The organization of two new cortical interneuronal circuits

Nat Neurosci. 2013 Feb;16(2):210-8. doi: 10.1038/nn.3305. Epub 2013 Jan 13.

Abstract

Deciphering the interneuronal circuitry is central to understanding brain functions, yet it remains a challenging task in neurobiology. Using simultaneous quadruple-octuple in vitro and dual in vivo whole-cell recordings, we found two previously unknown interneuronal circuits that link cortical layer 1-3 (L1-3) interneurons and L5 pyramidal neurons in the rat neocortex. L1 single-bouquet cells (SBCs) preferentially formed unidirectional inhibitory connections on L2/3 interneurons that inhibited the entire dendritic-somato-axonal axis of ∼1% of L5 pyramidal neurons located in the same column. In contrast, L1 elongated neurogliaform cells (ENGCs) frequently formed mutual inhibitory and electric connections with L2/3 interneurons, and these L1-3 interneurons inhibited the distal apical dendrite of >60% of L5 pyramidal neurons across multiple columns. Functionally, SBC→L2/3 interneuron→L5 pyramidal neuronal circuits disinhibited and ENGC↔L2/3 interneuron→L5 pyramidal neuronal circuits inhibited the initiation of dendritic complex spikes in L5 pyramidal neurons. As dendritic complex spikes can serve coincidence detection, these cortical interneuronal circuits may be essential for salience selection.

Publication types

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

MeSH terms

  • Age Factors
  • Analysis of Variance
  • Animals
  • Cerebral Cortex / cytology*
  • Electron Microscope Tomography
  • Female
  • In Vitro Techniques
  • Interneurons / classification*
  • Interneurons / physiology*
  • Interneurons / ultrastructure
  • Male
  • Membrane Potentials / physiology
  • Nerve Net / physiology*
  • Neural Inhibition / physiology
  • Neural Pathways / physiology*
  • Patch-Clamp Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Vibrissae / innervation