Electrophysiological characterization of Grueneberg ganglion olfactory neurons: spontaneous firing, sodium conductance, and hyperpolarization-activated currents

J Neurophysiol. 2012 Sep;108(5):1318-34. doi: 10.1152/jn.00907.2011. Epub 2012 May 30.

Abstract

Mammals rely on their acute olfactory sense for their survival. The most anterior olfactory subsystem in the nose, the Grueneberg ganglion (GG), plays a role in detecting alarm pheromone, cold, and urinary compounds. GG neurons respond homogeneously to these stimuli with increases in intracellular [Ca(2+)] or transcription of immediate-early genes. In this electrophysiological study, we used patch-clamp techniques to characterize the membrane properties of GG neurons. Our results offer evidence of functional heterogeneity in the GG. GG neurons fire spontaneously and independently in several stable patterns, including phasic and repetitive single-spike modes of discharge. Whole cell recordings demonstrated two distinct voltage-gated fast-inactivating Na(+) currents with different steady-state voltage dependencies and different sensitivities to tetrodotoxin. Hodgkin-Huxley simulations showed that these Na(+) currents confer dual mechanisms of action potential generation and contribute to different firing patterns. Additionally, GG neurons exhibited hyperpolarization-activated inward currents that modulated spontaneous firing in vitro. Thus, in GG neurons, the heterogeneity of firing patterns is linked to the unusual repertoire of ionic currents. The membrane properties described here will aid the interpretation of chemosensory function in the GG.

Publication types

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

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Animals, Newborn
  • Biophysical Phenomena / drug effects
  • Biophysical Phenomena / physiology*
  • Biophysics
  • Cesium / pharmacology
  • Chlorides / pharmacology
  • Computer Simulation
  • Cyclic GMP / analogs & derivatives
  • Cyclic GMP / pharmacology
  • Cyclic Nucleotide-Gated Cation Channels / drug effects
  • Cyclic Nucleotide-Gated Cation Channels / genetics
  • Cyclic Nucleotide-Gated Cation Channels / metabolism*
  • Electric Stimulation
  • Ganglia, Sensory / cytology*
  • Glial Fibrillary Acidic Protein / metabolism
  • Green Fluorescent Proteins / genetics
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • In Vitro Techniques
  • Mice
  • Mice, Transgenic
  • Models, Neurological
  • Nerve Growth Factors / metabolism
  • Olfactory Receptor Neurons / drug effects
  • Olfactory Receptor Neurons / physiology*
  • Patch-Clamp Techniques
  • Potassium Channels / drug effects
  • Potassium Channels / genetics
  • Potassium Channels / metabolism*
  • RNA, Messenger / metabolism
  • S100 Calcium Binding Protein beta Subunit
  • S100 Proteins / metabolism
  • Sodium Channel Blockers / pharmacology
  • Sodium Channels / drug effects
  • Sodium Channels / genetics
  • Sodium Channels / metabolism*
  • Tetrodotoxin / pharmacology
  • Thionucleotides / pharmacology

Substances

  • Chlorides
  • Cyclic Nucleotide-Gated Cation Channels
  • Glial Fibrillary Acidic Protein
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Nerve Growth Factors
  • Potassium Channels
  • RNA, Messenger
  • S100 Calcium Binding Protein beta Subunit
  • S100 Proteins
  • Sodium Channel Blockers
  • Sodium Channels
  • Thionucleotides
  • Green Fluorescent Proteins
  • 8-bromoguanosino-3',5'-cyclic monophosphorothioate
  • Cesium
  • Tetrodotoxin
  • cesium chloride
  • Cyclic GMP