K+ homeostasis and central pattern generation in the metathoracic ganglion of the locust

J Insect Physiol. 2009 Jul;55(7):599-607. doi: 10.1016/j.jinsphys.2009.03.004. Epub 2009 Mar 26.

Abstract

Stress-induced arrest of ventilatory motor pattern generation is tightly correlated with an abrupt increase in extracellular potassium concentration ([K+]o) within the metathoracic neuropil of the locust, Locusta migratoria. Na+/K+-ATPase inhibition with ouabain elicits repetitive surges of [K+]o that coincide with arrest and recovery of motor activity. Here we show that ouabain induces repetitive [K+]o events in a concentration-dependent manner. 10(-5)M, 10(-4)M, and 10(-3)M ouabain was bath-applied in semi-intact locust preparations. 10(-4)M and 10(-3)M ouabain reliably induced repetitive [K+]o events whereas 10(-5)M ouabain had no significant effect. In comparison to 10(-4)M ouabain, 10(-3)M ouabain increased the number and hastened the time to onset of repetitive [K+]o waves, prolonged [K+]o event duration, increased resting [K+]o, and diminished the absolute value of [K+]o waves. Recovery of motor patterning following [K+]o events was less likely in 10(-3)M ouabain. In addition, we show that K+ channel inhibition using TEA suppressed the onset and decreased the amplitude of ouabain-induced repetitive [K+]o waves. Our results demonstrate that ventilatory circuit function in the locust CNS is dependent on the balance between mechanisms of [K+] accumulation and [K+] clearance. We suggest that with an imbalance in favour of accumulation the system tends towards a bistable state with transitions mediated by positive feedback involving voltage-dependent K+ channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ganglia, Sensory / drug effects
  • Ganglia, Sensory / growth & development
  • Ganglia, Sensory / metabolism
  • Insect Proteins / metabolism
  • Locusta migratoria / drug effects
  • Locusta migratoria / enzymology
  • Locusta migratoria / growth & development*
  • Locusta migratoria / metabolism*
  • Male
  • Neuropil / drug effects
  • Neuropil / metabolism
  • Ouabain / pharmacology
  • Potassium / metabolism*
  • Sodium-Potassium-Exchanging ATPase / metabolism

Substances

  • Insect Proteins
  • Ouabain
  • Sodium-Potassium-Exchanging ATPase
  • Potassium