scholarly journals Role of Axonal Odorant Receptors in Olfactory Topography

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):  
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.


Physiology ◽  
2012 ◽  
Vol 27 (4) ◽  
pp. 200-212 ◽  
Author(s):  
Claudia Lodovichi ◽  
Leonardo Belluscio

In mammals, smell is mediated by odorant receptors expressed by sensory neurons in the nose. These specialized receptors are found both on olfactory sensory neurons' cilia and axon terminals. Although the primary function of ciliary odorant receptors is to detect odorants, their axonal role remains unclear but is thought to involve axon guidance. This review discusses findings that show axonal odorant receptors are indeed functional and capable of modulating neural connectivity.


2018 ◽  
Vol 315 (4) ◽  
pp. F870-F879 ◽  
Author(s):  
Nicolas Montalbetti ◽  
James G. Rooney ◽  
Allison L. Marciszyn ◽  
Marcelo D. Carattino

Acid-sensing ion channels (ASICs) are trimeric proton-activated, cation-selective neuronal channels that are considered to play important roles in mechanosensation and nociception. Here we investigated the role of ASIC3, a subunit primarily expressed in sensory neurons, in bladder sensory signaling and function. We found that extracellular acidification evokes a transient increase in current, consistent with the kinetics of activation and desensitization of ASICs, in ~25% of the bladder sensory neurons harvested from both wild-type (WT) and ASIC3 knockout (KO) mice. The absence of ASIC3 increased the magnitude of the peak evoked by extracellular acidification and reduced the rate of decay of the ASIC-like currents. These findings suggest that ASICs are assembled as heteromers and that the absence of ASIC3 alters the composition of these channels in bladder sensory neurons. Consistent with the notion that ASIC3 serves as a proton sensor, 59% of the bladder sensory neurons harvested from WT, but none from ASIC3 KO mice, fired action potentials in response to extracellular acidification. Studies of bladder function revealed that ASIC3 deletion reduces voiding volume and the pressure required to trigger micturition. In summary, our findings indicate that ASIC3 plays a role in the control of bladder function by modulating the response of afferents to filling.


2021 ◽  
Author(s):  
Jane S Huang ◽  
Tenzin Kunkhyen ◽  
Beichen Liu ◽  
Ryan J Muggleton ◽  
Jonathan T Avon ◽  
...  

Postnatal neurogenesis provides an opportunity to understand how newborn neurons functionally integrate into circuits to restore lost function. Newborn olfactory sensory neurons (OSNs) wire into highly organized olfactory bulb (OB) circuits throughout life, enabling lifelong plasticity and regeneration. Immature OSNs can form functional synapses capable of evoking firing in OB projection neurons. However, what contribution, if any, immature OSNs make to odor processing is unknown. Indeed, because immature OSNs can express multiple odorant receptors, any input that they do provide could degrade the odorant selectivity of input to OB glomeruli. Here, we used a combination of in vivo 2-photon calcium imaging, optogenetics, electrophysiology and behavioral assays to show that immature OSNs provide odor input to the OB, where they form monosynaptic connections with excitatory neurons. Importantly, immature OSNs responded as selectively to odorants as mature OSNs. Furthermore, mice successfully performed odor detection tasks using sensory input from immature OSNs alone. Immature OSNs responded more strongly to low odorant concentrations but their responses were less concentration dependent than those of mature OSNs, suggesting that immature and mature OSNs provide distinct odor input streams to each glomerulus. Together, our findings suggest that sensory input mediated by immature OSNs plays a previously unappreciated role in olfactory-guided behavior.


2000 ◽  
Vol 355 (1404) ◽  
pp. 1801-1812 ◽  
Author(s):  
Kensaku Mori ◽  
Harald von Campenhausen ◽  
Yoshihiro Yoshihara

Zonal organization is one of the characteristic features observed in both main and accessory olfactory systems. In the main olfactory system, most of the odorant receptors are classified into four groups according to their zonal expression patterns in the olfactory epithelium. Each group of odorant receptors is expressed by sensory neurons distributed within one of four circumscribed zones. Olfactory sensory neurons in a given zone of the epithelium project their axons to the glomeruli in a corresponding zone of the main olfactory bulb. Glomeruli in the same zone tend to represent similar odorant receptors having similar tuning specificity to odorants. Vomeronasal receptors (or pheromone receptors) are classified into two groups in the accessory olfactory system. Each group of receptors is expressed by vomeronasal sensory neurons in either the apical or basal zone of the vomeronasal epithelium. Sensory neurons in the apical zone project their axons to the rostral zone of the accessory olfactory bulb and form synaptic connections with mitral–tufted cells belonging to the rostral zone. Signals originated from basal zone sensory neurons are sent to mitral–tufted cells in the caudal zone of the accessory olfactory bulb. We discuss functional implications of the zonal organization in both main and accessory olfactory systems.


2021 ◽  
Author(s):  
You Wu ◽  
Xiaocui Xu ◽  
Meijie Qi ◽  
Chuan Chen ◽  
Meiling Zhang ◽  
...  

N6-methyladenosine (m6A) and its regulatory components play critical roles in various developmental processes in mammals(1-5). However, the landscape and function of m6A in the maternal-to-zygotic transition (MZT) remain unclear due to limited materials. Here, by developing an ultralow-input MeRIP-seq method, we revealed the dynamics of the m6A RNA methylome during the MZT process in mice. We found that more than 1/3 maternal decay and 2/3 zygotic mRNAs were modified by m6A. Moreover, m6As are highly enriched in the RNA of transposable elements MTA and MERVL, which are highly expressed in oocytes and 2-cell embryos, respectively. Notably, maternal depletion of Kiaa1429, a component of the m6A methyltransferase complex, leads to a reduced abundance of m6A-marked maternal RNAs, including both genes and MTA, in GV oocytes, indicating m6A-dependent regulation of RNA stability in oocytes. Interestingly, when the writers were depleted, some m6A-marked 2-cell specific RNAs, including Zscan4 and MERVL, appeared normal at the 2-cell stage but failed to be decayed at later stages, suggesting that m6A regulates the clearance of these transcripts. Together, our study uncovered that m6As function in context-specific manners during MZT, which ensures the transcriptome stability of oocytes and regulates the stage specificity of zygotic transcripts after fertilization.


2019 ◽  
Author(s):  
Andrew K. Moran ◽  
Thomas P. Eiting ◽  
Matt Wachowiak

ABSTRACTMitral/tufted (MT) cells of the olfactory bulb (OB) show diverse temporal responses to odorant stimulation that are thought to encode odor information. To understand the role of sensory input dynamics versus OB circuit mechanisms in generating this diversity, we imaged glutamate signaling onto MT cell dendrites in anesthetized and awake mice. We found surprising diversity in the dynamics of these signals, including excitatory, suppressive, and biphasic responses as well as nonlinear changes in glutamate signaling across inhalations. Simultaneous imaging of glutamate and calcium signals from MT cell dendrites revealed highly correlated responses for both signals. Glutamate responses were only weakly impacted by blockade of postsynaptic activity, implicating sensory neurons as a primary source of glutamate signaling onto MT cells. Thus, the dynamics of sensory input alone, rather than emergent features of OB circuits, may account for much of the diversity in MT cell responses that underlies OB odor representations.


Development ◽  
1998 ◽  
Vol 125 (18) ◽  
pp. 3563-3569 ◽  
Author(s):  
N. Grillenzoni ◽  
J. van Helden ◽  
C. Dambly-Chaudiere ◽  
A. Ghysen

Sensory neurons can establish topologically ordered projections in the central nervous system, thereby building an internal representation of the external world. We analyze how this ordering is genetically controlled in Drosophila, using as a model system the neurons that innervate the mechanosensory bristles on the back of the fly (the notum). Sensory neurons innervating the medially located bristles send an axonal branch that crosses the central nervous system midline, defining a ‘medial’ identity, while the ones that innervate the lateral bristles send no such branch, defining a ‘lateral’ identity. We analyze the role of the proneural genes achaete and scute, which are involved in the formation of the medial and lateral bristles, and we show that they have no effect on the ‘medial’ and ‘lateral’ identities of the neurons. We also analyze the role of the prepattern genes araucan and caupolican, two members of the iroquois gene complex which are required for the expression of achaete and scute in the lateral region of the notum, and we show that their expression is responsible for the ‘lateral’ identity of the projection.


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