Two functionally distinct networks of gap junction-coupled inhibitory neurons in the thalamic reticular nucleus

J Neurosci. 2014 Sep 24;34(39):13170-82. doi: 10.1523/JNEUROSCI.0562-14.2014.

Abstract

Gap junctions (GJs) electrically couple GABAergic neurons of the forebrain. The spatial organization of neuron clusters coupled by GJs is an important determinant of network function, yet it is poorly described for nearly all mammalian brain regions. Here we used a novel dye-coupling technique to show that GABAergic neurons in the thalamic reticular nucleus (TRN) of mice and rats form two types of GJ-coupled clusters with distinctive patterns and axonal projections. Most clusters are elongated narrowly along functional modules within the plane of the TRN, with axons that selectively inhibit local groups of relay neurons. However, some coupled clusters have neurons arrayed across the thickness of the TRN and target their axons to both first- and higher-order relay nuclei. Dye coupling was reduced, but not abolished, among cells of connexin36 knock-out mice. Our results suggest that GJs form two distinct types of inhibitory networks that correlate activity either within or across functional modules of the thalamus.

Keywords: dye-coupling; electrical coupling; electrical synapses; gap junctions; thalamic reticular nucleus.

Publication types

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

MeSH terms

  • Animals
  • Axons / metabolism
  • Axons / physiology
  • Connexins / genetics
  • Connexins / metabolism
  • Electrical Synapses / metabolism
  • Electrical Synapses / physiology*
  • GABAergic Neurons / cytology
  • GABAergic Neurons / metabolism
  • GABAergic Neurons / physiology*
  • Gap Junction delta-2 Protein
  • Interneurons / cytology
  • Interneurons / metabolism
  • Interneurons / physiology
  • Intralaminar Thalamic Nuclei / cytology*
  • Intralaminar Thalamic Nuclei / physiology
  • Mice
  • Mice, Inbred C57BL
  • Neural Inhibition
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Connexins