Local and commissural IC neurons make axosomatic inputs on large GABAergic tectothalamic neurons

J Comp Neurol. 2014 Oct 15;522(15):3539-54. doi: 10.1002/cne.23623. Epub 2014 May 21.

Abstract

Large GABAergic (LG) neurons are a distinct type of neuron in the inferior colliculus (IC) identified by their dense vesicular glutamate transporter 2 (VGLUT2)-containing axosomatic synaptic terminals. Yet the sources of these terminals are unknown. Since IC glutamatergic neurons express VGLUT2, and IC neurons are known to have local collaterals, we tested the hypothesis that these excitatory, glutamatergic axosomatic inputs on LG neurons come from local axonal collaterals and commissural IC neurons. We injected a recombinant viral tracer into the IC which enabled Golgi-like green fluorescent protein (GFP) labeling in both dendrites and axons. In all cases, we found terminals positive for both GFP and VGLUT2 (GFP+/VGLUT2+) that made axosomatic contacts on LG neurons. One to six axosomatic contacts were made on a single LG cell body by a single axonal branch. The GFP-labeled neurons giving rise to the VGLUT2+ terminals on LG neurons were close by. The density of GFP+/VGLUT2+ terminals on the LG neurons was related to the number of nearby GFP-labeled cells. On the contralateral side, a smaller number of LG neurons received axosomatic contacts from GFP+/VGLUT2+ terminals. In cases with a single GFP-labeled glutamatergic neuron, the labeled axonal plexus was flat, oriented in parallel to the fibrodendritic laminae, and contacted 9-30 LG cell bodies within the plexus. Our data demonstrated that within the IC microcircuitry there is a convergence of inputs from local IC excitatory neurons on LG cell bodies. This suggests that LG neurons are heavily influenced by the activity of the nearby laminar glutamatergic neurons in the IC.

Keywords: GABA; RGD ID: 1566430; RRID: AB_2278725; auditory system; excitatory axosomatic synapse; inferior colliculus; vesicular glutamate transporter.

Publication types

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

MeSH terms

  • Animals
  • Axons* / metabolism
  • Dendrites
  • Female
  • Fluorescent Antibody Technique
  • GABAergic Neurons / cytology*
  • GABAergic Neurons / metabolism
  • Immunohistochemistry
  • Inferior Colliculi / cytology*
  • Inferior Colliculi / metabolism
  • Male
  • Microscopy, Immunoelectron
  • Neuroanatomical Tract-Tracing Techniques
  • Neurons / cytology*
  • Neurons / metabolism
  • Presynaptic Terminals* / metabolism
  • Rats, Long-Evans
  • Vesicular Glutamate Transport Protein 2 / metabolism

Substances

  • Slc17a6 protein, rat
  • Vesicular Glutamate Transport Protein 2