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The Journal of Neuroscience, March 24, 2004, 24(12):3023-3030; doi:10.1523/JNEUROSCI.5745-03.2004
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Cellular/Molecular
Sensory Neuron Signaling to the Brain: Properties of Transmitter Release from Olfactory Nerve Terminals
Gabe J. Murphy,
Lindsey L. Glickfeld,
Zev Balsen, and
Jeffry S. Isaacson
Neuroscience Graduate Program and Department of Neuroscience, University of California, San Diego School of Medicine, La Jolla, California 92093-0608
Olfactory receptor neurons (ORNs) convey sensory information directly to the CNS via conventional glutamatergic synaptic contacts in olfactory bulb glomeruli. To better understand the process by which information contained in the odorant-evoked firing of ORNs is transmitted to the brain, we examined the properties of glutamate release from olfactory nerve (ON) terminals in slices of the rat olfactory bulb. We show that marked paired pulse depression is the same in simultaneously recorded periglomerular and tufted neurons, and that this form of short-term plasticity is attributable to a reduction of glutamate release from ON terminals. We used the progressive blockade of NMDA receptor (NMDAR) EPSCs by MK-801 [(5R,10S)-(+)-5-methyl-10,11-dihydro-5H-dibenzo[a,d]cyclohepten-5-10-imine hydrogen maleate] and stationary fluctuation analysis of AMPA receptor (AMPAR) EPSCs to determine the probability of release (Pr) of ON terminals; both approaches indicated that Pr is unusually high ( 0.8). The low-affinity glutamate receptor antagonists  -D-glutamylglycine and L-amino-5-phosphonovaleric acid blocked ON-evoked AMPAR- and NMDAR-mediated EPSCs, respectively, to the same extent under conditions of low and high Pr, suggesting that multivesicular release is not a feature of ON terminals. Although release from most synapses exhibits a highly nonlinear dependence on extracellular Ca2+, we find that the relationship between glutamate release and extracellular Ca2+ at ON terminals is nearly linear. Our results suggest that ON terminals have specialized features that may contribute to the reliable transmission of sensory information from nose to brain.
Key words: MK-801; olfactory bulb; glutamate; release probability; paired pulse depression; calcium; multivesicular release
Received Dec 30, 2003;
revised February 10, 2003;
accepted February 10, 2003.
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|
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|
|
|
|
|
|
|
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|
|
|
|
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|
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|
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|
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