Stimulus-evoked neural oscillations are commonly observed in the brains of many animals, particularly within olfactory systems. How do these oscillations originate, and how are they regulated? In insects, these oscillations are produced in the antennal lobe by the interaction of excitatory projection neurons and inhibitory local interneurons, and are transmitted to Kenyon cells in the mushroom body via axons of the projection neurons. All of these structures have analogs in vertebrates. In the mushroom body, oscillations can be monitored as local field potentials (LFPs). In some species (locusts, for example), odor-evoked oscillation frequency varies only slightly over the course of an odor stimulus and over a wide range of concentrations. However, in the moth Manduca sexta, we found that oscillations induced by lengthy odor presentations (like those encountered during feeding) were initially fast (40 Hz for 1 s) and then rapidly shifted to a much slower rate (10-20 Hz for the remainder of the odor pulse). Shorter odor pulses (<1 s) induced fast oscillations only. This observation provided us the opportunity to explore basic mechanisms underlying stimulus-elicited oscillations: how they originate, and what determines their properties. Our intracellular recordings from projection neurons, local neurons and Kenyon cells together with LFP recordings from the mushroom body revealed that moths employ essentially the same neural mechanism as that characterized in the locust to generate oscillations in the antennal lobe and to influence the fine spike timing of Kenyon cells. However, the rapid change in oscillation properties we observed in the moth provided an opportunity to examine mechanisms underlying the regulation of oscillation frequency. In the moth, a lengthy odor pulse elicits an electroantennogram (EAG) deflection that, over the course of the response, decreases in amplitude;this decrease is a consequence of sensory adaptation in the receptor neurons. We found that oscillation frequency roughly tracked EAG amplitude, suggesting frequency may depend on the intensity of input to the antennal lobe circuitry. Interestingly, the initial oscillation frequency remained invariant over a wide range of odor concentrations, whereas EAG amplitudes varied greatly with concentration. To explore this apparent contradiction, we developed a computational model of the moth antennal lobe. The model mimicked the sharp transition between discrete fast and slow oscillatory states when input intensity gradually decreased. Recruiting additional, but less well-tuned, olfactory receptor neurons to simulate responses to higher concentrations did not affect oscillation frequency. Our recordings from olfactory receptor neurons showed that long odor pulses caused most individual olfactory receptor neurons to rapidly adapt their firing rates;this firing rate change closely matched the time course of the shift in oscillation frequency. Our results suggest that oscillation frequency can shift between two states, dependent upon the varying output intensity of adapting receptors, rather than upon the odor concentration. Our model indicates this is possible if olfactory receptor neurons that are highly tuned for a given odor fire at near saturating rates even when presented with low odor concentrations, with higher concentrations recruiting additional, but less tuned olfactory receptor neurons.
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