Odorant-induced oscillations in the mushroom bodies of the locust

Abstract

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.

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