- Open Access
Representations of odor plume flux are accentuated deep within the moth brain
© BioMed Central Ltd 2009
- Published: 20 February 2009
Odor space, the representation of odor quality in the insect brain, is known to be optimally resolved when lateral inhibitory pathways are functioning normally. A new study published in the Journal of Biology now shows that odor time resolution also depends on the normal functioning of such pathways.
- Mushroom Body
- Antennal Lobe
- Odor Quality
- Odor Plume
- Upwind Flight
Understanding how insects detect, discriminate, and act upon relevant olfactory stimuli such as pheromones and host odors has been a major challenge for researchers for decades. The 'act upon' part of this challenge involves understanding insects' odor-mediated behavior; that is, how they maneuver when they smell something relevant. Much has been learned over the years about sex-pheromone-mediated flight maneuvers in moths, and much has also been learned about odor discrimination from work on moth sex pheromone systems. The olfactory part of these systems involves the activities of an array of thousands of tightly and differentially tuned olfactory receptor neurons (ORNs) on the male antenna, imbuing it with a distributed specificity of signal acquisition for each of the two or three sex pheromone components in the blend. Acquisition is followed by signal processing by networks of interneurons that form a fine-grained odor quality pattern-recognition system. One part of sex pheromone olfaction thus involves a sampling and reporting of the relative abundances of the different chemicals that comprise the blend and classifying the resulting pattern of neuronal excitation as occupying a certain behaviorally effective position in 'odor space' .
Another, less investigated aspect of pheromone olfaction involves temporal odor resolution, and in a new paper in the Journal of Biology Lei et al.  present findings that illuminate new features of the temporal fine tuning that goes on in moths' pheromone olfactory pathways. Notably, in a rare effort they directly and elegantly link the impairment of inhibitory circuits in the signal-processing network in the moth's antennal lobe with behavioral impairment of upwind flight.
Lei et al. point out that the task for the insect's olfactory system "is to resolve the spatiotemporal dynamics of olfactory stimuli" in an odor plume, and they have focused on the temporal portion. A pheromone odor plume can be envisioned as having been sheared from its emission source as a strong single strand. The strand is then stretched and shredded into myriad sub-strands by turbulence  as it is transported by larger-scale turbulent air masses away from the source along fairly straight lines out into the environment. Because insects' olfactory receptor organs, their sensilla, are directly exposed to wind flowing over them, they are subjected to an odor flux from odor strands and the clean air pockets between strands that usually varies over milliseconds.
The pheromone blend occurs in every strand, and moths discriminate and behaviorally respond to it on a single strand basis, resulting in optimal maneuvering for upwind flight within a couple of hundred milliseconds of a signal being received . The spatial position of the time-averaged plume or its strands relative to the environment has not been shown to be sensed by the olfactory system. So for research on the spatiotemporal dynamics of olfaction, the 'spatio' portion might be viewed as the brain's representation of a particular blend in odor space, not in environmental space.
Flying male moths responding to pheromone do not steer according to the chemical concentration in environmental space. In other words, they do not 'follow their nose'; they follow the wind when their nose tells them to. In insects there is a need for speed in olfaction , and the ORNs are built to be flux detectors rather than concentration analyzers. The key element of ORNs that allows flux detection is a self-cleaning feature provided by the pheromone-binding proteins and degradative enzymes bathing an ORN. Within milliseconds, this gets rid of lingering pheromone molecules after each strand contact and allows the ORNs to disadapt and be able to respond with high fidelity to the next strand.
Lei et al. have now shown that further downstream, in post-synaptic olfactory pathways, inhibitory GABAA-ergic interneurons act to clean up the action-potential activity lingering between strand-induced bursts. These neurons reduce inter-strand action-potential frequency and preserve in the brain a high-fidelity representation of the environmental odor flux that is being reported by the ORNs. The odor-flux peaks of the plume's pheromone strands and the troughs of the clean air pockets are sharpened by the antennal lobe's inhibitory circuitry, and their temporal integrity is kept intact deep within the olfactory system.
I thank Neil Vickers for reading through a penultimate draft of this paper and providing many helpful comments.
- Hallem EA, Carlson JR: Coding of odors by a receptor repertoire. Cell. 2006, 125: 143-160. 10.1016/j.cell.2006.01.050.PubMedView ArticleGoogle Scholar
- Lei H, Riffell JA, Gage SL, Hildebrand JG: Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance. J Biol. 2009, 8: 21-10.1186/jbiol120.PubMedPubMed CentralView ArticleGoogle Scholar
- Murlis J: The structure of odor plumes. Mechanisms in Insect Olfaction. Edited by: Payne TL, Kennedy CEJ, Birch MC. 1986, Oxford: Clarendon Press, 27-39.Google Scholar
- DeBruyne M, Baker TC: Odor detection in insects: Volatile codes. J Chem Ecol. 2008, 34: 882-897. 10.1007/s10886-008-9485-4.View ArticleGoogle Scholar
- Baker TC, Vickers NJ: Pheromone-mediated flight in moths. Pheromone Research: New Directions. Edited by: Cardé RT, Minks AK. 1997, New York: Chapman and Hall, 248-264.View ArticleGoogle Scholar
- Stopfer M, Bhagavan S, Smith BH, Laurent G: Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature. 1997, 390: 70-74. 10.1038/36335.PubMedView ArticleGoogle Scholar
- Wright RH: The olfactory guidance of flying insects. Can Entomol. 1958, 90: 81-89. 10.4039/Ent9081-2.View ArticleGoogle Scholar
- Kennedy JS: Zigzagging and casting as a programmed response to wind-borne odour: a review. Physiol Entomol. 1983, 8: 109-120. 10.1111/j.1365-3032.1983.tb00340.x.View ArticleGoogle Scholar
- Baker TC, Willis MA, Haynes KF, Phelan PL: A pulsed cloud of sex pheromone elicits upwind flight in male moths. Physiol Entomol. 1985, 10: 257-265. 10.1111/j.1365-3032.1985.tb00045.x.View ArticleGoogle Scholar
- Vickers NJ, Baker TC: Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc Natl Acad Sci USA. 1994, 91: 5756-5760. 10.1073/pnas.91.13.5756.PubMedPubMed CentralView ArticleGoogle Scholar
- Lee SG, Carlsson MA, Hansson BS, Todd JL, Baker TC: Antennal lobe projection destinations of Helicoverpa zea male olfactory receptor neurons responsive to heliothine sex pheromone components. J Comp Physiol A. 2006, 192: 351-363. 10.1007/s00359-005-0071-8.View ArticleGoogle Scholar