  • Cochlear Nucleus / cytology*
  • Connexins / deficiency
  • Connexins / metabolism
  • Electrical Synapses / drug effects
  • Electrical Synapses / physiology*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Interleukin-2 Receptor alpha Subunit / genetics
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Lidocaine / analogs & derivatives
  • Lidocaine / pharmacology
  • Mice
  • Mice, Transgenic
  • Nerve Net / drug effects
  • Nerve Net / physiology
  • Neurons / drug effects
  • Neurons / physiology*
  • Neurotransmitter Agents / pharmacology
  • Patch-Clamp Techniques
  • Potassium Channel Blockers / pharmacology
  • Reaction Time / drug effects
  • Reaction Time / physiology
  • Receptors, Metabotropic Glutamate / genetics
  • Receptors, Metabotropic Glutamate / metabolism

Substances

  • Anesthetics, Local
  • Chlorides
  • Connexins
  • Interleukin-2 Receptor alpha Subunit
  • Neurotransmitter Agents
  • Potassium Channel Blockers
  • Receptors, Metabotropic Glutamate
  • connexin 36
  • metabotropic glutamate receptor 2
  • Green Fluorescent Proteins
  • Cesium
  • QX-314
  • Lidocaine
  • cesium chloride