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.(ABSTRACT TRUNCATED AT 400 WORDS)

Mammalian-like features of sleep structure in zebra finches

“…results are therefore consistent with previous studies of Kcomplexes in reptiles (33) and nonlaminar networks from multiple species displaying increased power in a given frequency range because of network synchronization (34)(35)(36)(37)(38)(39)(40).…”

Coordination of central odor representations through transient, non-oscillatory synchronization of glomerular output neurons

“…Spectral analysis therefore shows that LFP oscillations occur spontaneously, but that an olfactory stimulus greatly increases the spectral power in the resting frequency range with only a small change in the dominant frequency. Furthermore, unlike findings in other studies (3,8,17), in no case during olfactory stimulation did spike trains in the PN and oscillations in the LFP share the same dominant frequency.…”

“…The physiological characteristics of PNs in both male and female moths are distinctly different from those reported in some other insects. For example, PNs in male and female moths do not exhibit slow patterning in their responses to brief olfactory stimuli (3,8,17). Rather, PN responses in the moth are multiphasic (not unlike those observed in some vertebrate mitral͞tufted cells; ref.…”

“…In the insect AL, PN dendrites receive synaptic input exclusively within the olfactory glomeruli and then relay processed information to several sites in the protocerebrum, including the mushroom body (MB) (15, 16). We used similar recording methods to those in earlier studies (3,8,14,17) to analyze the temporal relationships between PN spikes and LFP oscillations at these two processing stages in the moth olfactory pathway. An example of simultaneous intracellular and surface LFP recordings from the same glomerular region of the AL (the male MGC) is shown in Fig. …”

Odors Elicit Three Different Oscillations in the Turtle Olfactory Bulb

“…Since their first discovery in the hedgehog (Adrian, 1942), odor-induced oscillations have been observed across phylogenetically distant species, including locust, (Laurent and Naraghi, 1994), frog (Ottoson, 1959b), turtle (Beuerman, 1975(Beuerman, , 1977, rabbit (Adrian, 1950), and monkey (Hughes and Mazurowski, 1962).…”