Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons

Neuron. 2005 Dec 22;48(6):1039-53. doi: 10.1016/j.neuron.2005.10.031.

Abstract

Input to the central nervous system from olfactory sensory neurons (OSNs) is modulated presynaptically. We investigated the functional organization of this inhibition and its role in odor coding by imaging neurotransmitter release from OSNs in slices and in vivo in mice expressing synaptopHluorin, an optical indicator of vesicle exocytosis. Release from OSNs was strongly suppressed by heterosynaptic, intraglomerular inhibition. In contrast, inhibitory connections between glomeruli mediated only weak lateral inhibition of OSN inputs in slices and did not do so in response to odorant stimulation in vivo. Blocking presynaptic inhibition in vivo increased the amplitude of odorant-evoked input to glomeruli but had little effect on spatial patterns of glomerular input. Thus, intraglomerular inhibition limits the strength of olfactory input to the CNS, whereas interglomerular inhibition plays little or no role. This organization allows for control of input sensitivity while maintaining the spatial maps of glomerular activity thought to encode odorant identity.

Publication types

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

MeSH terms

  • Animals
  • Dendrites / drug effects
  • Dendrites / metabolism
  • Dopamine Antagonists / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Fluorescent Dyes / metabolism
  • GABA-B Receptor Antagonists
  • Mice
  • Mice, Transgenic
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / metabolism*
  • Neuropil / drug effects
  • Neuropil / metabolism
  • Neurotransmitter Agents / metabolism
  • Odorants
  • Olfactory Bulb / anatomy & histology
  • Olfactory Bulb / metabolism*
  • Olfactory Pathways / anatomy & histology
  • Olfactory Pathways / metabolism*
  • Organ Culture Techniques
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / metabolism
  • Receptors, GABA-B / metabolism
  • Smell / drug effects
  • Smell / physiology*
  • Synapses / drug effects
  • Synapses / metabolism*
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology

Substances

  • Dopamine Antagonists
  • Excitatory Amino Acid Antagonists
  • Fluorescent Dyes
  • GABA-B Receptor Antagonists
  • Neurotransmitter Agents
  • Receptors, GABA-B