Inhibition of Na+/K+ ATPase potentiates synaptic transmission in tactile sensory neurons of the leech

Eur J Neurosci. 2007 Jan;25(1):159-67. doi: 10.1111/j.1460-9568.2006.05257.x.

Abstract

Increasing evidence indicates that modulation of Na(+)/K(+) ATPase activity is involved in forms of neuronal and synaptic plasticity. In tactile (T) neurons of the leech Hirudo medicinalis, Na(+)/K(+) ATPase is the main determinant of the afterhyperpolarization (AHP), which characterizes the firing of these mechanosensory neurons. Previously, it has been reported that cAMP (3',5'-cyclic adenosine monophosphate), which mediates the effects of serotonin (5HT) in some forms of learning in the leech, negatively modulates Na(+)/K(+) ATPase activity, thereby reducing the AHP amplitude in T neurons. Here, we show that a transient inhibition of Na(+)/K(+) ATPase can affect the synaptic connection between two ipsilateral T neurons. Bath application of 10 nm dihydroouabain (DHO), an ouabain analogue, causes an increase in the amplitude of the synaptic potential (SP) recorded in the postsynaptic element when a test stimulus is applied in the presynaptic neuron. Iontophoretic injection of cAMP into the presynaptic T neuron also produces an increase of SP. Simulations carried out by using a computational model of the T neuron suggest that a reduction of the pump rate and a consequent depression of the AHP might facilitate the conduction of action potentials to the synaptic terminals. Moreover, nearly intact leeches injected with 10 nm DHO respond with a swimming episode more quickly to an electrical stimulation, which selectively activates T neurons exhibiting sensitization of swimming induction. Collectively, our results show that inhibition of Na(+)/K(+) ATPase is critical for short-term plasticity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal
  • Cyclic AMP / metabolism
  • Electric Stimulation / methods
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • Excitatory Postsynaptic Potentials / radiation effects
  • Ganglia, Invertebrate / cytology
  • In Vitro Techniques
  • Leeches
  • Models, Neurological
  • Movement / drug effects
  • Movement / physiology
  • Movement / radiation effects
  • Neural Inhibition / drug effects
  • Neural Inhibition / physiology*
  • Neurons, Afferent / physiology*
  • Ouabain / analogs & derivatives
  • Ouabain / pharmacology
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / physiology
  • Presynaptic Terminals / radiation effects
  • Reaction Time / drug effects
  • Reaction Time / physiology
  • Reaction Time / radiation effects
  • Skin / innervation
  • Sodium-Potassium-Exchanging ATPase / metabolism*
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology*
  • Touch*

Substances

  • dihydroouabain
  • Ouabain
  • Cyclic AMP
  • Sodium-Potassium-Exchanging ATPase