Zebrafish crypt neurons project to a single, identified mediodorsal glomerulus

Ahuja, Gaurav; Ivandic, Ivan; Saltürk, Mehmet; Oka, Y.; Nadler, Walter; Korsching, Sigrun I.

doi:10.1038/srep02063

Cited by 64 publications

(87 citation statements)

References 49 publications

(112 reference statements)

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“…In the current study, label application was confined to the medial glomerular region containing the dendrites and cell bodies on the medial projection neurons that extend to the posterior tuberculum (Green et al, 2013) and the retrogradely labelled sensory neurons were restricted to the accessory olfactory organ. The short, rounded shape of these sensory neurons matched the morphology reported by Ren et al (2009), and is similar to crypt cells that project to the lateral margin of the olfactory bulb in lungfish (Gonzalez et al, 2010) and to crypt cells distributed throughout the olfactory epithelium and projecting to dorso-medial glomeruli in the zebrafish olfactory bulb (Gayoso et al, 2012;Ahuja et al, 2013;Biechl et al, 2016).…”

Section: Discussionsupporting

confidence: 74%

Odorant organization in the olfactory bulb of the sea lamprey

Green

Boyes

McFadden

et al. 2017

Journal of Experimental Biology

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Olfactory sensory neurons innervate the olfactory bulb, where responses to different odorants generate a chemotopic map of increased neural activity within different bulbar regions. In this study, insight into the basal pattern of neural organization of the vertebrate olfactory bulb was gained by investigating the lamprey. Retrograde labelling established that lateral and dorsal bulbar territories receive the axons of sensory neurons broadly distributed in the main olfactory epithelium and that the medial region receives sensory neuron input only from neurons projecting from the accessory olfactory organ. The response duration for local field potential recordings was similar in the lateral and dorsal regions, and both were longer than medial responses. All three regions responded to amino acid odorants. The dorsal and medial regions, but not the lateral region, responded to steroids. These findings show evidence for olfactory streams in the sea lamprey olfactory bulb: the lateral region responds to amino acids from sensory input in the main olfactory epithelium, the dorsal region responds to steroids (taurocholic acid and pheromones) and to amino acids from sensory input in the main olfactory epithelium, and the medial bulbar region responds to amino acids and steroids stimulating the accessory olfactory organ. These findings indicate that olfactory subsystems are present at the base of vertebrate evolution and that regionality in the lamprey olfactory bulb has some aspects previously seen in other vertebrate species.

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Section: Discussionsupporting

confidence: 74%

Odorant organization in the olfactory bulb of the sea lamprey

Green

Boyes

McFadden

et al. 2017

Journal of Experimental Biology

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“…Four morphologically and functionally different types of olfactory sensory neurons have been described so far in teleost fishes (37). Of these, crypt neurons can be excluded (38,39), and ciliated neurons appear unlikely (39), which leaves the newly discovered kappe neurons (37) or microvillous neurons (39). The latter possibility would be analogous to the expression of v1r in microvillous neurons.…”

Section: Discussionmentioning

confidence: 99%

ORA1, a Zebrafish Olfactory Receptor Ancestral to All Mammalian V1R Genes, Recognizes 4-Hydroxyphenylacetic Acid, a Putative Reproductive Pheromone

Behrens

Frank

Rawel

et al. 2014

Journal of Biological Chemistry

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Background:No ligands are known for any olfactory receptor of the v1r-related ora gene family. Results: Zebrafish ORA1 recognizes with high sensitivity and specificity 4-hydroxyphenylacetic acid. This compound elicits oviposition behavior. Conclusion: ORA1 was deorphanized with a ligand that may be a reproductive pheromone. Significance: Pheromone reception conceivably might be the ancestral function of the ora/v1r family.

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“…The Western blot was performed as described previously (34). Details are provided in SI Materials and Methods.…”

Section: Methodsmentioning

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.

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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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Zebrafish crypt neurons project to a single, identified mediodorsal glomerulus

Cited by 64 publications

References 49 publications

Odorant organization in the olfactory bulb of the sea lamprey

Odorant organization in the olfactory bulb of the sea lamprey

ORA1, a Zebrafish Olfactory Receptor Ancestral to All Mammalian V1R Genes, Recognizes 4-Hydroxyphenylacetic Acid, a Putative Reproductive Pheromone

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

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