Cell type-specific inhibitory inputs to dendritic and somatic compartments of parvalbumin-expressing neocortical interneuron

J Neurosci. 2013 Jan 9;33(2):544-55. doi: 10.1523/JNEUROSCI.2255-12.2013.

Abstract

Parvalbumin (PV)-producing fast-spiking neurons are well known to generate gamma oscillation by mutual chemical and electrical connections in the neocortex. Although it was clearly demonstrated that PV neurons form a dense gap junction network with each other not only at the proximal sites but also at the distal dendrites, comprehensive quantitative data on the chemical connections are still lacking. To elucidate the connectivity, we investigated inhibitory inputs to PV neurons in the somatosensory cortex, using the transgenic mice in which the dendrites and cell bodies of PV neurons were clearly visualized. We first examined GABAergic inputs to PV neurons by labeling postsynaptic and presynaptic sites with the immunoreactivities for gephyrin and vesicular GABA transporter. The density of GABAergic inputs was highest on the cell bodies, and almost linearly decreased to the distal dendrites. We then investigated inhibitory inputs from three distinct subgroups of GABAergic interneurons by visualizing the axon terminals immunopositive for PV, somatostatin (SOM), or vasoactive intestinal polypeptide (VIP). PV and SOM inputs were frequently located on the dendrites with the ratio of 2.5:1, but much less on the cell bodies. By contrast, VIP inputs clearly preferred the cell bodies to the dendrites. Consequently, the dendritic and somatic compartments of PV neurons received ∼60 and 62% of inhibitory inputs from PV and VIP neurons, respectively. This compartmental organization of inhibitory inputs suggests that PV neurons, together with gap junctions, constitute mutual connections at the dendrites, and that their activities are negatively controlled by the somatic inputs of VIP neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / physiology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Dendrites / physiology*
  • Fluorescent Antibody Technique, Indirect
  • Green Fluorescent Proteins / metabolism
  • Image Processing, Computer-Assisted
  • In Situ Hybridization, Fluorescence
  • Interneurons / physiology*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microscopy, Immunoelectron
  • Neocortex / cytology
  • Neocortex / metabolism
  • Neocortex / physiology*
  • Nerve Endings / physiology
  • Neural Pathways
  • Parvalbumins / physiology*
  • Somatostatin / genetics
  • Somatostatin / metabolism
  • Vasoactive Intestinal Peptide / genetics
  • Vasoactive Intestinal Peptide / metabolism
  • gamma-Aminobutyric Acid / physiology

Substances

  • Carrier Proteins
  • Membrane Proteins
  • Parvalbumins
  • gephyrin
  • Green Fluorescent Proteins
  • Vasoactive Intestinal Peptide
  • Somatostatin
  • gamma-Aminobutyric Acid