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The Journal of Neuroscience, October 15, 1999, 19(20):8808-8817
Presynaptic Inhibition of Primary Olfactory Afferents Mediated by Different Mechanisms in Lobster and Turtle
Matt Wachowiak and Lawrence B. Cohen Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520, and Marine Biological Laboratory, Woods Hole, Massachusetts 02543
Presynaptic regulation of transmission at the first olfactory synapse was investigated by selectively imaging axon terminals of receptor neurons in the lobster olfactory lobe and turtle olfactory bulb. In both species, action potential propagation into axon terminals after olfactory nerve stimulation was measured using voltage-sensitive dyes. In addition, in the turtle, calcium influx into terminals was measured by selectively labeling receptor neurons with dextran-conjugated calcium indicator dyes. In the lobster, application of the inhibitory transmitters GABA or histamine suppressed action potentials in the terminals. The suppression was blocked by picrotoxin and cimetidine, respective antagonists to lobster GABA and histamine receptors. These results suggest that previously characterized GABA and histaminergic interneurons regulate olfactory input by suppressing action potential propagation into axon terminals of olfactory afferents. In contrast, in the turtle olfactory bulb, neither GABA nor dopamine had any effect on receptor cell action potentials as measured with voltage-sensitive dyes. However, calcium influx into axon terminals was reduced by the GABAB agonist baclofen and the dopamine D2 agonist quinpirole, and paired-pulse suppression of calcium influx was reduced by the GABAB antagonist saclofen. These results indicate that in the turtle, GABA and dopamine mediate presynaptic inhibition not by affecting action potentials directly, as in the lobster, but by reducing calcium influx via GABAB and dopamine D2 receptors. Thus, although mediated by different cellular mechanisms, presynaptic regulation of olfactory input to the CNS, via dual synaptic pathways, is a feature common to vertebrates and invertebrates. This inhibition may be important in the processing of olfactory information.
Key words: olfactory bulb; presynaptic inhibition; imaging; voltage-sensitive dye; calcium dye; GABA; dopamine; histamine
Copyright © 1999 Society for Neuroscience 0270-6474/99/19208808-10$05.00/0
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