Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems

Silbering , Ana F.
        . Center for Integrative Genomics, Faculty of Biology and Medicine; Rytz , Raphaël
        . Center for Integrative Genomics, Faculty of Biology and Medicine; Grosjean , Yaël
        INRA
        , Dijon .
         UMR 1324 Centre des Sciences du Goût et de l'Alimentation; Abuin , Liliane
        . Center for Integrative Genomics, Faculty of Biology and Medicine; Ramdya , Pavan
        . Center for Integrative Genomics, Faculty of Biology and MedicineLaboratory of Intelligent Systems, Microengineering Department; Jefferis , Gregory S.X.E.
        . Division of Neurology; Benton , Richard
        . Center for Integrative Genomics, Faculty of Biology and Medicine

Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems

2011

Silbering , Ana F. (Université de Lausanne(Suisse). Center for Integrative Genomics, Faculty of Biology and Medicine) | Rytz , Raphaël (Université de Lausanne(Suisse). Center for Integrative Genomics, Faculty of Biology and Medicine) | Grosjean , Yaël (INRA , Dijon (France). UMR 1324 Centre des Sciences du Goût et de l'Alimentation ) | Abuin , Liliane (Université de Lausanne(Suisse). Center for Integrative Genomics, Faculty of Biology and Medicine) | Ramdya , Pavan (Université de LausanneEcole Polytechnique Fédérale de Lausanne(Suisse). Center for Integrative Genomics, Faculty of Biology and MedicineLaboratory of Intelligent Systems, Microengineering Department) | Jefferis , Gregory S.X.E. (Medical Research Council, Cambridge(Royaume Uni). Division of Neurology) | Benton , Richard (Université de Lausanne(Suisse). Center for Integrative Genomics, Faculty of Biology and Medicine)

To sense myriad environmental odors, animals have evolved multiple, large families of divergent olfactory receptors. How and why distinct receptor repertoires and their associated circuits are functionally and anatomically integrated is essentially unknown. We have addressed these questions through comprehensive comparative analysis of the Drosophila olfactory subsystems that express the ionotropic receptors (IRs) and odorant receptors (ORs). We identify ligands for most IR neuron classes, revealing their specificity for select amines and acids, which complements the broader tuning of ORs for esters and alcohols. IR and OR sensory neurons exhibit glomerular convergence in segregated, although interconnected, zones of the primary olfactory center, but these circuits are extensively interdigitated in higher brain regions. Consistently, behavioral responses to odors arise from an interplay between IR- and OR-dependent pathways. We integrate knowledge on the different phylogenetic and developmental properties of these receptors and circuits to propose models for the functional contributions and evolution of these distinct olfactory subsystems.

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