Abstract
In aquatic and terrestrial environments, odorants are dispersed by currents that create concentration distributions that are spatially and temporally complex. Animals navigating in a plume must therefore rely upon intermittent, and time-varying information to find the source. Navigation has typically been studied as a spatial information problem, with the aim of movement towards higher mean concentrations. However, this spatial information alone, without information of the temporal dynamics of the plume, is insufficient to explain the accuracy and speed of many animals tracking odors. Recent studies have identified a subpopulation of olfactory receptor neurons (ORNs) that consist of intrinsically rhythmically active ‘bursting’ ORNs (bORNs) in the lobster, Panulirus argus. As a population, bORNs provide a neural mechanism dedicated to encoding the time between odor encounters. Using a numerical simulation of a large-scale plume, the lobster is used as a framework to construct a computer model to examine the utility of intermittency for orienting within a plume. Results show that plume intermittency is reliably detectable when sampling simulated odorants on the order of seconds, and provides the most information when animals search along the plume edge. Both the temporal and spatial variation in intermittency is predictably structured on scales relevant for a searching animal that encodes olfactory information utilizing bORNs, and therefore is suitable and useful as a navigational cue.
Highlights
Most research on olfaction in animals has been devoted to odor detection and discrimination based on highly sensitive detectors that respond to odorant concentration alone[17,18,19,20,21]
While the majority of olfactory receptor neurons (ORN) are canonical, tonically-active ORNs that respond to concentrations of odorants with changes in discharge frequency, some are intrinsically or conditionally rhythmically active ORNs and referred to as ‘bursting’ ORNs. bORNs have been identified across a range of taxa[33,34,35,36,37,38,39,40], and have been well characterized in the olfactory organ of the spiny lobster, Panulirus argus, where they show intrinsic bursts in response to odorants41. bORNs respond to odorants in a phase-dependent manner; i.e., their response depends not just on the concentration of the odorant, and on when the odorant arrives relative to their inherent bursting cycle
Canonical ORNs are known to respond to concentrations within this discrete sample, without memory of the previous time-course of odorant arrival it is currently unknown if canonical ORNs can be used to extract temporal variability of the plume. bORNs it appears, can quantify temporal aspects of the plume without higher-order brain function or memory of the last odorant encounter
Summary
Most research on olfaction in animals has been devoted to odor detection and discrimination based on highly sensitive detectors that respond to odorant concentration alone[17,18,19,20,21]. The temporal and spatial distributions of odor are complex[11,26] and a proper assessment of the parameters used by animals actively undergoing search first requires an understanding of the dynamic odor landscape. This is apparent in the case of crustaceans, and lobsters in particular, which are model aquatic organisms for olfactory search. The effect is that animals can take discrete samples in time of the chemical environment with each flick[29], and may be able to distinguish spatial information of odorants along the antennule length[9]. Infotaxis and stimulus intensity-based decisions are promising as a search strategy, supported by many computational studies and robotic models in air and water, but fail to explain many movements observed in organisms and fall short to match animals searching performance[42,43,44,45]
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