Parallel Olfactory Systems in Insects: Anatomy and Function

Galizia, C. Giovanni; Rößler, Wolfgang

doi:10.1146/annurev-ento-112408-085442

Cited by 293 publications

(325 citation statements)

References 121 publications

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“…C, Summed responses of OR (magenta) (Hallem and Carlson, 2006) and IR (green) OSNs to a set of odors common to both studies. Odor names are color coded by functional group as in present in the antennal lobes of honeybees (T4 glomeruli), cockroaches (T10 glomeruli), and ants (T7 glomeruli) (Zube et al, 2008;Nishino et al, 2009;Galizia and Rössler, 2010;Watanabe et al, 2010).…”

Section: Peripheral and Central Spatial Maps Of Ir Olfactory Sensory mentioning

confidence: 99%

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

448

739

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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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Section: Peripheral and Central Spatial Maps Of Ir Olfactory Sensory mentioning

confidence: 99%

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

448

739

View full text Add to dashboard Cite

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“…Several hundred projection neurons (PNs), with dendrites in one or more olfactory glomeruli, send axons to calyces and the lateral horn (l ho) (e.g. Malun et al, 1993;Tanaka et al, 2004;Galizia and Rössler, 2010). Extrinsic neurons, which have dendrites in specific layers of the MB lobes, are known to exhibit multimodal responses to various sensory stimuli (Schildberger, 1984;Strausfeld, 1997, 1999;Mizunami et al, 1998c;Okada et al, 1999), which suggests that sensory signals other than olfaction are delivered to the MB.…”

Section: Introductionmentioning

confidence: 99%

Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach

Nishino

Iwasaki

Yasuyama

et al. 2012

Arthropod Structure & Development

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The cockroach Periplaneta americana is an evolutionary basal neopteran insect, equipped with one of the largest and most elaborate mushroom bodies among insects.Using intracellular recording and staining in the protocerebrum, we discovered two new types of neurons that receive direct input from the optic lobe in addition to the neuron previously reported. These neurons have dendritic processes in the optic lobe, projection sites in the optic tracts, and send axonal terminals almost exclusively to the innermost layer of the MB calyces (input site of MB). Their responses were excitatory to visual but inhibitory to olfactory stimuli, and weak excitation occurred in response to mechanosensory stimuli to cerci. In contrast, interneurons with dendrites mainly in the antennal lobe projection sites send axon terminals to the middle to outer layers of the calyces. These were excited by various olfactory stimuli and mechanosensory stimuli to the antenna. These results suggest that there is general modality specific terminal segregation in the MB calyces and that this is an early event in insect evolution. Possible postsynaptic and presynaptic elements of these neurons are discussed.

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“…Communication is important to a broad range of organisms, yet relatively little is known about the genetic components of communication systems and how they evolve. A particularly interesting question in the field is how social signals are perceived and what sort of genetic and physiological specializations facilitate signal perception in highly social organisms (4,5). In the most tractable sociogenomic models, the eusocial hymenopteran insects, communication is largely chemical, and the genetics and physiology of chemosensation in these species may hold the key to understanding their advanced communication (4,6,74).…”

mentioning

confidence: 99%

“…Extensive work has investigated the higher level olfactory brain centers of bees, wasps, and ants, finding specializations in olfactory processing that are potentially linked to social communication (5). At the level of peripheral detection, several studies in ants (Hymenoptera: Formicidae) have identified sensilla types that respond to specific types of pheromones.…”

mentioning

confidence: 99%

Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication

McKenzie

Fetter-Pruneda

Ruta

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

112

175

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A major aim of sociogenomic research is to uncover common principles in the molecular evolution of sociality. This endeavor has been hampered by the small number of specific genes currently known to function in social behavior. Here we provide several lines of evidence suggesting that ants have evolved a large and novel clade of odorant receptor (OR) genes to perceive hydrocarbonbased pheromones, arguably the most important signals in ant communication. This genomic expansion is also mirrored in the ant brain via a corresponding expansion of a specific cluster of glomeruli in the antennal lobe. We show that in the clonal raider ant, hydrocarbon-sensitive basiconic sensilla are found only on the ventral surface of the female antennal club. Correspondingly, nearly all genes in a clade of 180 ORs within the 9-exon subfamily of ORs are expressed exclusively in females and are highly enriched in expression in the ventral half of the antennal club. Furthermore, we found that across species and sexes, the number of 9-exon ORs expressed in antennae is tightly correlated with the number of glomeruli in the antennal lobe region innervated by odorant receptor neurons from basiconic sensilla. Evolutionary analyses show that this clade underwent a striking gene expansion in the ancestors of all ants and slower but continued expansion in extant ant lineages. This evidence suggests that ants have evolved a large clade of genes to support pheromone perception and that gene duplications have played an important role in the molecular evolution of ant communication.sociogenomics | chemosensation | social evolution | antennal lobe | Formicidae T he field of sociogenomics seeks to understand the molecular basis of sociality, asking how social life evolved and how it is governed at the genomic level (1). A particularly pertinent question in the field is the role of novel genes vs. conserved genes in the evolution and regulation of social behaviors, including communication (2, 3). Communication is important to a broad range of organisms, yet relatively little is known about the genetic components of communication systems and how they evolve. A particularly interesting question in the field is how social signals are perceived and what sort of genetic and physiological specializations facilitate signal perception in highly social organisms (4, 5). In the most tractable sociogenomic models, the eusocial hymenopteran insects, communication is largely chemical, and the genetics and physiology of chemosensation in these species may hold the key to understanding their advanced communication (4,6, 74).Much is already known about the insect chemosensory system in general (8,9). Briefly, chemicals are detected by porous sensory hairs (sensilla) located on chemosensory organs such as the legs, wings, palps, and especially the antennae. The sensilla house the dendrites of olfactory and/or gustatory receptor neurons (ORNs/GRNs) with receptor proteins in the olfactory receptor (OR), the gustatory receptor (GR), or the ionotropic receptor (IR) gene ...

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Parallel Olfactory Systems in Insects: Anatomy and Function

Cited by 293 publications

References 121 publications

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach

Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication

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