scholarly journals Odor Coding of Nestmate Recognition in the Eusocial Ant Camponotus floridanus

2019 ◽  
Author(s):  
S.T. Ferguson ◽  
K.Y. Park ◽  
A. Ruff ◽  
I. Bakis ◽  
L.J. Zwiebel

AbstractBackgroundIn eusocial ants, aggressive behaviors require a sophisticated ability to detect and discriminate between chemical signatures such as cuticular hydrocarbons that distinguish nestmate friends from non-nestmate foes. It has been suggested that a mismatch between a chemical signature (label) and the internal, neuronal representation of the colony odor (template) leads to the recognition of and subsequent aggression between non-nestmates. While several studies have demonstrated that ant chemosensory systems, most notably olfaction, are largely responsible for the decoding of these chemical signatures, a definitive demonstration that odorant receptors are responsible for the detection and processing of the pheromonal signals that regulate nestmate recognition has thus far been lacking. To address this, we have developed an aggression-based bioassay incorporating a suite of highly selective odorant receptor modulators to characterize the role of olfaction in nestmate recognition in the formicine ant Camponotus floridanus.ResultsValidation of our aggression-based behavioral assay was carried out by demonstrating an antennal requirement for nestmate recognition. In order to adapt this bioassay for the volatile delivery of Orco modulators, electroantennography was used to show that both a volatilized Orco antagonist (VUANT1) and an Orco agonist (VUAA4) eliminated or otherwise interfered with the electrophysiological responses to the hydrocarbon decane, respectively. Volatilize administration of these compounds to adult workers significantly reduced aggression between non-nestmates without altering aggression levels between nestmates but did not alter aggressive responses towards a mechanical stimulus.ConclusionsOur studies provide direct evidence that the antennae (as olfactory appendages) and odorant receptors (at the molecular level) are necessary for mediating aggression towards non-nestmates. Furthermore, our observations support a hypothesis in which rejection of non-nestmates depends on the precise detection and decoding of chemical signatures present on non-nestmates as opposed to the absence of any information or the active acceptance of familiar signatures. In addition to describing a novel approach to assess olfactory signaling in genetically intractable insect systems, these studies contribute to a long-standing interest in odor coding and the molecular neuroethology of nestmate recognition.

Author(s):  
Smija M. Kurian ◽  
Rafaella G. Naressi ◽  
Diogo Manoel ◽  
Ann-Sophie Barwich ◽  
Bettina Malnic ◽  
...  

AbstractNoses are extremely sophisticated chemical detectors allowing animals to use scents to interpret and navigate their environments. Odor detection starts with the activation of odorant receptors (ORs), expressed in mature olfactory sensory neurons (OSNs) populating the olfactory mucosa. Different odorants, or different concentrations of the same odorant, activate unique ensembles of ORs. This mechanism of combinatorial receptor coding provided a possible explanation as to why different odorants are perceived as having distinct odors. Aided by new technologies, several recent studies have found that antagonist interactions also play an important role in the formation of the combinatorial receptor code. These findings mark the start of a new era in the study of odorant-receptor interactions and add a new level of complexity to odor coding in mammals.


2011 ◽  
Vol 106 (5) ◽  
pp. 2437-2449 ◽  
Author(s):  
Andreas Simon Brandstaetter ◽  
Christoph Johannes Kleineidam

In colonies of eusocial Hymenoptera cooperation is organized through social odors, and particularly ants rely on a sophisticated odor communication system. Neuronal information about odors is represented in spatial activity patterns in the primary olfactory neuropile of the insect brain, the antennal lobe (AL), which is analog to the vertebrate olfactory bulb. The olfactory system is characterized by neuroanatomical compartmentalization, yet the functional significance of this organization is unclear. Using two-photon calcium imaging, we investigated the neuronal representation of multicomponent colony odors, which the ants assess to discriminate friends (nestmates) from foes (nonnestmates). In the carpenter ant Camponotus floridanus, colony odors elicited spatial activity patterns distributed across different AL compartments. Activity patterns in response to nestmate and nonnestmate colony odors were overlapping. This was expected since both consist of the same components at differing ratios. Colony odors change over time and the nervous system has to constantly adjust for this (template reformation). Measured activity patterns were variable, and variability was higher in response to repeated nestmate than to repeated nonnestmate colony odor stimulation. Variable activity patterns may indicate neuronal plasticity within the olfactory system, which is necessary for template reformation. Our results indicate that information about colony odors is processed in parallel in different neuroanatomical compartments, using the computational power of the whole AL network. Parallel processing might be advantageous, allowing reliable discrimination of highly complex social odors.


2020 ◽  
Author(s):  
Smija M. Kurian ◽  
Rafaella G. Naressi ◽  
Diogo Manoel ◽  
Ann-Sophie Barwich ◽  
Bettina Malnic ◽  
...  

Noses are extremely sophisticated chemical detectors allowing animals to use scents to interpret and navigate their environments. Odor detection starts with the activation of odorant receptors (ORs), expressed in mature olfactory sensory neurons (OSNs) populating the olfactory mucosa. Different odorants, or different concentrations of the same odorant, activate unique ensembles of ORs. This mechanism of combinatorial receptor coding provided a possible explanation as to why different odorants are perceived as having distinct odors. Aided by new technologies, several recent studies have found that antagonist interactions also play an important role in the formation of the combinatorial receptor code. These findings mark the start of a new era in the study of odorant-receptor interactions and add a new level of complexity to odor coding in mammals.


2020 ◽  
Vol 223 (2) ◽  
pp. jeb215400 ◽  
Author(s):  
Stephen T. Ferguson ◽  
Kyu Young Park ◽  
Alexandra A. Ruff ◽  
Isaac Bakis ◽  
Laurence J. Zwiebel

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.


2010 ◽  
Vol 191 (3) ◽  
pp. 443-452 ◽  
Author(s):  
Shannon DeMaria ◽  
John Ngai

The olfactory system detects and discriminates myriad chemical structures across a wide range of concentrations. To meet this task, the system utilizes a large family of G protein–coupled receptors—the odorant receptors—which are the chemical sensors underlying the perception of smell. Interestingly, the odorant receptors are also involved in a number of developmental decisions, including the regulation of their own expression and the patterning of the olfactory sensory neurons' synaptic connections in the brain. This review will focus on the diverse roles of the odorant receptor in the function and development of the olfactory system.


2021 ◽  
Author(s):  
Claire A. de March ◽  
Hiroaki Matsunami ◽  
Masashi Abe ◽  
Matthew Cobb ◽  
Kara C. Hoover

AbstractThe largest and rapidly evolving gene family of odorant receptors detect odors to variable degrees due to amino acid sequence and protein structure. Hybridization between humans, Neandertals, and Denisovans implies shared behavior1,2, although some speculate that Neandertals were poor smellers 3,4. We identified genetic and functional variation in humans and extinct lineages in 30 receptors with known function. We show that structural changes in receptor proteins altered odor sensitivity not specificity, indicating a common repertoire across lineages. In humans, variation in receptors may change odor perception or induce odor-specific anosmia 5,6. Variation in sensitivity may reflect local adaptations (e.g., Denisovan sensitivity to honey, Neandertals sensitivity to grass and sulphur). Extinct human lineages had highly conserved receptor genes and proteins. We observe a similar pattern in the Neandertal OR5P3 variant, which produced no response to ∼350 odors. Our data suggest that receptor structure was highly conserved in our closest relatives, but not in living humans. The diversity of geographic adaptations in humans may have produced greater functional variation, increasing our olfactory repertoire and expanding our adaptive capacity 5. Our results provide insight into odorant receptor function and shed light on the olfactory ecology of ancient humans and their extinct relatives. By studying the function of ancient odorant receptor genes, we have been able to get a glimpse of the sensory world of our extinct ancestors and relatives, with some of the variants giving specific insights into potential adaptations shown by these long-dead populations. The functional variability we have identified in the molecular structure of the odorant receptor proteins will aid in the more general problem of understanding the function of odorant receptor proteins and the neurons they are carried by, opening the road to linking receptor function to perception.


2019 ◽  
Author(s):  
Fabio Miazzi ◽  
Carolin Hoyer ◽  
Silke Sachse ◽  
Markus Knaden ◽  
Dieter Wicher ◽  
...  

AbstractInsect odorant receptors show a limited functional expression in various heterologous expression systems including insect and mammalian cells. This may be in part due to the absence of key components driving the release of these proteins from the endoplasmic reticulum and directing them to the plasma membrane. In order to mitigate this problem we took advantage of small export signals within the human HCN1 and Rhodopsin that have been shown to promote protein release from the endoplasmic reticulum and the trafficking of post-Golgi vesicles, respectively. Moreover, we designed a new vector based on a bidirectional expression cassette to drive the functional expression of the insect odorant receptor co-receptor (Orco) and an odor-binding odorant receptor, simultaneously. We show that this new method can be used to reliably express insect odorant receptors in HEK293 cells via transient transfection and that is highly suitable for downstream applications using automated and high-throughput imaging platforms.


Author(s):  
Steve Rodriguez ◽  
Luxiang Cao ◽  
Gregory T. Rickenbacher ◽  
Eric G. Benz ◽  
Colin Magdamo ◽  
...  

Post-infectious anosmias typically follow death of olfactory sensory neurons (OSNs) with a months-long recovery phase associated with parosmias. While profound anosmia is the leading symptom associated with COVID-19 infection, many patients regain olfactory function within days to weeks without distortions. Here, we demonstrate that sterile induction of anti-viral type I interferon signaling in the mouse olfactory epithelium is associated with diminished odor discrimination and reduced odor-evoked local field potentials. RNA levels of all class I, class II, and TAAR odorant receptors are markedly reduced in OSNs in a non-cell autonomous manner. We find that people infected with COVID-19 rate odors with lower intensities and have odor discrimination deficits relative to people that tested negative for COVID-19. Taken together, we propose that inflammatory-mediated loss of odorant receptor expression with preserved circuit integrity accounts for the profound anosmia and rapid recovery of olfactory function without parosmias caused by COVID-19.


Sign in / Sign up

Export Citation Format

Share Document