Structural organization of the dendritic reticulum linked by gap junctions in layer 4 of the visual cortex

Neuroscience. 2017 Jan 6;340:76-90. doi: 10.1016/j.neuroscience.2016.10.050. Epub 2016 Oct 27.

Abstract

Neuronal gap junctions are ubiquitous in the brain, but their precise positions in actual neuronal circuits have been uncertain, and their functional roles remain unclear. In this study, I visualized connexin36-immunoreactive gap junctions and examined the structural features of the interconnected dendrites arising from parvalbumin (PV)-positive interneurons in layer 4 of the feline visual cortex. I observed evidence for net-like dense linkages of dendrites among virtually all PV neurons (56/58 cells, 96.6%) in the tissue. This dendritic reticulum established connections among clustered cells and further among remote cells. The latter connectivity exhibited a preference for vertical direction, including translaminar linkages, but was also characterized by lateral continuity. Measurement of the distances from each dendritic gap junction back to the two connected somata revealed that at least one of two somata was within 50μm from the junction in 77.5% of the cases and within 75μm in 91.2% of the cases. Thus, distal gap junctions mediated morphologically asymmetrical connection where one soma was close to, but the other soma was far from the connecting junction. This connectivity was typically observed between neurons located apart in the same columnar space, where a long vertical dendrite bridged two neurons through an asymmetrically positioned gap junction. In contrast, gap junctions formed between nearby cells were close to both somata. Thalamocortical afferents established synapses densely on somata of layer 4 PV neurons, indicating the possible involvement of proximal gap junctions in visual stimulus-driven feedforward regulation. These findings provide a new structural basis for cortical investigations.

Keywords: GABA; connexin 36; gap junction; interneuron; parvalbumin; visual cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cats
  • Cell Size
  • Dendrites / metabolism*
  • Female
  • Gap Junctions / metabolism*
  • Imaging, Three-Dimensional
  • Immunohistochemistry
  • Male
  • Microscopy, Electron, Transmission
  • Neurons / cytology
  • Neurons / metabolism
  • Parvalbumins / metabolism
  • Thalamus / cytology
  • Thalamus / metabolism
  • Visual Cortex / cytology*
  • Visual Cortex / metabolism*
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Parvalbumins
  • gamma-Aminobutyric Acid