Complementary postsynaptic activity patterns elicited in olfactory bulb by stimulation of mitral/tufted and centrifugal fiber inputs to granule cells

J Neurophysiol. 2007 Jan;97(1):296-306. doi: 10.1152/jn.00823.2006. Epub 2006 Oct 11.

Abstract

Main olfactory bulb (MOB) granule cells receive spatially segregated glutamatergic synaptic inputs from the dendrites of mitral/tufted cells as well as from the axons of centrifugal fibers (CFFs) originating in olfactory cortical areas. Dendrodendritic synapses from mitral/tufted cells occur on granule cell distal dendrites in the external plexiform layer (EPL), whereas CFFs preferentially target the somata/proximal dendrites of granule cells in the granule cell layer (GCL). In the present study, tract tracing, and recordings of field potentials and voltage-sensitive dye optical signals were used to map activity patterns elicited by activation of these two inputs to granule cells in mouse olfactory bulb slices. Stimulation of the lateral olfactory tract (LOT) produced a negative field potential in the EPL and a positivity in the GCL. CFF stimulation produced field potentials of opposite polarity in the EPL and GCL to those elicited by LOT. LOT-evoked optical signals appeared in the EPL and spread subsequently to deeper layers, whereas CFF-evoked responses appeared in the GCL and then spread superficially. Evoked responses were reduced by N-methyl-d-aspartate (NMDA) receptor antagonists and completely suppressed by AMPA receptor antagonists. Reduction of extracellular Mg(2+) enhanced the strength and spatiotemporal extent of the evoked responses. These and additional findings indicate that LOT- and CFF-evoked field potentials and optical signals reflect postsynaptic activity in granule cells, with moderate NMDA and dominant AMPA receptor components. Taken together, these results demonstrate that LOT and CFF stimulation in MOB slices selectively activate glutamatergic inputs to the distal dendrites versus somata/proximal dendrites of granule cells.

Publication types

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

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Animals
  • Carbocyanines
  • Dendrites / drug effects
  • Dendrites / physiology
  • Dendrites / ultrastructure
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • Glutamic Acid / metabolism
  • Interneurons / cytology
  • Interneurons / drug effects
  • Interneurons / physiology*
  • Magnesium / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neural Pathways / cytology
  • Neural Pathways / drug effects
  • Neural Pathways / physiology*
  • Olfactory Bulb / cytology
  • Olfactory Bulb / drug effects
  • Olfactory Bulb / physiology*
  • Olfactory Pathways / cytology
  • Olfactory Pathways / drug effects
  • Olfactory Pathways / physiology
  • Organ Culture Techniques
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / physiology
  • Presynaptic Terminals / ultrastructure
  • Pyridinium Compounds
  • Receptors, Glutamate / drug effects
  • Receptors, Glutamate / metabolism
  • Smell / physiology
  • Synapses / drug effects
  • Synapses / physiology*
  • Synapses / ultrastructure
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology*

Substances

  • 3,3'-dihexadecylindocarbocyanine
  • Carbocyanines
  • Excitatory Amino Acid Antagonists
  • Pyridinium Compounds
  • Receptors, Glutamate
  • 4-(4-dihexadecylaminostyryl)-N-methylpyridium
  • Glutamic Acid
  • Magnesium