Characterization of rhythmic Ca2+ transients in early embryonic chick motoneurons: Ca2+ sources and effects of altered activation of transmitter receptors

J Neurosci. 2009 Dec 2;29(48):15232-44. doi: 10.1523/JNEUROSCI.3809-09.2009.

Abstract

In the nervous system, spontaneous Ca(2+) transients play important roles in many developmental processes. We previously found that altering the frequency of electrically recorded rhythmic spontaneous bursting episodes in embryonic chick spinal cords differentially perturbed the two main pathfinding decisions made by motoneurons, dorsal-ventral and pool-specific, depending on the sign of the frequency alteration. Here, we characterized the Ca(2+) transients associated with these bursts and showed that at early stages while motoneurons are still migrating and extending axons to the base of the limb bud, they display spontaneous, highly rhythmic, and synchronized Ca(2+) transients. Some precursor cells in the ependymal layer displayed similar transients. T-type Ca(2+) channels and a persistent Na(+) current were essential to initiate spontaneous bursts and associated transients. However, subsequent propagation of activity throughout the cord resulted from network-driven chemical transmission mediated presynaptically by Ca(2+) entry through N-type Ca(2+) channels and postsynaptically by acetylcholine acting on nicotinic receptors. The increased [Ca(2+)](i) during transients depended primarily on L-type and T-type channels with a modest contribution from TRP (transient receptor potential) channels and ryanodine-sensitive internal stores. Significantly, the drugs used previously to produce pathfinding errors altered transient frequency but not duration or amplitude. These observations imply that different transient frequencies may differentially modulate motoneuron pathfinding. However, the duration of the Ca(2+) transients differed significantly between pools, potentially enabling additional distinct pool-specific downstream signaling. Many early events in spinal motor circuit formation are thus potentially sensitive to the rhythmic Ca(2+) transients we have characterized and to any drugs that perturb them.

Publication types

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

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Cell Movement / physiology
  • Chick Embryo
  • Electric Stimulation / methods
  • Embryonic Stem Cells / physiology
  • Estrenes / pharmacology
  • In Vitro Techniques
  • Motor Neurons / metabolism*
  • Neurotransmitter Agents / pharmacology
  • Organic Chemicals / metabolism
  • Patch-Clamp Techniques / methods
  • Periodicity*
  • Phosphodiesterase Inhibitors / pharmacology
  • Presynaptic Terminals / physiology*
  • Pyrrolidinones / pharmacology
  • Receptors, Neurotransmitter / agonists
  • Receptors, Neurotransmitter / antagonists & inhibitors
  • Receptors, Neurotransmitter / physiology*
  • Spinal Cord / cytology
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology

Substances

  • Calcium Channel Blockers
  • Estrenes
  • Neurotransmitter Agents
  • Organic Chemicals
  • Phosphodiesterase Inhibitors
  • Pyrrolidinones
  • Receptors, Neurotransmitter
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • calcium green
  • Calcium