J Neurosci. 2011 Sep 21;31(38):13357-75.
Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems.
Silbering AF, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis GS, Benton R.
Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015, Lausanne, Switzerland, Laboratory of Intelligent Systems, Microengineering Department, École Polytechnique Fédérale de Lausanne, CH-1015, Lausanne, Switzerland, and Division of Neurobiology, Medical Research Council Laboratory of Molecular Biology, Cambridge CB2 0QH, United Kingdom.
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.