VIP-containing deep short-axon cells of the olfactory bulb innervate interneurons different from granule cells

Eur J Neurosci. 2003 Oct;18(7):1751-63. doi: 10.1046/j.1460-9568.2003.02895.x.


This study investigates the targets of the population of vasoactive intestinal polypeptide (VIP)-containing deep short-axon cells of the rat olfactory bulb (OB), combining single- and double-immunocytochemical approaches under light and electron microscopy. It has been assumed that deep short-axon cells innervate granule cells in the mammalian OB, but their synaptic connectivity has not been demonstrated to date. Our results indicate that, instead of the accepted scheme of the bulbar circuitry, VIP-containing deep short-axon cells are gamma-aminobutyric acid (GABA)ergic interneurons specialized in the selective innervation of other GABAergic deep short-axon cells. Their axons contact with the perisomatic region and the dendritic portions of subsets of deep short-axon cells that contain VIP, calbindin D-28k and neuropeptide Y. Electron microscopy reveals axo-somatic and axo-dendritic symmetrical synapses from VIP-containing boutons. Taken altogether, our data show that the VIP-containing deep short-axon cells of the rat OB form an interneuronal network that modulates the function of other interneurons different from granule cells. They might be involved indirectly in the inhibition or disinhibition of principal cells or might participate in the generation of oscillatory activity and in the synchronization of populations of interneurons and, then, of principal cells. Present data demonstrate that modulation of the OB by local circuits is more complex than the simple inhibition from periglomerular cells and granule cells, and remark the importance of considering the contribution of other classes of GABAergic interneurons different from periglomerular cells and granule cells to the bulbar circuitry.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / classification
  • Axons / metabolism*
  • Axons / ultrastructure
  • Calbindin 2
  • Calbindins
  • Female
  • Immunohistochemistry
  • Microscopy, Electron
  • Neurons / classification
  • Neurons / metabolism*
  • Neurons / ultrastructure
  • Neuropeptide Y / metabolism
  • Olfactory Bulb / cytology*
  • Parvalbumins / metabolism
  • Rats
  • Rats, Wistar
  • S100 Calcium Binding Protein G / metabolism
  • Vasoactive Intestinal Peptide / metabolism*
  • gamma-Aminobutyric Acid / metabolism


  • Calbindin 2
  • Calbindins
  • Neuropeptide Y
  • Parvalbumins
  • S100 Calcium Binding Protein G
  • Vasoactive Intestinal Peptide
  • gamma-Aminobutyric Acid