Olfactory sensory neurons expressing class I odorant receptors converge their axons on an antero‐dorsal domain of the olfactory bulb in the mouse

Tsuboi, Akito; Miyazaki, T.; Imai, Takeshi; Sakano, Hitoshi

doi:10.1111/j.1460-9568.2006.04675.x

Cited by 91 publications

(75 citation statements)

References 45 publications

(69 reference statements)

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“…Class I and class II ORs are phylogenetically distinct, and their glomeruli are segregated into the DI and DII regions of the dorsal OB, respectively ( Fig. 1 A) (Zhang et al, 2004;Miyamichi et al, 2005;Tsuboi et al, 2006;Kobayakawa et al, 2007;Bozza et al, 2009). Activation of glomeruli in these two regions has been linked to innate avoidance responses to aversive odors, such as those emanating from spoiled food and predator urine (Kobayakawa et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

The Pattern of Glomerular Map Formation Defines Responsiveness to Aversive Odorants in Mice

Cho

Prince²,

Cutforth³

et al. 2011

J. Neurosci.

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In many species, the detection and recognition of odors is critical to regulate behaviors that are essential for survival, such as foraging for food and avoidance of predators. The formation of complex stereotypic connections between olfactory sensory neurons (OSNs) and second-order neurons in the olfactory bulb (OB) is believed to be important for accurate odorant information processing. In mice, ablation of OSNs that innervate the dorsal region of the OB leads to a loss of avoidance behavior in response to aversive and predator odorants (Kobayakawa et al., 2007). It remains to be determined whether the accurate formation of a glomerular map in this region of the OB is required for these innate responses. Here, we have generated mice that lack expression of the axon guidance receptor Robo-2 in OSNs and found that ablation of Robo-2 expression leads to mistargeting of subsets of OSN axons within the dorsal region of the OB. Furthermore, these mice show decreased avoidance behavior toward the predator odorant trimethyl-thiazoline. Our results indicate that the pattern of glomerular innervation in the OB is critical for innate behavioral responses in mice.

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Section: Introductionmentioning

confidence: 99%

The Pattern of Glomerular Map Formation Defines Responsiveness to Aversive Odorants in Mice

Cho

Prince²,

Cutforth³

et al. 2011

J. Neurosci.

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“…The staining of axons indicates a prominent transcytosis in the olfactory sensory neurons (Hocini et al, 2001;Miller et al, 1994). It is tempting to associate such a transcytosis with the essential role of odorant receptors in targeting axonal projection to precise sites in the olfactory bulb Tsuboi et al, 2006;Wang et al, 1998). The participation of odorant receptors in targeting requires transport of these receptors to the axon terminals, and ligand-specific endocytosis may play a part in such processes.…”

Section: Endocytosismentioning

confidence: 99%

Visualizing a set of olfactory sensory neurons responding to a bile salt

Døving

Hansson

Bäckström

et al. 2011

Journal of Experimental Biology

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SUMMARYIn the present study, we exposed the olfactory epithelia of crucian carp, Carassius carassius, and brown trout, Salmo trutta, to dextran coupled with Alexa dyes together with odorants. Dye uptake was severely reduced after pre-exposure to nocodazole, an inhibitor of microtubule polymerization that impairs endocytosis, supporting the hypothesis that odour-activated olfactory receptor molecules undergo endocytosis. Application of the bile acid taurolithocholate, a potent and specific odorant for fish, resulted in the labelling of a sparse (less than 3%) cell population with the typical morphology of ciliated sensory neurons (CSNs) -long dendrites and cell somata deep in the sensory epithelium. The dye was distributed throughout the sensory neuron, also revealing axons and target glomeruli. Stained axons redistribute at the entrance of the olfactory bulb and terminate in two small target areas, a dorsal and a medial one. These results are consistent with the notion that taurolithocholate is detected specifically by a few ciliated sensory neurons. Application of the olfactory epithelium of brown trout to bile acid stained cells with the appearance of CSNs. Application of an alarm agonist, hypxanthine-3-N-oxide, to crucian carp olfactory organ caused staining of another set of sensory neurons. Furthermore, our results show that odour-induced uptake of a dye can serve to identify the subtype of olfactory sensory neurons responding to a particular odorant, and to pinpoint the target regions of these neurons in the olfactory bulb as a first step to elucidating the neuronal network responding to a particular odour.

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“…Although Class I ORs are mostly expressed within the D zone (Zhang et al, 2004;Tsuboi et al, 2006), class II OR genes are expressed in both D and V zones. Within the D zone, class I and class II expressing cells are intermingled and there is no restricted distribution for both classes (Tsuboi et al 2006). In the V zone, however, each class II OR gene possesses its unique expression area, distributed in a continuous and overlapping manner along the dorsomedial -ventrolateral axis in the OE (Miyamichi et al 2005).…”

Section: Spatial Organization Of the Rodent Olfactory Epithelium And mentioning

confidence: 99%

“…1B). Systematic in situ hybridization and genetic labeling indicated that OSNs expressing class I ORs project their axons to the most anterodorsal areas (DI) within the D domain (Tsuboi et al 2006;Kobayakawa et al 2007;Bozza et al 2009). The OR-specific expression area along the dorsomedial-ventrolateral axis of the V zone OE is well correlated with D-V positioning of glomeruli in the OB (Miyamichi et al 2005).…”

Section: Mechanisms Of Olfactory Map Formation In Mammals Topographicmentioning

confidence: 99%

“…The OR genes are divided phylogenetically into two different classes, I and II, based on homology of deduced amino acid sequences (Glusman et al 2001;Zhang and Firestein 2002;Tsuboi et al 2006). Although Class I ORs are mostly expressed within the D zone (Zhang et al, 2004;Tsuboi et al, 2006), class II OR genes are expressed in both D and V zones. Within the D zone, class I and class II expressing cells are intermingled and there is no restricted distribution for both classes (Tsuboi et al 2006).…”

Section: Spatial Organization Of the Rodent Olfactory Epithelium And mentioning

confidence: 99%

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Topographic Mapping--The Olfactory System

Imai¹,

Sakano²,

Vosshall³

2010

Cold Spring Harbor Perspectives in Biology

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Sensory systems must map accurate representations of the external world in the brain. Although the physical senses of touch and vision build topographic representations of the spatial coordinates of the body and the field of view, the chemical sense of olfaction maps discontinuous features of chemical space, comprising an extremely large number of possible odor stimuli. In both mammals and insects, olfactory circuits are wired according to the convergence of axons from sensory neurons expressing the same odorant receptor. Synapses are organized into distinctive spherical neuropils-the olfactory glomeruli-that connect sensory input with output neurons and local modulatory interneurons. Although there is a strong conservation of form in the olfactory maps of mammals and insects, they arise using divergent mechanisms. Olfactory glomeruli provide a unique solution to the problem of mapping discontinuous chemical space onto the brain.T he olfactory system detects airborne organic and inorganic chemicals that originate from plant and animal metabolites and environmental and industrial sources. Odors mediate both innate and learned behaviors such as attraction and aversion, governing decisions to eat, mate, attack or flee from aggressors and predators. A remarkable feature of the olfactory system is the extraordinary diversity of possible odor molecules that exist. Although accurate measurements can be made of the detection range of visual wavelengths or auditory frequencies in humans, there are no reliable estimates of the number of odorous molecules that exist on earth or those that can be detected by a given animal species (Gilbert 2008). Nevertheless, the number of possible odorants is thought to be high, in the range of many thousands. Beyond odor detection lies the problem of odor discrimination: how can chemicals with slightly different physical properties be discriminated and associated with distinct odor percepts?Experiments investigating the molecular logic of olfaction over the last 20 years have led to major insights into how animals solve the problem of detecting and discriminating a vast number of different odor stimuli (Axel 1995). Four organizational principles have emerged from this work. First, large numbers of distinct odorant receptor (OR) genes are dedicated

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Olfactory sensory neurons expressing class I odorant receptors converge their axons on an antero‐dorsal domain of the olfactory bulb in the mouse

Cited by 91 publications

References 45 publications

The Pattern of Glomerular Map Formation Defines Responsiveness to Aversive Odorants in Mice

The Pattern of Glomerular Map Formation Defines Responsiveness to Aversive Odorants in Mice

Visualizing a set of olfactory sensory neurons responding to a bile salt

Topographic Mapping--The Olfactory System

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