Encoding Olfactory Signals via Multiple Chemosensory Systems

ABSTRACT

Most animals have evolved multiple olfactory systems to detect general odors as well as social cues. The sophistication and interaction of these systems permit precise detection of food, danger, and mates, all crucial elements for survival. In most mammals, the nose contains two well described chemosensory apparatuses (the main olfactory epithelium and the vomeronasal organ), each of which comprises several subtypes of sensory neurons expressing distinct receptors and signal transduction machineries. In many species (e.g., rodents), the nasal cavity also includes two spatially segregated clusters of neurons forming the septal organ of Masera and the Grueneberg ganglion. Results of recent studies suggest that these chemosensory systems perceive diverse but overlapping olfactory cues and that some neurons may even detect the pressure changes carried by the airflow. This review provides an update on how chemosensory neurons transduce chemical (and possibly mechanical) stimuli into electrical signals, and what information each system brings into the brain. Future investigation will focus on the specific ligands that each system detects with a behavioral context and the processing networks that each system involves in the brain. Such studies will lead to a better understanding of how the multiple olfactory systems, acting in concert, offer a complete representation of the chemical world.     

The combined role of the main olfactory and vomeronasal systems in social communication in mammals

The main olfactory and the vomeronasal systems are the two systems by which most vertebrates detect chemosensory cues that mediate social behavior. Much research has focused on how one system or the other is critical for particular behaviors. This has lead to a vision of two distinct and complexly autonomous olfactory systems. A closer look at research over the past 30 years reveals a different picture however. These two seemingly distinct systems are much more integrated than previously thought. One novel set of chemosensory cues in particular (MHC Class I peptide ligands) can show us how both systems are capable of detecting the same chemosensory cues, through different mechanisms yet provide the same general information (genetic individuality). Future research will need to now focus on how two seemingly distinct chemosensory systems together detect pheromones and mediate social behaviors. Do these systems work independently, synergistically or competitively in communicating between individuals of the same species?     

Molecular and cellular organization of insect chemosensory neurons

Animals use their chemosensory systems to detect and discriminate among chemical cues in the environment. Remarkable progress has recently been made in our knowledge of the molecular and cellular basis of chemosensory perception in insects, based largely on studies in Drosophila. This progress has been possible due to the identification of gene families for olfactory and gustatory receptors, the use of electro-physiological recording techniques on sensory neurons, the multitude of genetic manipulations that are available in this species, and insights from several insect model systems. Recent studies show that the superfamily of chemoreceptor proteins represent the essential elements in chemosensory coding, endowing chemosensory neurons with their abilities to respond to specific sets of odorants, tastants or pheromones. Investigating how insects detect chemicals in their environment can show us how receptor protein structures relate to ligand binding, how nervous systems process complex information, and how chemosensory systems and genes evolve.     

The combined role of the main olfactory and vomeronasal systems in social communication in mammals

The main olfactory and the vomeronasal systems are the two systems by which most vertebrates detect chemosensory cues that mediate social behavior. Much research has focused on how one system or the other is critical for particular behaviors. This has lead to a vision of two distinct and complexly autonomous olfactory systems. A closer look at research over the past 30 years reveals a different picture however. These two seemingly distinct systems are much more integrated than previously thought. One novel set of chemosensory cues in particular (MHC Class I peptide ligands) can show us how both systems are capable of detecting the same chemosensory cues, through different mechanisms yet provide the same general information (genetic individuality). Future research will need to now focus on how two seemingly distinct chemosensory systems together detect pheromones and mediate social behaviors. Do these systems work independently, synergistically or competitively in communicating between individuals of the same species?     

Olfactory networks: from sensation to perception

Olfactory networks, comprised of sensory neurons and interneurons, detect and process changes in the chemical environment to drive animal behavior. Recent studies combining genetics with behavioral analyses and imaging in worms, flies and mice have revealed new insights into the mechanisms of olfaction. In this discussion, we focus on three interesting findings. First, sensory neuron responses to odor are modulated by neuropeptides. This modulation might serve to extend the range of responses of the sensory neurons and also to integrate internal state information into the chemosensory circuit. Second, genetic tracing studies in mice and flies have shown that the first layer of connections in chemosensory circuits from olfactory epithelium to the glomeruli are stereotyped, while the subsequent connections to higher order sensory processing regions are not. Distributed connectivity to the higher order sensory processing regions has profound implications for how odors are represented in those regions. Third, recent work has revealed that odors are surprisingly sparsely represented in the piriform cortex. The sparse coding in the higher brain centers implies a much greater role for experience and learning in mediating responses to olfactory cues. Analyzing olfactory network function in various species provides us with fascinating clues about how sensory information is acquired, processed and represented at multiple levels within the nervous system.     

The vomeronasal system in mice: from the nose to the hypothalamus- and back!

The vomeronasal pathway in rodents runs parallel to the main olfactory pathway and mediates responses to different classes of chemosensory stimuli. Both olfactory systems can converge and synergize to control reproductive behaviors and hormonal changes triggered by chemosensory cues. Novel experimental approaches expressing genetic transneuronal tracers in hypothalamic neurons regulating reproduction have set the stage to analyze how chemosensory inputs are integrated in the brain to elicit reproductive behaviors and hormonal changes, and how neuroendocrine status might modulate susceptibility to chemosensory cues.     

The effects of sex on chemosensory communication in a terrestrial salamander (Plethodon shermani)

Although much evidence reveals sexually dimorphic processing of chemosensory cues by the brain, potential sex differences at more peripheral levels of chemoreception are understudied. In plethodontid salamanders, the volume of the vomeronasal organ (VNO) is almost twice as large in males as compared to females, both in absolute and relative size. To determine whether the structural sexual dimorphism in VNO volume is associated with sex differences in other peripheral aspects of chemosensation, we measured sex differences in chemo-investigation and in responsiveness of the VNO to chemosensory cues. Males and females differed in traits influencing stimulus access to VNO chemosensory neurons. Males chemo-investigated (“nose tapped”) neutral substrates and substrates moistened with female body rinses more than did females. Compared to females, males had larger narial structures (cirri) associated with the transfer of substrate-borne chemical cues to the lumen of the VNO. These sex differences in chemo-investigation and narial morphology likely represent important mechanisms for regulating sex differences in chemical communication. In contrast, males and females did not differ in responsiveness of VNO chemosensory neurons to male mental gland extract or female skin secretions. This important result indicates that although males have a substantially larger VNO compared to females, the male VNO was not more responsive to every chemosensory cue that is detected by the VNO. Future studies will determine whether the male VNO is specialized to detect a subset of chemosensory cues, such as female body rinses or female scent marks.     

Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice

In rodents, the nasal cavity contains two separate chemosensory epithelia, the main olfactory epithelium, located in the posterior dorsal aspect of the nasal cavity, and the vomeronasal/accessory olfactory epithelium, located in a capsule in the anterior aspect of the ventral floor of the nasal cavity. Both the main and accessory olfactory systems play a role in detection of biologically relevant odors. The accessory olfactory system has been implicated in response to pheromones, while the main olfactory system is thought to be a general molecular analyzer capable of detecting subtle differences in molecular structure of volatile odorants. However, the role of the two systems in detection of biologically relevant chemical signals appears to be partially overlapping. Thus, while it is clear that the accessory olfactory system is responsive to putative pheromones, the main olfactory system can also respond to some pheromones. Conversely, while the main olfactory system can mediate recognition of differences in genetic makeup by smell, the vomeronasal organ (VNO) also appears to participate in recognition of chemosensory differences between genetically distinct individuals. The most salient feature of our review of the literature is that there are no general rules that allow classification of the accessory olfactory system as a pheromone detector and the main olfactory system as a detector of general odorants. Instead, each behavior must be considered within a specific behavioral context to determine the role of these two chemosensory systems. In each case, one system or the other (or both) participates in a specific behavioral or hormonal response.     

The morphology and ultrastructure of the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus Bleeker (Gobiidae, Teleostei)

We examined the peripheral olfactory organ in newly metamorphosed coral-dwelling gobies, Paragobiodon xanthosomus (SL=5.8mm+/-0.8mm, N=15), by the aid of electron microscopy (scanning and transmission) and light microscopy. Two bilateral olfactory placodes were present in each fish. They were oval-shaped and located medio-ventrally, one in each of the olfactory chambers. Each placode had a continuous cover of cilia. The placode epithelium contained three different types of olfactory receptor neurons: ciliated, microvillous and crypt cells. The latter type was rare. Following a pelagic larval phase, P. xanthosomus settle to the reef and form an obligate association with one species of coral, Seriatopora hystrix. Their well-developed olfactory organs likely enable larvae of P. xanthosomus to detect chemical cues that assist in navigating towards and selecting appropriate coral habitat at settlement. Our findings support past studies showing that the peripheral olfactory organ develops early in coral reef fishes.     

The rodent accessory olfactory system

The accessory olfactory system contributes to the perception of chemical stimuli in the environment. This review summarizes the structure of the accessory olfactory system, the stimuli that activate it, and the responses elicited in the receptor cells and in the brain. The accessory olfactory system consists of a sensory organ, the vomeronasal organ, and its central projection areas: the accessory olfactory bulb, which is connected to the amygdala and hypothalamus, and also to the cortex. In the vomeronasal organ, several receptors—in contrast to the main olfactory receptors—are sensitive to volatile or nonvolatile molecules. In a similar manner to the main olfactory epithelium, the vomeronasal organ is sensitive to common odorants and pheromones. Each accessory olfactory bulb receives input from the ipsilateral vomeronasal organ, but its activity is modulated by centrifugal projections arising from other brain areas. The processing of vomeronasal stimuli in the amygdala involves contributions from the main olfactory system, and results in long-lasting responses that may be related to the activation of the hypothalamic–hypophyseal axis over a prolonged timeframe. Different brain areas receive inputs from both the main and the accessory olfactory systems, possibly merging the stimulation of the two sensory organs to originate a more complex and integrated chemosensory perception.     

Immunocytochemical localization of serotonin in the central and peripheral chemosensory system of mosquitoes

Female mosquitoes depend on blood to complete their reproductive cycle and rely mainly on chemosensory systems to obtain blood meals. An immunocytochemical analysis reveals a number of serotonin-immunoreactive neurons that innervate the chemosensory systems, suggesting a potential role of serotonin in modulating chemosensory processes. In the primary olfactory system, we identify a single ipsilateral centrifugal neuron with arborizations in higher brain centers; the varicosities of this neuron display volumetric changes in response to both blood feeding and during a circadian rhythm. Six to eight pairs of serotonin-immunoreactive neurons are identified in the primary gustatory neuropil, including the subesophageal ganglion and tritocerebrum. The peripheral chemosensory organs, i.e. the antenna, the maxillary palp and the labium, are described as having extensive serotonergic neurohemal plexi. In addition, we describe the presence of serotonin-immunoreactive fibers in the mechanosensory Johnston's organ. Taking these results together, we discuss the potential role of serotonin as a neuromodulator in the chemosensory system of disease vector mosquitoes.     

Processing by the main olfactory system of chemosignals that facilitate mammalian reproduction

This article is part of a Special Issue “Chemosignals and Reproduction”.Most mammalian species possess two parallel circuits that process olfactory information. One of these circuits, the accessory system, originates with sensory neurons in the vomeronasal organ (VNO). This system has long been known to detect non-volatile pheromonal odorants from conspecifics that influence numerous aspects of social communication, including sexual attraction and mating as well as the release of luteinizing hormone from the pituitary gland. A second circuit, the main olfactory system, originates with sensory neurons in the main olfactory epithelium (MOE). This system detects a wide range of non-pheromonal odors relevant to survival (e.g., food and predator odors). Over the past decade evidence has accrued showing that the main olfactory system also detects a range of volatile odorants that function as pheromones to facilitate mate recognition and activate the hypothalamic-pituitary-gonadal neuroendocrine axis. We review early studies as well as the new literature supporting the view that the main olfactory system processes a variety of different pheromonal cues that facilitate mammalian reproduction.     

Chemosensory signal transduction in Caenorhabditis elegans

Chemosensory neurons translate perception of external chemical cues, including odorants, tastants, and pheromones, into information that drives attraction or avoidance motor programs. In the laboratory, robust behavioral assays, coupled with powerful genetic, molecular and optical tools, have made Caenorhabditis elegans an ideal experimental system in which to dissect the contributions of individual genes and neurons to ethologically relevant chemosensory behaviors. Here, we review current knowledge of the neurons, signal transduction molecules and regulatory mechanisms that underlie the response of C. elegans to chemicals, including pheromones. The majority of identified molecules and pathways share remarkable homology with sensory mechanisms in other organisms. With the development of new tools and technologies, we anticipate that continued study of chemosensory signal transduction and processing in C. elegans will yield additional new insights into the mechanisms by which this animal is able to detect and discriminate among thousands of chemical cues with a limited sensory neuron repertoire.     

Taste perception and coding in Drosophila

BACKGROUND: Discrimination between edible and contaminated foods is crucial for the survival of animals. In Drosophila, a family of gustatory receptors (GRs) expressed in taste neurons is thought to mediate the recognition of sugars and bitter compounds, thereby controlling feeding behavior. RESULTS: We have characterized in detail the expression of eight Gr genes in the labial palps, the fly's main taste organ. These genes fall into two distinct groups: seven of them, including Gr66a, are expressed in 22 or fewer taste neurons in each labial palp. Additional experiments show that many of these genes are coexpressed in partially overlapping sets of neurons. In contrast, Gr5a, which encodes a receptor for trehalose, is expressed in a distinct and larger set of taste neurons associated with most chemosensory sensilla, including taste pegs. Mapping the axonal targets of cells expressing Gr66a and Gr5a reveals distinct projection patterns for these two groups of neurons in the brain. Moreover, tetanus toxin-mediated inactivation of Gr66a- or Gr5a-expressing cells shows that these two sets of neurons mediate distinct taste modalities-the perception of bitter (caffeine) and sweet (trehalose) taste, respectively. CONCLUSION: Discrimination between two taste modalities-sweet and bitter-requires specific sets of gustatory receptor neurons that express different Gr genes. Unlike the Drosophila olfactory system, where each neuron expresses a single olfactory receptor gene, taste neurons can express multiple receptors and do so in a complex Gr gene code that is unique for small sets of neurons.     

Strong links between genomic and anatomical diversity in both mammalian olfactory chemosensory systems

Mammalian olfaction comprises two chemosensory systems: the odorant-detecting main olfactory system (MOS) and the pheromone-detecting vomeronasal system (VNS). Mammals are diverse in their anatomical and genomic emphases on olfactory chemosensation, including the loss or reduction of these systems in some orders. Despite qualitative evidence linking the genomic evolution of the olfactory systems to specific functions and phenotypes, little work has quantitatively tested whether the genomic aspects of the mammalian olfactory chemosensory systems are correlated to anatomical diversity. We show that the genomic and anatomical variation in these systems is tightly linked in both the VNS and the MOS, though the signature of selection is different in each system. Specifically, the MOS appears to vary based on absolute organ and gene family size while the VNS appears to vary according to the relative proportion of functional genes and relative anatomical size and complexity. Furthermore, there is little evidence that these two systems are evolving in a linked fashion. The relationships between genomic and anatomical diversity strongly support a role for natural selection in shaping both the anatomical and genomic evolution of the olfactory chemosensory systems in mammals.     

Something in the air? New insights into mammalian pheromones

Olfaction is the dominant sensory modality for most animals and chemosensory communication is particularly well developed in many mammals. Our understanding of this form of communication has grown rapidly over the last ten years since the identification of the first olfactory receptor genes. The subsequent cloning of genes for rodent vomeronasal receptors, which are important in pheromone detection, has revealed an unexpected diversity of around 250 receptors belonging to two structurally different classes. This review will focus on the chemical nature of mammalian pheromones and the complementary roles of the main olfactory system and vomeronasal system in mediating pheromonal responses. Recent studies using genetically modified mice and electrophysiological recordings have highlighted the complexities of chemosensory communication via the vomeronasal system and the role of this system in handling information about sex and genetic identity. Although the vomeronasal organ is often regarded as only a pheromone detector, evidence is emerging that suggests it might respond to a much broader variety of chemosignals.     

Olfactory receptor gene evolution is unusually rapid across Tetrapoda and outpaces chemosensory phenotypic change

Chemosensation is the most ubiquitous sense in animals, enacted by the products of complex gene families that detect environmental chemical cues and larger-scale sensory structures that process these cues. While there is a general conception that olfactory receptor (OR) genes evolve rapidly, the universality of this phenomenon across vertebrates, and its magnitude, are unclear. The supposed correlation between molecular rates of chemosensory evolution and phenotypic diversity of chemosensory systems is largely untested. We combine comparative genomics and sensory morphology to test whether OR genes and olfactory phenotypic traits evolve at faster rates than other genes or traits. Using published genomes, we identified ORs in 21 tetrapods, including amphibians, reptiles, birds, and mammals and compared their rates of evolution to those of orthologous non-OR protein-coding genes. We found that, for all clades investigated, most OR genes evolve nearly an order of magnitude faster than other protein-coding genes, with many OR genes showing signatures of diversifying selection across nearly all taxa in this study. This rapid rate of evolution suggests that chemoreceptor genes are in “evolutionary overdrive,” perhaps evolving in response to the ever-changing chemical space of the environment. To obtain complementary morphological data, we stained whole fixed specimens with iodine, µCT-scanned the specimens, and digitally segmented chemosensory and nonchemosensory brain regions. We then estimated phenotypic variation within traits and among tetrapods. While we found considerable variation in chemosensory structures, they were no more diverse than nonchemosensory regions. We suggest chemoreceptor genes evolve quickly in reflection of an ever-changing chemical space, whereas chemosensory phenotypes and processing regions are more conserved because they use a standardized or constrained architecture to receive and process a range of chemical cues.     

昆虫的化学感觉机理

昆虫是通过化学感觉器与其周围环境中的大量化学信息发生联系的。通过特定的化学感觉机制 ,昆虫可感知来自种内和种间 ,以及无机环境中的各种化学信息 ,并由此而作出相应的行为反应 ,从而为其自身寻找适宜的食物、配偶以及生存与繁殖场所 (如躲避天敌、避免或减少竞争等等 ) ,达到最大的繁殖成功。阐明昆虫的化学感觉机理 ,不仅可在理论上进一步加深对昆虫与植物、昆虫与昆虫相互关系的了解 ,而且可在实践上为开发害虫治理的新途径提供理论指导。本文将根据目前的最新研究成果 ,主要就昆虫的化学感觉机理 ,包括嗅觉和味觉机理作一综述 ,以期…     

Taste and pheromone perception in mammals and flies

The olfactory systems of insects and mammals have analogous anatomical features and use similar molecular logic for olfactory coding. The molecular underpinnings of the chemosensory systems that detect taste and pheromone cues have only recently been characterized. Comparison of these systems in Drosophila and mouse uncovers clear differences and a few surprising similarities.