Innate versus learned odour processing in the mouse olfactory bulb

Kobayakawa, Ko; Kobayakawa, Reiko; Matsumoto, Hideyuki; Oka, Y.; Imai, Takeshi; Ikawa, Masahito; Okabe, Masaru; Ikeda, Toshio; Itohara, Shigeyoshi; Kikusui, Takefumi; Mori, Kensaku; Sakano, Hitoshi

doi:10.1038/nature06281

Cited by 583 publications

(645 citation statements)

References 42 publications

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“…In vitro studies did not identify a high-affinity cadaverine receptor among mouse, rat, or human TAARs (18), although cadaverine reportedly activates TAAR-containing glomeruli in mice at high concentrations (8). Other mammalian TAARs also detect aversive amines; for example, isoamylamine (TAAR3) and 2-phenylethylamine (TAAR4), both likewise produced by decarboxylation of amino acids (16,18,19,32). Indeed, amines are an odor group that is chemically suited both to aquatic and airborne detection.…”

Section: Discussionmentioning

confidence: 99%

High-affinity olfactory receptor for the death-associated odor cadaverine

Hussain

Saraiva

Ferrero

et al. 2013

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

172

234

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Carrion smell is strongly repugnant to humans and triggers distinct innate behaviors in many other species. This smell is mainly carried by two small aliphatic diamines, putrescine and cadaverine, which are generated by bacterial decarboxylation of the basic amino acids ornithine and lysine. Depending on the species, these diamines may also serve as feeding attractants, oviposition attractants, or social cues. Behavioral responses to diamines have not been investigated in zebrafish, a powerful model system for studying vertebrate olfaction. Furthermore, olfactory receptors that detect cadaverine and putrescine have not been identified in any species so far. Here, we show robust olfactory-mediated avoidance behavior of zebrafish to cadaverine and related diamines, and concomitant activation of sparse olfactory sensory neurons by these diamines. The large majority of neurons activated by low concentrations of cadaverine expresses a particular olfactory receptor, trace amineassociated receptor 13c (TAAR13c). Structure-activity analysis indicates TAAR13c to be a general diamine sensor, with pronounced selectivity for odd chains of medium length. This receptor can also be activated by decaying fish extracts, a physiologically relevant source of diamines. The identification of a sensitive zebrafish olfactory receptor for these diamines provides a molecular basis for studying neural circuits connecting sensation, perception, and innate behavior.Danio rerio | aversion | heterologous expression | polyamines C adaverine, putrescine, and other biogenic diamines are strongly repulsive odors to humans, for whom these odors presumably signal bacterial contamination. It may be expected that animal species feeding on carcasses attribute a more positive valence to diamines, and indeed both putrescine and cadaverine have been reported to be feeding attractants for rats (1) as well as goldfish (2). Similarly, insects depositing their eggs in carcasses or other proteineacous materials are attracted by these diamines (3). Beyond signaling danger or food, putrescine and cadaverine also serve as social cues in several vertebrate species, both for marking of territories-for example, in feline species (4)-and for burial of conspecifics (5).Very little is known about the molecular and cellular basis of cadaverine-driven behaviors. Cadaverine and putrescine evoke electrophysiological responses in the olfactory epithelium of two fish species (2, 6) and cadaverine-responsive olfactory sensory neurons and glomeruli have been identified in the mouse (7,8). However, chemosensory receptors that detect cadaverine or related diamines are unknown in any species, and could provide valuable tools to study how the olfactory system mediates innate aversion or attraction.Here, we show that cadaverine is a major product of zebrafish tissue decay, activates a zebrafish olfactory receptor (trace amineassociated receptor 13c, TAAR13c) with high affinity, and elicits a strong, low-threshold, and olfactory-mediated avoidance response in zebrafish. In vivo me...

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Section: Discussionmentioning

confidence: 99%

High-affinity olfactory receptor for the death-associated odor cadaverine

Hussain

Saraiva

Ferrero

et al. 2013

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

172

234

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“…Dorsoventral organization within the olfactory epithelium plays an essential role in odorant receptor choice as well as in guiding topographic projections of ORN axons to the olfactory bulb (Miyamichi et al, 2005;Imai and Sakano, 2007). At a functional level, olfactory neurons of the dorsomedial epithelium mediate innate responses to odors, whereas the ventrolateral epithelium appears to subserve learned, perceptual functions Kobayakawa et al, 2007). However, the mechanisms that establish regionalization within the olfactory epithelium are mostly unknown.…”

Section: Regional Identity In the Olfactory Epitheliummentioning

confidence: 99%

Foxg1Is Required for Development of the Vertebrate Olfactory System

Duggan

DeMaria²,

Baudhuin³

et al. 2008

J. Neurosci.

107

102

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Illuminating the molecular identity and regulation of early progenitor cells in the olfactory sensory epithelium represents an important challenge in the field of neural development. We show in both mouse and zebrafish that the winged helix transcription factor Foxg1 is expressed in an early progenitor population of the olfactory placode. In the mouse, Foxg1 is first expressed throughout the olfactory placode but later becomes restricted to the ventrolateral olfactory epithelium. The essential role of Foxg1 in olfactory development is demonstrated by the strikingly severe phenotype of Foxg1 knock-out mice: older embryos have no recognizable olfactory structures, including epithelium, bulb, or vomeronasal organs. Initially, a small number of olfactory progenitors are specified but show defects in both proliferation and differentiation. Similarly, antisense RNA knockdown of Foxg1 expression in the zebrafish shows a reduction in the number of neurons and mitotic cells in olfactory rosettes, mirroring the phenotype seen in the mouse Foxg1 null mutant. Using mosaic analysis in the zebrafish, we show that Foxg1 is required cell-autonomously for the production of mature olfactory receptor neurons. Therefore, we identified an evolutionarily conserved requirement for Foxg1 in the development of the vertebrate olfactory system.

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“…In contrast, the anterior olfactory nucleus and the cortical amygdala receive topographic and biased projections from the OB, respectively 9,10 . Thus, a conceptual organization has been proposed in which the secondary olfactory pathway bifurcates to transform odour information into stereotyped and random representations, features suited for directing innate and learned behaviours, respectively 12,13 . However, it is not entirely clear how projections of individual output neurons to multiple brain areas are organized, because each of these studies in mice analysed only a small fraction of mitral cells and/or a restricted subset of its target areas.…”

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confidence: 99%

Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling

et al. 2014

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Chemotopic odour representations in the olfactory bulb are transferred to multiple forebrain areas and translated into appropriate output responses. However, a comprehensive projection map of bulbar output neurons at single-axon resolution is lacking in vertebrates. Here we unravel a projectome of the zebrafish olfactory bulb through genetic single-neuron tracing and image registration. We show that five major target regions receive distinct modes of projections from olfactory bulb glomeruli. The central portion of posterior telencephalon receives non-selective, interspersed inputs from all glomeruli, whereas the ventral telencephalon is diffusely innervated by axons from particular glomerular clusters. The right habenula and posterior tuberculum (diencephalic nuclei) receive convergent inputs from restricted and all glomerular clusters, respectively. The bulbar recurrent projections are coarsely topographic. Thus, the primary chemotopic organization is transformed into distinct sensory representations in higher olfactory centres. These findings provide a framework to understand general principles as well as species-specific features in decoding of odour information.

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Innate versus learned odour processing in the mouse olfactory bulb

Cited by 583 publications

References 42 publications

High-affinity olfactory receptor for the death-associated odor cadaverine

High-affinity olfactory receptor for the death-associated odor cadaverine

Foxg1Is Required for Development of the Vertebrate Olfactory System

Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling

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