Antennal Lobe Processing Correlates to Moth Olfactory Behavior

Abstract

Animals typically perceive their olfactory environment as a complex blend of natural odor cues. In insects, the initial processing of odors occurs in the antennal lobe (AL). Afferent peripheral input from olfactory sensory neurons (OSNs) is modified via mostly inhibitory local interneurons (LNs) and transferred by projection neurons (PNs) to higher brain centers. Here we performed optophysiological studies in the AL of the moth, Manduca sexta, and recorded odor-evoked calcium changes in response to antennal stimulation with five monomolecular host volatiles and their artificial mixture. In a double staining approach, we simultaneously measured OSN network input in concert with PN output across the glomerular array. By comparing odor-evoked activity patterns and response intensities between the two processing levels, we show that host mixtures could generally be predicted from the linear summation of their components at the input of the AL, but output neurons established a unique, nonlinear spatial pattern separate from individual component identities. We then assessed whether particularly high levels of signal modulation correspond to behavioral relevance. One of our mixture components, phenyl acetaldehyde, evoked significant levels of nonlinear input-output modulation in observed spatiotemporal activation patterns that were unique from the other individual odorants tested. This compound also accelerated behavioral activity in subsequent wind tunnel tests, whereas another compound that did not exhibit high levels of modulation also did not affect behavior. These results suggest that the high degree of input-output modulation exhibited by the AL for specific odors can correlate to behavioral output.

Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition

“…OSNs expressing the same receptor, and thus responding to the same set of odorants, converge onto the same glomerulus in the AL (Gao et al, 2000; Vosshall, 2000) as has been demonstrated for Drosophila melanogaster and indirectly also in several moth species (Hansson, 1997). Spatio-temporal patterns of neuronal activity representing sensory input to the AL can be visualized by optical imaging methods (Hansson et al, 2003; Skiri et al, 2004; Carlsson et al, 2005; Silbering and Galizia, 2007) enabling identification of compound- and blend-specific responses in the AL of M. sexta (Hansson et al, 2003; Bisch-Knaden et al, 2012; Kuebler et al, 2012). …”

Natural search algorithms as a bridge between organisms, evolution, and ecology

“…Mapping natural search algorithms onto the MAB framework would constitute a major step toward a quantitative understanding of the similarities and differences between search strategies. Recent studies of the neural and biophysical mechanisms involved in search behavior (6,7,9,10,46,58) provide the quantitative information needed to define such models in a way that respects the constraints on search strategies in real biological systems.…”

“…Mayer and his contemporaries, including Jean-Henri Fabre (2), initiated the study of what is now one of the most heavily investigated search algorithms in nature: the olfactory search strategies of insects. Over a century later, studies of how insects and other animals find odor targets have led to major discoveries about the structure and information contained within chemical plumes (3)(4)(5) and the properties of the nervous system that allow animals to extract and respond to that information in a complex and ever-changing landscape (6)(7)(8)(9)(10)(11).…”

Compound valence is conserved in binary odor mixtures in Drosophila melanogaster

“…Furthermore, olfactory information is significantly modulated by a dense network of local neurons in the first olfactory center of the insect brain, the antennal lobe (AL) (reviewed in Galizia and Rössler, 2010;Masse et al, 2009;Wilson, 2013;Wilson and Mainen, 2006). Nevertheless, physiological odor mixture responses in the AL are qualitatively predictable on the basis of mixture constituent responses in Drosophila (Olsen et al, 2010;Silbering and Galizia, 2007) and other insects (Carlsson et al, 2007;Deisig et al, 2006;Deisig et al, 2010;Fernandez et al, 2009;Joerges et al, 1997;Stierle et al, 2013; but see Anton and Hansson, 1996;Kuebler et al, 2011;Kuebler et al, 2012;Meyer and Galizia, 2012). Therefore, if single OSN class responses are already behaviorally meaningful, the innate hedonic valence of odor mixtures may in fact be predictable on the basis of the valences of mixture constituents.…”