Inhibition of Na+/K+ ATPase potentiates synaptic transmission in tactile sensory neurons of the leech.
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.
Scuri
Rossana
R
Department of Biology, General Physiology Unit, University of Pisa, Via S. Zeno, 31, 56127 Pisa, Italy. rscuri@biologia.unipi.it
Lombardo
Paola
P
Cataldo
Enrico
E
Ristori
Chiara
C
Brunelli
Marcello
M
D000818:Animals; D001522:Behavior, Animal; D000242:Cyclic AMP / Q000378:metabolism; D004558:Electric Stimulation / Q000379:methods; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D017952:Ganglia, Invertebrate / Q000166:cytology; D066298:In Vitro Techniques; D007865:Leeches; D008959:Models, Neurological; D009068:Movement / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D009433:Neural Inhibition / Q000187:drug effects / Q000502:physiology*; D009475:Neurons, Afferent / Q000502:physiology*; D010042:Ouabain / Q000031:analogs & derivatives / Q000494:pharmacology; D017729:Presynaptic Terminals / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D011930:Reaction Time / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D012867:Skin / Q000294:innervation; D000254:Sodium-Potassium-Exchanging ATPase / Q000378:metabolism*; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology*; D014110:Touch
C000977:dihydroouabain; D010042:Ouabain; D000242:Cyclic AMP; D000254:Sodium-Potassium-Exchanging ATPase