Dopamine inhibits N-type channels in visceral afferents to reduce synaptic transmitter release under normoxic and chronic intermittent hypoxic conditions

J Neurophysiol. 2009 May;101(5):2270-8. doi: 10.1152/jn.91304.2008. Epub 2009 Feb 25.

Abstract

Glutamatergic synaptic currents elicited in second-order neurons in the nucleus of the solitary tract (nTS) by activation of chemosensory and other visceral afferent fibers are severely reduced following 10 days of chronic intermittent hypoxia (CIH). The mechanism by which this occurs is unknown. A strong candidate for producing the inhibition is dopamine, which is also released from the presynaptic terminals and which we have shown exerts a tonic presynaptic inhibition on glutamate release. We postulated that tonic activation of the D2 receptors inhibits presynaptic calcium currents to reduce transmitter release and that in CIH this occurs in conjunction with an increase in the dopamine inhibitory response due to the increase in presynaptic D2 receptors or an increase in dopamine release further suppressing the evoked excitatory postsynaptic current (eEPSC). Thus we predicted that blockade of the D2 receptors would return the EPSC to values of animals maintained under normoxic conditions. We found that dopamine and quinpirole, the selective D2-like agonist, inhibit calcium currents via the D2 receptors by acting on the N-type calcium channel in presynaptic neurons and their nTS central terminals. However, in brain slice studies from CIH animals, although the D2 antagonist sulpiride increased the CIH-reduced amplitude of synaptic currents, EPSCs were not restored to normal levels. This indicates that while the dopamine inhibitory effect remains intact in CIH, most of the reduction in the eEPSC amplitude occurs via alternative mechanisms.

Publication types

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

MeSH terms

  • Animals
  • Biophysics
  • Calcium / metabolism
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, N-Type / physiology*
  • Cells, Cultured
  • Dopamine / metabolism
  • Dopamine / pharmacology*
  • Dopamine Agonists / pharmacology
  • Drug Interactions
  • Electric Stimulation / methods
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Female
  • Glutamic Acid / metabolism*
  • Hypoxia / pathology
  • Hypoxia / physiopathology*
  • In Vitro Techniques
  • Male
  • Membrane Potentials / drug effects
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology
  • Neurons / drug effects
  • Neurons / physiology*
  • Nodose Ganglion / cytology
  • Patch-Clamp Techniques
  • Pyridinium Compounds / metabolism
  • Quinpirole / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Solitary Nucleus / pathology
  • Synapses / drug effects*
  • Visceral Afferents / drug effects
  • Visceral Afferents / physiopathology*

Substances

  • Calcium Channel Blockers
  • Calcium Channels, N-Type
  • Dopamine Agonists
  • Pyridinium Compounds
  • 4-(4-dihexadecylaminostyryl)-N-methylpyridium
  • Quinpirole
  • Glutamic Acid
  • Calcium
  • Dopamine