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Journal of Neuroscience, Vol 14, 2993-3004, Copyright © 1994 by Society for Neuroscience
Odorant-induced oscillations in the mushroom bodies of the locust
G Laurent and M Naraghi
California Institute of Technology, Biology Division, Pasadena 91125.
Kenyon cells are the intrinsic interneurons of the mushroom bodies in the
insect brain, a center for olfactory and multimodal processing and
associative learning. These neurons are small (3-8 microns soma diameter)
and numerous (340,000 and 400,000 in the bee and cockroach brains,
respectively). In Drosophila, Kenyon cells are the dominant site of
expression of the dunce, DC0, and rutabaga gene products, enzymes in the
cAMP cascade whose absence leads to specific defects in olfactory learning.
In honeybees, the volume of the mushroom body neurophils may depend on the
age or social status of the individual. Although the anatomy of these
neurons has been known for nearly a century, their physiological properties
and the principles of information processing in the circuits that they form
are totally unknown. This article provides a first such characterization.
The activity of Kenyon cells was recorded in vivo from locust brains with
intracellular and local field potential electrodes during olfactory
processing. Kenyon cells had a high input impedance (approximately 1 G
omega at the soma). They produced action potentials upon depolarization,
and consistently showed spike adaptation during long depolarizing current
pulses. They generally displayed a low resting level of spike activity in
the absence of sensory stimulation, despite a large background of
spontaneous synaptic activity, and showed no intrinsic bursting behavior.
Presentation of an airborne odor, but not air alone, to an antenna evoked
spatially coherent field potential oscillations in the ipsilateral mushroom
body, with a frequency of approximately 20 Hz. The frequency of these
oscillations was independent of the nature of the odorant. Short bouts of
oscillations sometimes occurred spontaneously, that is, in the absence of
odorant stimulation. Autocorrelograms of the local field potentials in the
absence of olfactory stimulation revealed small peaks at +/- 50 msec,
suggesting an intrinsic tendency of the mushroom body networks to oscillate
at 20 Hz. Such oscillatory behavior could not be seen from local field
potential recordings in the antennal lobes, and may thus be generated in
the mushroom body, or via feedback interactions with downstream neurons in
the protocerebrum. During the odor-induced oscillations, the membrane
potential of Kenyon cells oscillated around the resting level, under the
influence of excitatory inputs phase- locked to the field activity. Each
phasic wave of depolarization in a Kenyon cell could be amplified by
intrinsic excitable properties of the dendritic membrane, and sometimes led
to one action potential, whose timing was phase-locked to the population
oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)
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