Acid sensing by the Drosophila olfactory system

Ai, Minrong; Min, Soohong; Grosjean, Yaël; Leblanc, Charlotte; Bell, Rati; Benton, Richard; Suh, Greg S.B.

doi:10.1038/nature09537

Cited by 309 publications

(409 citation statements)

References 25 publications

(47 reference statements)

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“…As shown previously (Ai et al, 2010), IR64a neurons project to two glomeruli, DC4 and DP1m (Fig. 3C).…”

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

confidence: 86%

“…The wild-type strain for the electrophysiological screen was the genome-sequenced strain (Bloomington Stock Center stock number 2057) (Adams et al, 2000) and an isogenized w 1118 strain for the behavioral experiments. We used the following mutant and transgenic strains: IR8a 1 , IR8a-GAL4, IR25a-GAL4 (Abuin et al, 2011), IR25a 2 (Benton et al, 2009), Orco 1 (formerly OR83b 1 ) (Larsson et al, 2004), OR35a f02057 (Yao et al, 2005), IR64a-GAL4 (Ai et al, 2010), IR76a-GAL4 (Benton et al, 2009), OR35a-GAL4 (Fishilevich and Vosshall, 2005), GR28b.d-GAL4 (Thorne and Amrein, 2008), UASnls:GFP (Sachse et al, 2007), UAS-mCD8:GFP (Lee and Luo, 1999), UAS-nsyb:GFP (Vosshall et al, 2000), and UAS-DTI (diphtheria toxin) (Han et al, 2000).…”

Section: Methodsmentioning

confidence: 99%

“…Previous analysis of IR OSNs demonstrated that one (IR76a) projects to one glomerulus, whereas another (IR64a), unusually, innervates two glomeruli (Benton et al, 2009;Ai et al, 2010). To determine the global anatomical organization of this olfactory subsystem, we traced the axons of each individual population of IR-expressing OSN class using a GAL4-responsive membranetargeted mCD8:GFP reporter.…”

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

confidence: 99%

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Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

456

749

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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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“…As shown previously (Ai et al, 2010), IR64a neurons project to two glomeruli, DC4 and DP1m (Fig. 3C).…”

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

confidence: 86%

Section: Methodsmentioning

confidence: 99%

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

confidence: 99%

See 1 more Smart Citation

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Silbering¹,

Rytz²,

Grosjean³

et al. 2011

J. Neurosci.

456

749

View full text Add to dashboard Cite

show abstract

“…Later work showed that avoidance of higher CO 2 concentration requires an additional, functionally segregated population of olfactory receptor neurons that likely detect CO 2 -induced acidosis (71). However, flies also can exhibit behavioral attraction to CO 2 mediated by the gustatory system (72), suggesting different behaviors can be generated in different contexts by using different modes of sensory detection.…”

Section: Resultsmentioning

confidence: 99%

Environmental CO ₂ inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

Fenk

Bono

2015

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

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Carbon dioxide (CO 2 ) gradients are ubiquitous and provide animals with information about their environment, such as the potential presence of prey or predators. The nematode Caenorhabditis elegans avoids elevated CO 2 , and previous work identified three neuron pairs called "BAG," "AFD," and "ASE" that respond to CO 2 stimuli. Using in vivo Ca 2+ imaging and behavioral analysis, we show that C. elegans can detect CO 2 independently of these sensory pathways. Many of the C. elegans sensory neurons we examined, including the AWC olfactory neurons, the ASJ and ASK gustatory neurons, and the ASH and ADL nociceptors, respond to a rise in CO 2 with a rise in Ca 2+ . In contrast, glial sheath cells harboring the sensory endings of C. elegans' major chemosensory neurons exhibit strong and sustained decreases in Ca 2+ in response to high CO 2 . Some of these CO 2 responses appear to be cell intrinsic. Worms therefore may couple detection of CO 2 to that of other cues at the earliest stages of sensory processing. We show that C. elegans persistently suppresses oviposition at high CO 2 . Hermaphrodite-specific neurons (HSNs), the executive neurons driving egg-laying, are tonically inhibited when CO 2 is elevated. CO 2 modulates the egg-laying system partly through the AWC olfactory neurons: High CO 2 tonically activates AWC by a cGMP-dependent mechanism, and AWC output inhibits the HSNs. Our work shows that CO 2 is a more complex sensory cue for C. elegans than previously thought, both in terms of behavior and neural circuitry.neural circuit | behavioral choice | olfactory system | oviposition | glia M ost living matter creates temporal or spatial gradients of carbon dioxide (CO 2 ). Animals across phylogeny use such gradients to help detect food, conspecifics, or predators (1, 2). The ubiquity of CO 2 suggests that the ecologically relevant information it communicates will depend on the dynamics of the CO 2 stimulus and on context. CO 2 -responsive excitable cells have been identified in mammals (3), arthropods (4), and nematodes (5, 6). However, the number of CO 2 -responsive neurons that are functional in vivo, how they are embedded in neural circuits, and how they shape behavior is unclear.CO 2 crosses membranes readily and dissolves to generate CO 2 (aq), H + , and HCO 3 − . Many proteins whose activity is modified by CO 2 or its solvation products have been identified. pH changes can modulate G protein-coupled receptors (7), Ca 2+ -activated K + channels (8), inwardly rectifying K + channels (9), two pore domain K + channels (10), transient receptor potential (TRP) channels (11, 12), acid-sensing ion channels (ASICs) (13,14), and Pyk2 and ErbB1/2 kinases (15). HCO 3 − modulates soluble adenylate cyclase (16) and transmembrane guanylate cyclases (17); and CO 2 (aq) has been proposed to regulate transmembrane guanylate cyclases (18) and connexin 26 (19) directly. Cells expressing any of these proteins potentially could transduce changes in CO 2 /H + , raising the question: Do animals use a few specific sensory channe...

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“…Because CO 2 works in both gas and dissolved forms (converted to H + and HCO 3 -), it evokes diverse responses in different tissues and cell types [83] . In fruit flies, gaseous CO 2 is detected by TRCs on the antenna whereas dissolved CO 2 is detected by those on the proboscis [84][85][86][87] . It is intriguing to work out how CO 2 activates these receptors.…”

Section: Acid-sensing Receptors In Sensory System Sour Tastementioning

confidence: 99%

Proton production, regulation and pathophysiological roles in the mammalian brain

Zeng

2012

Neurosci. Bull.

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Abstract:The recent demonstration of proton signaling in C. elegans muscle contraction suggests a novel mechanism for proton-based intercellular communication and has stimulated enthusiasm for exploring proton signaling in higher organisms. Emerging evidence indicates that protons are produced and regulated in localized space and time. Furthermore, identification of proton regulators and sensors in the brain leads to the speculation that proton production and regulation may be of major importance for both physiological and pathological functions ranging from nociception to learning and memory. Extracellular protons may play a role in signal transmission by not only acting on adjacent cells but also affecting the cell from which they were released. In this review, we summarize the upstream and downstream pathways of proton production and regulation in the mammalian brain, with special emphasis on the proton extruders and sensors that are critical in the homeostatic regulation of pH, and discuss their potential roles in proton signaling under normal and pathophysiological conditions.

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Acid sensing by the Drosophila olfactory system

Cited by 309 publications

References 25 publications

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Environmental CO ₂ inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

Proton production, regulation and pathophysiological roles in the mammalian brain

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Acid sensing by the Drosophila olfactory system

Cited by 309 publications

References 25 publications

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Complementary Function and Integrated Wiring of the Evolutionarily DistinctDrosophilaOlfactory Subsystems

Environmental CO 2 inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

Proton production, regulation and pathophysiological roles in the mammalian brain

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Product

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Environmental CO ₂ inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity