Different mechanisms promote astrocyte Ca2+ waves and spreading depression in the mouse neocortex

J Neurosci. 2003 Oct 29;23(30):9888-96. doi: 10.1523/JNEUROSCI.23-30-09888.2003.

Abstract

Cortical spreading depression (CSD) is thought to play an important role in different pathological conditions of the human brain. Here we investigated the interaction between CSD and Ca2+ waves within the astrocyte population in slices from mouse neocortex (postnatal days 10-14). After local KCl ejection as a trigger for CSD, we recorded the propagation of Ca2+ increases within a large population of identified astrocytes in synchrony with CSD measured as intrinsic optical signal (IOS) or negative DC-potential shift. The two events spread with 39.2 +/- 3.3 mum/sec until the IOS and negative DC-potential shift decayed after approximately 1 mm. However, the astrocyte Ca2+ wave continued to propagate for up to another 500 microm but with a reduced speed of 18.3 +/- 2.5 microm/sec that is also typical for glial Ca2+ waves in white matter or culture. While blocking CSD using MK-801 (40 microm), an NMDA-receptor antagonist, the astrocyte Ca2+ wave persisted with a reduced speed (13.2 +/- 1.5 microm/sec). The specific gap junction blocker carbenoxolon (100 microm) did not prevent CSD but decelerated the speed (2.9 +/- 0.9 microm/sec) of the astrocyte Ca2+ wave in the periphery of CSD. We also found that interfering with intracellular astrocytic Ca2+ signaling by depletion of internal Ca2+ stores does not affect the spread of the IOS. We conclude that CSD determines the velocity of an accompanying astrocytic Ca2+ response, but the astrocyte Ca2+ wave penetrates a larger territory and by this represents a self-reliant phenomenon with a different mechanism of propagation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Astrocytes / physiology*
  • Calcium / metabolism
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Carbenoxolone / pharmacology
  • Cortical Spreading Depression / drug effects
  • Cortical Spreading Depression / physiology*
  • Dizocilpine Maleate / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Gap Junctions / drug effects
  • Gap Junctions / physiology
  • In Vitro Techniques
  • Mice
  • Mice, Transgenic
  • Neocortex / cytology
  • Neocortex / drug effects
  • Neocortex / physiology*
  • Nerve Net / cytology
  • Nerve Net / drug effects
  • Nerve Net / physiology
  • Neurons / drug effects
  • Neurons / metabolism
  • Patch-Clamp Techniques
  • Time Factors

Substances

  • Excitatory Amino Acid Antagonists
  • Dizocilpine Maleate
  • Carbenoxolone
  • Calcium