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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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