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First published online May 24, 2005
Journal of Experimental Biology 208, 2135-2145 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01633
Interaction between facilitation and presynaptic inhibition at the crayfish neuromuscular junction
Department of Biology, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada
* Author for correspondence (e-mail: cddemill{at}sfu.ca) at present address: Department of Biology, University of Victoria, PO Box 3020, Station CSC, Victoria, British Columbia, V8W 3N5, Canada
Accepted 15 March 2005
Action potential-mediated calcium (Ca) entry into excitor nerve terminal boutons during presynaptic inhibition and the effects of co-activation of the inhibitor on the kinetics of muscle contraction were studied at crayfish claw opener muscle. Inhibition reduced postsynaptic excitatory junction potentials (EJPs) below the threshold to initiate contraction. Upon cessation of inhibition, EJP amplitudes immediately increased several-fold due to the build-up of presynaptic facilitation during inhibition. Consequently, muscle contraction was initiated more rapidly after a period of inhibitor-excitor coactivation.
Presynaptic inhibition reduced Ca entry into presynaptic excitor terminal boutons (range 0-50%, mean ± S.E.M.=20±1%, N=122 terminals; 12 preparations) and reduced the EJP amplitude (range 30-70%, mean ± S.E.M.=51±2%, N=27 cells). The decline in the EJP was proportional to the reduction of Ca influx raised to the power of 2.8. Since presynaptic inhibition reduces the number of Ca channels opened by an action potential, our data suggest cooperativity between Ca channel microdomains to initiate vesicle fusion at this synapse.
The amount of inhibition of Ca influx into an excitor bouton was not correlated with either the distance to the closest inhibitor bouton or the main excitor branch, although slightly more inhibition was seen for excitor boutons on tertiary versus secondary branches. Unlike inhibitor axon stimulation, bath application of GABA caused inhibition of Ca influx that steadily increased from proximal to distal terminal boutons on a branch. We propose a model where presynaptic inhibition causes localized shunting of an actively propagated action potential in the vicinity of release sites, which can recover its amplitude outside the shunted region.
Key words: calcium imaging, contraction, GABA, Procambarus clarkii