Abstract
BackgroundAn animal navigating to an unseen odor source must accurately resolve the spatiotemporal distribution of that stimulus in order to express appropriate upwind flight behavior. Intermittency of natural odor plumes, caused by air turbulence, is critically important for many insects, including the hawkmoth, Manduca sexta, for odor-modulated search behavior to an odor source. When a moth's antennae receive intermittent odor stimulation, the projection neurons (PNs) in the primary olfactory centers (the antennal lobes), which are analogous to the olfactory bulbs of vertebrates, generate discrete bursts of action potentials separated by periods of inhibition, suggesting that the PNs may use the binary burst/non-burst neural patterns to resolve and enhance the intermittency of the stimulus encountered in the odor plume.ResultsWe tested this hypothesis first by establishing that bicuculline methiodide reliably and reversibly disrupted the ability of PNs to produce bursting response patterns. Behavioral studies, in turn, demonstrated that after injecting this drug into the antennal lobe at the effective concentration used in the physiological experiments animals could no longer efficiently locate the odor source, even though they had detected the odor signal.ConclusionsOur results establish a direct link between the bursting response pattern of PNs and the odor-tracking behavior of the moth, demonstrating the behavioral significance of resolving the dynamics of a natural odor stimulus in antennal lobe circuits.
Highlights
An animal navigating to an unseen odor source must accurately resolve the spatiotemporal distribution of that stimulus in order to express appropriate upwind flight behavior
Effects of bicuculline on the firing pattern of macroglomerular complex (MGC)-projection neurons (PNs) This study focused on MGC-PNs with dendritic arborizations confined to one of the two main glomeruli of the MGC, the cumulus (C-PNs) or toroid I (T-PNs) [23]
These PNs are readily identifiable through their response specificity and pattern, and were further verified by the electrode location (Materials and methods)
Summary
An animal navigating to an unseen odor source must accurately resolve the spatiotemporal distribution of that stimulus in order to express appropriate upwind flight behavior. Odor molecules released from a source form an odor plume with a dynamic, intermittent structure due to turbulent movement of the fluid [3] Animals navigating in such odor plumes are exposed to intermittent olfactory stimulation, which is further aided by the animal’s movement in the plume [4,5]. Results from further studies in moths and other insects detail a nearly universal strategy for odor-source location, that is, upwind locomotion modulated by moment-to-moment encounter with individual odor filaments, with each encounter resulting in an upwind surge [11,12,13,14] These findings suggest that stimulus intermittency is a critical feature that must be resolved with high fidelity by the insect’s olfactory system
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