Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons

Nat Neurosci. 2013 Aug;16(8):1068-76. doi: 10.1038/nn.3446. Epub 2013 Jun 30.

Abstract

Cortical inhibitory neurons contact each other to form a network of inhibitory synaptic connections. Our knowledge of the connectivity pattern underlying this inhibitory network is, however, still incomplete. Here we describe a simple and complementary interaction scheme between three large, molecularly distinct interneuron populations in mouse visual cortex: parvalbumin-expressing interneurons strongly inhibit one another but provide little inhibition to other populations. In contrast, somatostatin-expressing interneurons avoid inhibiting one another yet strongly inhibit all other populations. Finally, vasoactive intestinal peptide-expressing interneurons preferentially inhibit somatostatin-expressing interneurons. This scheme occurs in supragranular and infragranular layers, suggesting that inhibitory networks operate similarly at the input and output of the visual cortex. Thus, as the specificity of connections between excitatory neurons forms the basis for the cortical canonical circuit, the scheme described here outlines a standard connectivity pattern among cortical inhibitory neurons.

Publication types

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

MeSH terms

  • Animals
  • Biomarkers
  • Channelrhodopsins
  • Female
  • Genes, Reporter
  • Inhibitory Postsynaptic Potentials / radiation effects
  • Interneurons / chemistry
  • Interneurons / classification
  • Interneurons / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nerve Tissue Proteins / analysis
  • Neural Inhibition / physiology*
  • Optogenetics
  • Organophosphorus Compounds / pharmacology
  • Parvalbumins / analysis
  • Patch-Clamp Techniques
  • Photic Stimulation
  • Principal Component Analysis
  • Pyramidal Cells / physiology
  • Quinoxalines / pharmacology
  • Recombinant Fusion Proteins / physiology
  • Somatostatin / analysis
  • Synaptic Transmission / physiology
  • Synaptic Transmission / radiation effects
  • Vasoactive Intestinal Peptide / analysis
  • Visual Cortex / physiology*

Substances

  • Biomarkers
  • Channelrhodopsins
  • Nerve Tissue Proteins
  • Organophosphorus Compounds
  • Parvalbumins
  • Quinoxalines
  • Recombinant Fusion Proteins
  • 2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline
  • CGP 54626
  • Vasoactive Intestinal Peptide
  • Somatostatin