Novel interneuronal network in the mouse posterior piriform cortex

J Comp Neurol. 2006 Dec 20;499(6):1000-15. doi: 10.1002/cne.21166.

Abstract

The neural circuits of the piriform cortex mediate field potential oscillations and complex functions related to integrating odor cues with behavior, affective states, and multisensory processing. Previous anatomical studies have established major neural pathways linking the piriform cortex to other cortical and subcortical regions and major glutamatergic and GABAergic neuronal subtypes within the piriform circuits. However, the quantitative properties of diverse piriform interneurons are unknown. Using quantitative neural anatomical analysis and electrophysiological recording applied to a GAD65-EGFP transgenic mouse expressing GFP (green fluorescent protein) under the control of the GAD65 promoter, here we report a novel inhibitory network that is composed of neurons positive for GAD65-EGFP in the posterior piriform cortex (PPC). These interneurons had stereotyped dendritic and axonal properties that were distinct from basket cells or interneurons expressing various calcium-binding proteins (parvalbumin, calbindin, and calretinin) within the PPC. The GAD65-GFP neurons are GABAergic and outnumbered any other interneurons (expressing parvalbumin, calbindin, and calretinin) we studied. The firing pattern of these interneurons was highly homogenous and is similar to the regular-spiking nonpyramidal (RSNP) interneurons reported in primary sensory and other neocortical regions. Robust dye coupling among these interneurons and expression of connexin 36 suggested that they form electrically coupled networks. The predominant targets of descending axons of these interneurons were the dendrites of Layer III principal cells. Additionally, synapses were found on dendrites and somata of deep Layer II principal neurons and Layer III basket cells. A similar interneuronal subtype was also found in GAD65-EGFP-negative mouse. The extensive dendritic bifurcation at superficial lamina IA among horizontal afferent fibers and unique axonal targeting pattern suggests that these interneurons may play a role in direct feedforward inhibitory and disinhibitory olfactory processing. We conclude that the GAD65-GFP neurons may play distinct roles in regulating information flow and olfactory-related oscillation within the PPC in vivo.

Publication types

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

MeSH terms

  • Animals
  • Axons / physiology
  • Axons / ultrastructure
  • Brain Mapping
  • Calcium-Binding Proteins / metabolism
  • Connexins / metabolism
  • Dendrites / physiology
  • Dendrites / ultrastructure
  • Gap Junction delta-2 Protein
  • Gap Junctions / metabolism
  • Glutamate Decarboxylase / metabolism
  • Green Fluorescent Proteins / metabolism
  • Immunohistochemistry
  • Interneurons / cytology*
  • Interneurons / physiology
  • Isoenzymes / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nerve Net / cytology*
  • Nerve Net / physiology
  • Neural Inhibition / physiology
  • Neural Pathways / cytology*
  • Neural Pathways / physiology
  • Olfactory Pathways / cytology*
  • Olfactory Pathways / physiology
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Calcium-Binding Proteins
  • Connexins
  • Isoenzymes
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • gamma-Aminobutyric Acid
  • Glutamate Decarboxylase
  • glutamate decarboxylase 2