Canonical Organization of Layer 1 Neuron-Led Cortical Inhibitory and Disinhibitory Interneuronal Circuits

Cereb Cortex. 2015 Aug;25(8):2114-26. doi: 10.1093/cercor/bhu020. Epub 2014 Feb 18.


Interneurons play a key role in cortical function and dysfunction, yet organization of cortical interneuronal circuitry remains poorly understood. Cortical Layer 1 (L1) contains 2 general GABAergic interneuron groups, namely single bouquet cells (SBCs) and elongated neurogliaform cells (ENGCs). SBCs predominantly make unidirectional inhibitory connections (SBC→) with L2/3 interneurons, whereas ENGCs frequently form reciprocal inhibitory and electric connections (ENGC↔) with L2/3 interneurons. Here, we describe a systematic investigation of the pyramidal neuron targets of L1 neuron-led interneuronal circuits in the rat barrel cortex with simultaneous octuple whole-cell recordings and report a simple organizational scheme of the interneuronal circuits. Both SBCs→ and ENGC ↔ L2/3 interneuronal circuits connect to L2/3 and L5, but not L6, pyramidal neurons. SBC → L2/3 interneuronal circuits primarily inhibit the entire dendritic-somato-axonal axis of a few L2/3 and L5 pyramidal neurons located within the same column. In contrast, ENGC ↔ L2/3 interneuronal circuits generally inhibit the distal apical dendrite of many L2/3 and L5 pyramidal neurons across multiple columns. Finally, L1 interneuron-led circuits target distinct subcellular compartments of L2/3 and L5 pyramidal neurons in a L2/3 interneuron type-dependent manner. These results suggest that L1 neurons form canonical interneuronal circuits to control information processes in both supra- and infragranular cortical layers.

Keywords: attention; circuits; cortex; disinhibition; inhibition; interneurons; salient selection.

Publication types

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

MeSH terms

  • Animals
  • Female
  • Interneurons / physiology*
  • Interneurons / ultrastructure
  • Male
  • Microscopy, Electron
  • Neural Inhibition / physiology*
  • Neural Pathways / physiology
  • Neural Pathways / ultrastructure
  • Patch-Clamp Techniques
  • Pyramidal Cells / physiology
  • Pyramidal Cells / ultrastructure
  • Rats, Sprague-Dawley
  • Somatosensory Cortex / physiology*
  • Somatosensory Cortex / ultrastructure
  • Synapses / physiology*
  • Synapses / ultrastructure
  • Tissue Culture Techniques
  • Vibrissae / physiology