The neurobiology of insect olfaction: Sensory processing in a comparative context

Department of Neuroscience, College of Science, University of Arizona, 1040 East Fourth Street, Tucson, AZ 85721-0077, USA.
Progress in Neurobiology (Impact Factor: 9.99). 09/2011; 95(3):427-47. DOI: 10.1016/j.pneurobio.2011.09.007
Source: PubMed


The simplicity and accessibility of the olfactory systems of insects underlie a body of research essential to understanding not only olfactory function but also general principles of sensory processing. As insect olfactory neurobiology takes advantage of a variety of species separated by millions of years of evolution, the field naturally has yielded some conflicting results. Far from impeding progress, the varieties of insect olfactory systems reflect the various natural histories, adaptations to specific environments, and the roles olfaction plays in the life of the species studied. We review current findings in insect olfactory neurobiology, with special attention to differences among species. We begin by describing the olfactory environments and olfactory-based behaviors of insects, as these form the context in which neurobiological findings are interpreted. Next, we review recent work describing changes in olfactory systems as adaptations to new environments or behaviors promoting speciation. We proceed to discuss variations on the basic anatomy of the antennal (olfactory) lobe of the brain and higher-order olfactory centers. Finally, we describe features of olfactory information processing including gain control, transformation between input and output by operations such as broadening and sharpening of tuning curves, the role of spiking synchrony in the antennal lobe, and the encoding of temporal features of encounters with an odor plume. In each section, we draw connections between particular features of the olfactory neurobiology of a species and the animal's life history. We propose that this perspective is beneficial for insect olfactory neurobiology in particular and sensory neurobiology in general.

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    • "Orthologous ORs are of particular interest since may be tuned to odorants that are behaviorally and ecologically relevant across species (Bohbot et al., 2011). Insect ORs identified so far generally show a low level of sequence conservation between species, ranging from 20 to 40% amino acid identity (Rützler and Zwiebel, 2005; Bohbot et al., 2007; Martin et al., 2011; Engsontia et al., 2014). A striking exception is the OR co-receptor, ORco, which shares 60– 90% amino acid identity across different insect orders (Krieger et al., 2003; Larsson et al., 2004). "
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    ABSTRACT: Odorant receptors (ORs) interface animals with airborne chemical signals. They are under strong selection pressure and are therefore highly divergent in different taxa. Yet, some OR orthologs are highly conserved. These ORs may be tuned to odorants of broad importance, across species boundaries. Two widely distributed lepidopteran herbivores, codling moth Cydia pomonella (Tortricidae) feeding in apples and pears, and the African cotton leafworm Spodoptera littoralis (Noctuidae), a moth feeding on foliage of a wide range of herbaceous plants, both express a receptor ortholog, OR19, which shares 58% amino acid identity and 69% amino acid similarity. Following heterologous expression in the empty neuron system of Drosophila melanogaster, we show by single sensillum recordings that CpomOR19 and SlitOR19 show similar affinity to several substituted indanes. Tests with a series of compounds structurally related to 1-indanone show that 2-methyl-1-indanone, 2-ethyl-1-indanone, 3-methyl-1-indanone, and 1-indanone elicit a strong response from both ORs. A keto group in position 1 is essential for biological activity and so are both rings of the indane skeleton. However, there is an important difference in steric complementary of the indane rings and the receptor. Methyl substituents on the benzene ring largely suppressed the response. On the other hand, alkyl substituents at position 2 and 3 of the five-membered ring increased the response indicating a higher complementarity with the receptor cavity, in both CpomOR19 and SlitOR19. Our results demonstrate a conserved function of an odorant receptor in two moths that are phylogenetically and ecologically distant. It is conceivable that a conserved OR is tuned to signals that are relevant for both species, although their ecological roles are yet unknown. Our finding demonstrates that functional characterization of ORs leads to the discovery of novel semiochemicals that have not yet been found through chemical analysis of odorants from insects and their associated host plants.
    11/2015; 3(53). DOI:10.3389/fevo.2015.00131
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    • " 2008 ; Yamagata et al . , 2009 ; Brandstaetter and Kleineidam , 2011 ; Dacks and Nighorn , 2011 ; Rössler and Zube , 2011 ; Nishikawa et al . , 2012 ; Brill et al . , 2013 ; Carcaud et al . , 2015 ) . In the long run the knowledge gained from these studies might be transferred to insects with different tract layouts ( Galizia and Rössler , 2010 ; Martin et al . , 2011 ) and thus promote a more fundamental understanding of olfactory guided behavior ."
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    ABSTRACT: To rapidly process biologically relevant stimuli, sensory systems have developed a broad variety of coding mechanisms like parallel processing and coincidence detection. Parallel processing (e.g. in the visual system), increases both computational capacity and processing speed by simultaneously coding different aspects of the same stimulus. Coincidence detection is an efficient way to integrate information from different sources. Coincidence has been shown to promote associative learning and memory or stimulus feature detection (e.g. in auditory delay lines). Within the dual olfactory pathway of the honeybee both of these mechanisms might be implemented by uniglomerular projection neurons (PNs) that transfer information from the primary olfactory centers, the antennal lobe (AL), to a multimodal integration center, the mushroom body (MB). PNs from anatomically distinct tracts respond to the same stimulus space, but have different physiological properties, characteristics that are prerequisites for parallel processing of different stimulus aspects. However, the PN pathways also display mirror-imaged like anatomical trajectories that resemble neuronal coincidence detectors as known from auditory delay lines. To investigate temporal processing of olfactory information, we recorded PN odor responses simultaneously from both tracts and measured coincident activity of PNs within and between tracts. Our results show that coincidence levels are different within each of the two tracts. Coincidence also occurs between tracts, but to a minor extent compared to coincidence within tracts. Taken together our findings support the relevance of spike timing in coding of olfactory information (temporal code).
    Frontiers in Physiology 07/2015; 6(208). DOI:10.3389/fphys.2015.00208 · 3.53 Impact Factor
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    • "This is particularly relevant to the coevolution of plant signal generation and insect reception, because parasitoids and predators using volatile signals come from a variety of different taxonomic groups. It may be that there are phylogenetic constraints on the neural architecture of olfactory encoding that prevent some groups from using information in volatile blends or make certain groups' processing systems prone to noise (Martin et al. 2011). One important processing task for an insect is to be able to track an olfactory plume to its source. "
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    ABSTRACT: Noise shapes the efficacy and evolution of biological communication systems. Although examined in auditory and visual communication, the effects of noise on olfactory communication remains poorly known. We propose using information theory as a tool for analyzing noise in one type of olfactory signaling: between plants and insects. Plants and insects are cornerstones of terrestrial ecosystems, and understanding communication between them is crucial to describing the full scope of their interactions and how human-caused disturbances disrupt those interactions. Here, we outline sources of noise affecting parts of the signaling channels between plants and insects: signal generation by plants, transmission through the air, and reception by insects. Sources of noise include environmental variation that affects plant and insect physiologies, as well as turbulence and chemical interference. Information theory provides methods for analyzing chemical communication and hypotheses for how selection might act to reduce noise. © 2015 The Author(s) 2015. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights reserved. For Permissions, please e-mail: [email protected] /* */
    BioScience 05/2015; 65(7). DOI:10.1093/biosci/biv062 · 5.38 Impact Factor
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