Dopamine-induced oscillations of the pyloric pacemaker neuron rely on release of calcium from intracellular stores

J Neurophysiol. 2011 Sep;106(3):1288-98. doi: 10.1152/jn.00456.2011. Epub 2011 Jun 15.

Abstract

Endogenously bursting neurons play central roles in many aspects of nervous system function, ranging from motor control to perception. The properties and bursting patterns generated by these neurons are subject to neuromodulation, which can alter cycle frequency and amplitude by modifying the properties of the neuron's ionic currents. In the stomatogastric ganglion (STG) of the spiny lobster, Panulirus interruptus, the anterior burster (AB) neuron is a conditional oscillator in the presence of dopamine (DA) and other neuromodulators and serves as the pacemaker to drive rhythmic output from the pyloric network. We analyzed the mechanisms by which DA evokes bursting in the AB neuron. Previous work showed that DA-evoked bursting is critically dependent on external calcium (Harris-Warrick RM, Flamm RE. J Neurosci 7: 2113-2128, 1987). Using two-photon microscopy and calcium imaging, we show that DA evokes the release of calcium from intracellular stores well before the emergence of voltage oscillations. When this release from intracellular stores is blocked by antagonists of ryanodine or inositol trisphosphate (IP(3)) receptor channels, DA fails to evoke AB bursting. We further demonstrate that DA enhances the calcium-activated inward current, I(CAN), despite the fact that it significantly reduces voltage-activated calcium currents. This suggests that DA-induced release of calcium from intracellular stores activates I(CAN), which provides a depolarizing ramp current that underlies endogenous bursting in the AB neuron.

Publication types

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

MeSH terms

  • Animals
  • Biological Clocks / drug effects
  • Biological Clocks / physiology*
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Dopamine / pharmacology
  • Dopamine / physiology*
  • Evoked Potentials / drug effects
  • Evoked Potentials / physiology
  • Intracellular Fluid / drug effects
  • Intracellular Fluid / metabolism*
  • Neurons / drug effects
  • Neurons / metabolism*
  • Palinuridae
  • Pylorus / drug effects
  • Pylorus / metabolism*

Substances

  • Dopamine