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1 Biology, Boston University, Boston, MA, USA; Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT, USA
2 Biology, Boston University, Boston, MA, USA
3 Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, MD, USA
* To whom correspondence should be addressed. E-mail: dmattw{at}bu.edu.
We investigated the cellular mechanism underlying presynaptic regulation of olfactory receptor neuron (ORN) input to the mouse olfactory bulb using optical imaging techniques that selectively report activity in the ORN presynaptic terminal. First, we loaded ORNs with calcium-sensitive dye and imaged stimulus-evoked calcium influx in a slice preparation. Single olfactory nerve shocks evoked rapid fluorescence increases that were largely blocked by the N-type calcium channel blocker 
-conotoxin GVIA. Paired shocks revealed a long-lasting suppression of calcium influx, with ~ 40% suppression at 400 ms interstimulus intervals and a recovery time constant of ~ 450 ms. Blocking activation of postsynaptic olfactory bulb neurons with APV/CNQX reduced this suppression. The GABAB receptor agonist baclofen inhibited calcium influx, while GABAB antagonists reduced paired-pulse suppression without affecting the response to the conditioning pulse. We also imaged transmitter release directly using a mouse line that expresses synaptopHluorin selectively in ORNs. We found that the relationship between calcium influx and transmitter release was superlinear, and that paired-pulse suppression of transmitter release was reduced, but not eliminated, by APV/CNQX and GABAB antagonists. These results demonstrate that primary olfactory input to the CNS can be presynaptically regulated by GABA-ergic interneurons, and show that a major intracellular pathway for this regulation is via the suppression of calcium influx through N-type calcium channels in the presynaptic terminal. This mechanism is unique among primary sensory afferents.
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