Loss of olfactory cell adhesion molecule reduces the synchrony of mitral cell activity in olfactory glomeruli

J Physiol. 2011 Apr 15;589(Pt 8):1927-41. doi: 10.1113/jphysiol.2011.206276. Epub 2011 Feb 21.

Abstract

Odours generate activity in olfactory receptor neurons, whose axons contact the dendritic tufts of mitral cells within olfactory bulb glomeruli. These axodendritic synapses are anatomically separated from dendrodendritic synapses within each glomerulus. Mitral cells within a glomerulus show highly synchronized activity as assessed with whole-cell recording from pairs of mitral cells. We examined glomerular activity in mice lacking the olfactory cell adhesion molecule (OCAM). Glomeruli in mice lacking OCAM show a redistribution of synaptic subcompartments, but the total area occupied by axonal inputs was similar to wild-type mice. Stimulation of olfactory nerve bundles showed that excitatory synaptic input to mitral cells as well as dendrodendritic inhibition was unaffected in the knockout. However, correlated spiking in mitral cells was significantly reduced, as was electrical coupling between apical dendrites. To analyse slow network dynamics we induced slow oscillations with a glutamate uptake blocker. Evoked and spontaneous slow oscillations in mitral cells and external tufted cells were broader and had multiple peaks in OCAM knockout mice, indicating that synchrony of slow glomerular activity was also reduced. To assess the degree of shared activity between mitral cells under physiological conditions, we analysed spontaneous sub-threshold voltage oscillations using coherence analysis. Coherent activity was markedly reduced in cells from OCAM knockout mice across a broad range of frequencies consistent with a decrease in tightly time-locked activity. We suggest that synchronous activity within each glomerulus is dependent on segregation of synaptic subcompartments.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Animals
  • Electric Stimulation
  • Excitatory Postsynaptic Potentials
  • Glutamic Acid / metabolism
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials
  • Kinetics
  • Luminescent Proteins / biosynthesis
  • Luminescent Proteins / genetics
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Neural Cell Adhesion Molecules / deficiency*
  • Neural Cell Adhesion Molecules / genetics
  • Neural Inhibition
  • Neural Pathways / metabolism
  • Neurotransmitter Agents / pharmacology
  • Olfactory Bulb / drug effects
  • Olfactory Bulb / metabolism*
  • Patch-Clamp Techniques
  • Periodicity
  • Reaction Time
  • Smell*
  • Synaptic Transmission* / drug effects
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Luminescent Proteins
  • Ncam2 protein, mouse
  • Neural Cell Adhesion Molecules
  • Neurotransmitter Agents
  • Glutamic Acid
  • gamma-Aminobutyric Acid