Topographic Representation of Odorant Molecular Features in the Rat Olfactory Bulb

2004 ◽  
Vol 92 (4) ◽  
pp. 2413-2427 ◽  
Author(s):  
Yuji K. Takahashi ◽  
Masahide Kurosaki ◽  
Shuichi Hirono ◽  
Kensaku Mori

Individual glomeruli in the mammalian olfactory bulb (OB) most probably represent a single odorant receptor (OR). The assembly of glomeruli thus forms the maps of ORs. How is the approximately 1,000 ORs represented spatially in the glomerular map? Using the method of optical imaging of intrinsic signals and systematic panels of stimulus odorants, we recorded odorant-induced glomerular activity from the dorsal and dorsolateral areas of the rat OB, and examined the molecular receptive range (MRR) of individual glomeruli. We then deduced the characteristic molecular features that were shared by odorants effective in activating individual glomeruli. Analysis of the spatial representation of the MRR showed that glomeruli with similar MRRs gathered in close proximity and formed molecular feature clusters and subclusters. Although the shape of the clusters varied among different OBs, the clusters were arranged at stereotypical positions in relation to the zonal organization of the OB. Examination of the spatial representation of the characteristic molecular features of odorants using structurally semirigid aromatic compounds suggest a systematic and gradual change in the characteristic molecular features according to the position of subclusters in the map. The topographic map of the characteristic molecular features may reflect a systematic spatial representation of the ORs and may participate in the neural bases for the odorant structure–odor quality relationship.

2006 ◽  
Vol 86 (2) ◽  
pp. 409-433 ◽  
Author(s):  
Kensaku Mori ◽  
Yuji K. Takahashi ◽  
Kei M. Igarashi ◽  
Masahiro Yamaguchi

The olfactory bulb (OB) is the first relay station of the central olfactory system in the mammalian brain and contains a few thousand glomeruli on its surface. Because individual glomeruli represent a single odorant receptor, the glomerular sheet of the OB forms odorant receptor maps. This review summarizes the emerging view of the spatial organization of the odorant receptor maps. Recent studies suggest that individual odorant receptors are molecular-feature detecting units, and so are individual glomeruli in the OB. How are the molecular-feature detecting units spatially arranged in the glomerular sheet? To characterize the molecular-feature specificity of an individual glomerulus, it is necessary to determine the molecular receptive range (MRR) of the glomerulus and to compare the molecular structure of odorants within the MRR. Studies of the MRR mapping show that 1) individual glomeruli typically respond to a range of odorants that share a specific combination of molecular features, 2) each glomerulus appears to be unique in its MRR property, and 3) glomeruli with similar MRR properties gather together in proximity and form molecular-feature clusters. The molecular-feature clusters are located at stereotypical positions in the OB and might be part of the neural representation of basic odor quality. Detailed studies suggest that the glomerular sheet represents the characteristic molecular features in a systematic, gradual, and multidimensional fashion. The molecular-feature maps provide a basis for understanding how the olfactory cortex reads the odor maps of the OB.


2005 ◽  
Vol 93 (2) ◽  
pp. 1007-1019 ◽  
Author(s):  
Kei M. Igarashi ◽  
Kensaku Mori

The glomerular sheet of the olfactory bulb (OB) forms odorant receptor maps that are parceled into zones. We previously reported the molecular receptive range (MRR) property of individual glomeruli in the dorsal zone (zone 1) of the OB and showed that polar functional groups play a major role in activating glomeruli in this zone. However, the MRR property of glomeruli in zones 2–4 is not well understood yet. Using the method of intrinsic signal imaging, we recorded odorant-induced glomerular activity from the ventrolateral surface (zones 2–4) of rat OB. While hydrocarbon odorants that lack polar functional groups activate only a few glomeruli in zone 1, we found that a series of hydrocarbon odorants consistently activated many glomeruli in the ventrolateral surface. The hydrocarbon-responsive glomeruli were grouped into two clusters; glomeruli in one cluster (cluster H) responded to benzene-family hydrocarbons but not to cyclic terpene hydrocarbons. Glomeruli in the other cluster (cluster I) responded to both classes of hydrocarbons. Detailed analyses of MRR properties of individual glomeruli using hydrocarbon odorants and polar-functional-group-containing odorants showed that the common and characteristic molecular features effective in activating glomeruli in the clusters H and I are the hydrocarbon skeleton. These results suggest that ORs represented by glomeruli in these clusters recognize primarily the hydrocarbon skeleton of odorants, and thus imply a systematic difference in the manner of recognizing odorant molecular features between ORs in zone 1 and ORs in zones 2–4.


2010 ◽  
Vol 103 (6) ◽  
pp. 3490-3500 ◽  
Author(s):  
Hideyuki Matsumoto ◽  
Ko Kobayakawa ◽  
Reiko Kobayakawa ◽  
Takuya Tashiro ◽  
Kenji Mori ◽  
...  

The glomerular layer of the mammalian olfactory bulb (OB) forms odorant receptor (OR) maps. Each OR map is structurally and functionally compartmentalized into zones (dorsal and ventral) and domains (DI and DII in the dorsal zone). We previously reported that glomeruli with similar molecular receptive range properties formed molecular feature clusters at stereotypical positions in the rat OB. However, the spatial arrangement of the molecular feature clusters with regard to the OR zones and domains has not been systematically examined. In this study, we optically mapped the molecular feature clusters of glomeruli within the domain and zone framework of the OB using domain-visible class II GFP transgenic mice. In all mice examined, fatty acid-responsive cluster A was located in the lateral part of domain DI, whereas clusters B, C, and D were arranged in an anterior to posterior order within domain DII. We also found a new cluster of glomeruli that respond to fox odor trimethyl-thiazoline and its structural analogs (heterocyclic odorants that contain sulfur and nitrogen atoms within the ring). This cluster (named cluster J) was located posterior to cluster D within the DII domain. These results show that molecular feature clusters correspond to specific subsets of glomeruli in selective domains of the OR map, suggesting that the molecular feature clusters represent specific ORs that have similar molecular receptive range properties and functional roles.


2003 ◽  
Vol 31 (1) ◽  
pp. 134-136 ◽  
Author(s):  
K. Mori

The olfactory system is unique in that the sensory input is in the form of molecular information carried in a vast variety of odorants. Nearly 1000 types of odorant receptors mediate the initial detection and discrimination of odorants at the molecular-feature level. The discrimination at the molecular level is converted into that at the cellular level (olfactory sensory neurons) by the one sensory neuron–one odorant receptor rule, and then into that at the neuronal circuit level in the olfactory bulb by the specific olfactory axon connectivity pattern. Individual glomeruli in the olfactory bulb represent a single odorant receptor, and the glomerular sheet at the olfactory bulb surface forms odorant receptor maps. This review focuses on the spatial organization of the glomerular sensory map in the olfactory bulb. The analysis using the optical imaging method suggests that odorant receptors having a common molecular-feature receptive site are grouped together and represented by glomeruli that are localized in topographically fixed domains in the olfactory bulb. The domain organization may be a structural unit for the spatial organization of the glomerular sensory map, and might relate to the olfactory submodality.


Neuron ◽  
2002 ◽  
Vol 35 (4) ◽  
pp. 681-696 ◽  
Author(s):  
Anne Vassalli ◽  
Andrea Rothman ◽  
Paul Feinstein ◽  
Martin Zapotocky ◽  
Peter Mombaerts

Author(s):  
Richard P. Tucker ◽  
Qizhi Gong

Animals use their olfactory system for the procurement of food, the detection of danger, and the identification of potential mates. In vertebrates, the olfactory sensory neuron has a single apical dendrite that is exposed to the environment and a single basal axon that projects to the central nervous system (i.e., the olfactory bulb). The first odorant receptors to be discovered belong to an enormous gene family encoding G protein-coupled seven transmembrane domain proteins. Odorant binding to these classical odorant receptors initiates a GTP-dependent signaling cascade that uses cAMP as a second messenger. Subsequently, additional types of odorant receptors using different signaling pathways have been identified. While most olfactory sensory neurons are found in the olfactory sensory neuroepithelium, others are found in specialized olfactory subsystems. In rodents, the vomeronasal organ contains neurons that recognize pheromones, the septal organ recognizes odorant and mechanical stimuli, and the neurons of the Grüneberg ganglion are sensitive to cool temperatures and certain volatile alarm signals. Within the olfactory sensory neuroepithelium, each sensory neuron expresses a single odorant receptor gene out of the large gene family; the axons of sensory neurons expressing the same odorant receptor typically converge onto a pair of glomeruli at the periphery of the olfactory bulb. This results in the transformation of olfactory information into a spatially organized odortopic map in the olfactory bulb. The axons originating from the vomeronasal organ project to the accessory olfactory bulb, whereas the axons from neurons in the Grüneberg ganglion project to 10 specific glomeruli found in the caudal part of the olfactory bulb. Within a glomerulus, the axons originating from olfactory sensory neurons synapse on the dendrites of olfactory bulb neurons, including mitral and tufted cells. Mitral cells and tufted cells in turn project directly to higher brain centers (e.g., the piriform cortex and olfactory tubercle). The integration of olfactory information in the olfactory cortices and elsewhere in the central nervous system informs and directs animal behavior.


2020 ◽  
Vol 15 ◽  
pp. 263310552092341
Author(s):  
Claudia Lodovichi

A unique feature in the organization of the olfactory system is the dual role of the odorant receptors: they detect odors in the nasal epithelium and they play an instructive role in the convergence of olfactory sensory neuron axons in specific loci, ie, glomeruli, in the olfactory bulb. The dual role is corroborated by the expression of the odorant receptors in 2 specific locations of the olfactory sensory neurons: the cilia that protrude in the nostril, where the odorant receptors interact with odors, and the axon terminal, a suitable location for a potential axon guidance molecule. The mechanism of activation and function of the odorant receptors expressed at the axon terminal remained unknown for almost 20 years. A recent study identified the first putative ligand of the axonal odorant receptors, phosphatidylethanolamine-binding protein1, a molecule expressed in the olfactory bulb. The distinctive mechanisms of activation of the odorant receptors expressed at the opposite locations in sensory neurons, by odors, at the cilia, and by molecules expressed in the olfactory bulb, at the axon terminal, explain the dual role of the odorant receptors and link the specificity of odor perception with its internal representation, in the topographic map.


Author(s):  
Yaniv Cohen ◽  
Emmanuelle Courtiol ◽  
Regina M. Sullivan ◽  
Donald A. Wilson

Odorants, inhaled through the nose or exhaled from the mouth through the nose, bind to receptors on olfactory sensory neurons. Olfactory sensory neurons project in a highly stereotyped fashion into the forebrain to a structure called the olfactory bulb, where odorant-specific spatial patterns of neural activity are evoked. These patterns appear to reflect the molecular features of the inhaled stimulus. The olfactory bulb, in turn, projects to the olfactory cortex, which is composed of multiple sub-units including the anterior olfactory nucleus, the olfactory tubercle, the cortical nucleus of the amygdala, the anterior and posterior piriform cortex, and the lateral entorhinal cortex. Due to differences in olfactory bulb inputs, local circuitry and other factors, each of these cortical sub-regions appears to contribute to different aspects of the overall odor percept. For example, there appears to be some spatial organization of olfactory bulb inputs to the cortical nucleus of the amygdala, and this region may be involved in the expression of innate odor hedonic preferences. In contrast, the olfactory bulb projection to the piriform cortex is highly distributed and not spatially organized, allowing the piriform to function as a combinatorial, associative array, producing the emergence of experience-dependent odor-objects (e.g., strawberry) from the molecular features extracted in the periphery. Thus, the full perceptual experience of an odor requires involvement of a large, highly dynamic cortical network.


2020 ◽  
Vol 83 (1) ◽  
Author(s):  
Kensaku Mori ◽  
Hitoshi Sakano

In mammals, odor information detected by olfactory sensory neurons is converted to a topographic map of activated glomeruli in the olfactory bulb. Mitral cells and tufted cells transmit signals sequentially to the olfactory cortex for behavioral outputs. To elicit innate behavioral responses, odor signals are directly transmitted by distinct subsets of mitral cells from particular functional domains in the olfactory bulb to specific amygdala nuclei. As for the learned decisions, input signals are conveyed by tufted cells as well as by mitral cells to the olfactory cortex. Behavioral scene cells link the odor information to the valence cells in the amygdala to elicit memory-based behavioral responses. Olfactory decision and perception take place in relation to the respiratory cycle. How is the sensory quality imposed on the olfactory inputs for behavioral outputs? How are the two types of odor signals, innate and learned, processed during respiration? Here, we review recent progress on the study of neural circuits involved in decision making in the mouse olfactory system. Expected final online publication date for the Annual Review of Physiology, Volume 83 is February 10, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.


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