Three-dimensional synaptic analyses of mitral cell and external tufted cell dendrites in rat olfactory bulb glomeruli

J Comp Neurol. 2017 Feb 15;525(3):592-609. doi: 10.1002/cne.24089. Epub 2016 Aug 18.


Recent studies have suggested that the two excitatory cell classes of the mammalian olfactory bulb, the mitral cells (MCs) and tufted cells (TCs), differ markedly in physiological responses. For example, TCs are more sensitive and broadly tuned to odors than MCs and also are much more sensitive to stimulation of olfactory sensory neurons (OSNs) in bulb slices. To examine the morphological bases for these differences, we performed quantitative ultrastructural analyses of glomeruli in rat olfactory bulb under conditions in which specific cells were labeled with biocytin and 3,3'-diaminobenzidine. Comparisons were made between MCs and external TCs (eTCs), which are a TC subtype in the glomerular layer with large, direct OSN signals and capable of mediating feedforward excitation of MCs. Three-dimensional analysis of labeled apical dendrites under an electron microscope revealed that MCs and eTCs in fact have similar densities of several chemical synapse types, including OSN inputs. OSN synapses also were distributed similarly, favoring a distal localization on both cells. Analysis of unlabeled putative MC dendrites further revealed gap junctions distributed uniformly along the apical dendrite and, on average, proximally with respect to OSN synapses. Our results suggest that the greater sensitivity of eTCs vs. MCs is due not to OSN synapse number or absolute location but rather to a conductance in the MC dendrite that is well positioned to attenuate excitatory signals passing to the cell soma. Functionally, such a mechanism could allow rapid and dynamic control of OSN-driven action potential firing in MCs through changes in gap junction properties. J. Comp. Neurol. 525:592-609, 2017. © 2016 Wiley Periodicals, Inc.

Keywords: RRID:SCR_002716; gap junctions; glomerulus; olfaction; reconstructions; sensory neuron; serial section electron microscopy.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 3,3'-Diaminobenzidine
  • Animals
  • Dendrites / physiology
  • Dendrites / ultrastructure*
  • Female
  • Gap Junctions / physiology
  • Gap Junctions / ultrastructure
  • Imaging, Three-Dimensional
  • Lysine / analogs & derivatives
  • Male
  • Microscopy, Electron
  • Microscopy, Fluorescence
  • Neural Inhibition / physiology
  • Olfactory Bulb / physiology
  • Olfactory Bulb / ultrastructure*
  • Patch-Clamp Techniques
  • Rats, Sprague-Dawley
  • Synapses / physiology
  • Synapses / ultrastructure*


  • 3,3'-Diaminobenzidine
  • biocytin
  • Lysine