Extreme sensitivity in an olfactory system

We recorded olfactory-induced cardiac responses to evaluate olfactory response thresholds to behaviourally relevant odours in a moth. Specific antennal receptor neurons enable insects to detect biologically meaningful odours such as sex pheromones and host-plant volatiles. The response threshold values demonstrated here are well below anything earlier reported in any organism. A heart response was triggered by less than six molecules of the most efficient odours hitting the antennae of the insect. The behavioural significance of this extreme sensitivity most likely lies in the creation of awareness and readiness to respond behaviourally at higher concentration levels.     

Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour

In anoestrous ewes, male chemosignals elicit rapid increases in luteinizing hormone (LH) secretion that can ultimately lead to ovulation. To assess the possible involvement of the accessory (vomeronasal) olfactory system in the mediation of those chemical cues, we destroyed this pathway by vomeronasal organ electrocauterization (Exp. I) and vomeronasal nerve section (Exp. II). Neither of these lesions inhibited the LH response of ewes to the odour of the male. These results suggest that the vomeronasal system is not necessary to mediate the neuroendocrine response of the ewe to the male odour. As both surgical methods spared the main olfactory system but destroyed the vomeronasal system, it is likely that the main olfactory system is involved in the LH response to chemical stimulation in sexually experienced ewes.     

Single unit analysis of odour quality coding by the olfactory antennal receptor system of the Colorado beetle

Peripheral events underlying plant odour quality discrimination in the Colorado beetle were investigated. Responses to saturated and unsaturated C-6 alcohols and aldehydes (“green leaf” volatiles) and to other plant compounds were recorded extracellularly. The olfactory receptors could respond by inhibition and/or excitation; inhibition was especially observed at the higher stimulus intensities. Variations in the response patterns were analyzed for a number of receptors constituting a representative sample, as indicated by rank correlation between mean spike responses and electroantennogram amplitudes for each odour stimulus. Application of cluster analysis showed that the olfactory receptors may be divided into two main groups, one reacting differentially to the complex of “green leaf” volatiles and their isomers, and another group showing a selective sensitivity to the aromatic compound methylsalicylate. Evidence is provided suggesting that individual olfactory sensilla can be innervated by more than one functional type of receptor unit. Responses to natural plant odours support the conclusion that plant odour quality is encoded by response patterning across a limited number of olfactory receptor types. The findings are discussed in relation to concepts of chemosensory coding and to the behaviour of the Colorado beetle.

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Analyse Cellulaire du Codage de la Qualité des Odeurs par le Système de Récepteurs Antennaires Olfactifs Chez le Doryphore

Résumé On a étudié la capacité de distinguer la qualité des odeurs végétales chez le doryphore. On a enregistré extracellulairement les réactions de cellules de récepteur olfactif séparées à des C-6 alcools et des aldéhydes saturés et insaturés (substances volatiles de la “feuille verte”) et à d'autres composés végétaux. Les récepteurs olfactifs pouvaient réagir par inhibition et/ou par excitation; on a particulièrement observé l'inhibition aux intensités élevées de stimulus. Les variations des types de réactions ont été analysées pour un certain nombre de récepteurs, qui constituent un échantillon représentatif, sur la base de la corrélation de rang entre les réactions de pointe moyennes et les amplitudes de l'électroantennogramme pour chaque odeur-stimulus. L'application d'une analyse en grappe a montré que les récepteurs olfactifs peuvent être divisés en deux groupes principaux, un groupe qui réagit de fa?on différentielle au complexe des substances volatiles de la “feuille verte” et de leurs isomères et un autre groupe qui a une sensibilité sélective à l'égard du composé aromatique méthylsalicylate. Le premier groupe a été subdivisé en différents types de récepteurs avec des réactions qui se chevauchent. Il semble que les sensilles olfactives individuelles peuvent être innervées par plus d'un type fonctionnel de cellule réceptrice. Les réactions aux odeurs végétales naturelles enregistrées appuient la conclusion que la qualité d'une odeur végétale est codée par un modèle de réaction pour un nombre limité de types de récepteurs olfactifs. On discute les résultats par rapport aux concepts du codage chimiosensoriel et par rapport au comportement du doryphore.

     

Masking of host plant odour in the olfactory orientation of the Colorado potato beetle

The odour of potato plants Solanum tuberosum L., elicits a true odour-conditioned positive anemotaxis in the Colorado potato beetle, Leptinotarsa decemlineata Say. Blending the odour of non-host plant species, namely wild tomatoes Lycopersicon hirsutum f. glabratum C.H. Mull or cabbage Brassica oleracea L. var. gemmifera DC., with the attractive host plant odour blocks the release of upwind responses in non-experienced as well as experienced females. The neutralization of the beetle's orientation responses is obtained without repellency. It is expected that masking of host plant odour occurs often in mixed cropping systems.

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Résumé Un certain nombre d'articles rapporte une diminution du nombre des insectes phytophages spécialistes comme une conséquence à la diversification des agroécosystèmes (Altieri & Letourneau, 1982; Cromartie, 1981; Kareiva, 1983; Risch et al., 1983). Ainsi, il a été supposé que la présence de plantes non-hôtes pouvait interférer avec celle de plantes hôtes en modifiant la nature des informations chimiques parvenant aux insectes. Les modifications comportementales qui peuvent en résulter lors de l'attraction à distance sont toutefois encore peu claires. Les expérimentations présentées ici analysent les réponses individuelles du doryphore à diverses stimulations olfactives issues de plantes entières. Des femalles ont été ainsi étudiées un jour après l'émergeance en présence d'air vierge et d'air chargé d'odeurs de Solanum tuberosum, Lycopersicon hirsutum f. glabratum, Brassica oleracea var. gemmifera, ainsi que des mélanges, S. tuberosum avec L. hirsutum et S. tuberosum avec B. oleracea. A partir de l'enregistrement continu de l'activité locomotrice dans chaque condition (à l'aide du compensateur de locomotion), nous avons déterminé que L. hirsutum et B. oleracea masquaient l'odeur de la plante hôte S. tuberosum en supprimant la réponse anémotactique positive conditionnée par l'odeur de cette dernière. Les mélanges d'odeurs ainsi obtenus sont considérés comme neutres pour l'orientation à longue distance du doryphore. L'expérience préalable par le doryphore de l'ingestion de feuillage de pomme de terre ne modifie pas l'effet du camouflage obtenu. Ces résultats laissent penser qu'il est possible de limiter la découverte de la plante hôte chez les insectes, et que les méthodes de camouflages olfactives pourraient prévenir les attaques de certains ravageurs.

     

Quantitative investigation of the odour specificity of central olfactory neurones in the American cockroach

Dose-response characteristics were evaluated for two groups(I and II) of pheromonesensitive neurones in the antennal lobesof the brain of adult male Periplaneta americana. Group I neuronesreact with about equal sensitivity to periplanone A and periplanoneB, two major components of the female sexual attractant. GroupII neurones are much less sensitive to B than is group I, butA is similarly effective with this group. Each group revealsa specific innervation pattern of the sex-specific macroglomerulusin the olfactory neuropile of the deutocerebrum.     

Variation in complex olfactory stimuli and its influence on odour recognition

Natural olfactory stimuli are often complex and highly variable. The olfactory systems of animals are likely to have evolved to use specific features of olfactory stimuli for identification and discrimination. Here, we train honeybees to learn chemically defined odorant mixtures that systematically vary from trial to trial and then examine how they generalize to each odorant present in the mixture. An odorant that was present at a constant concentration in a mixture becomes more representative of the mixture than other variable odorants. We also show that both variation and intensity of a complex olfactory stimulus affect the rate of generalization by honeybees to subsequent olfactory stimuli. These results have implications for the way that all animals perceive and attend to features of olfactory stimuli.     

A model of olfactory adaptation and sensitivity enhancement in the olfactory bulb

It has been suggested that the olfactory bulb, the first processing center after the sensory cells in the olfactory pathway, plays a role in olfactory adaptation, odor sensitivity enhancement by motivation and other olfactory psychophysical phenomena. In a mathematical model based on the bulbar anatomy and physiology, the inputs from the higher olfactory centers to the inhibitory cells in the bulb are shown to be able to modulate the response, and thus the sensitivity of the bulb to specific odor inputs. It follows that the bulb can decrease its sensitivity to a pre-existing and detected odor (adaptation) while remaining sensitive to new odors, or increase its sensitivity to interested searching odors. Other olfactory psychophysical phenomena such as cross-adaptation etc. are discussed as well.     

'Microsmatic' primates revisited: olfactory sensitivity in the squirrel monkey

Using a conditioning paradigm, the olfactory sensitivity of three squirrel monkeys to nine odorants representing different chemical classes as well as members of a homologous series of substances was investigated. The animals significantly discriminated dilutions as low as 1:10,000 n-propionic acid, 1:30,000 n-butanoic acid and n-pentanoic acid, 1:100,000 n-hexanoic acid, 1:1Mio n-heptanoic acid, 1:30, 000 1-pentanol, 1:300,000 1,8-cineole, 1:1Mio n-heptanal and 1:30Mio amyl acetate from the near-odorless solvent, with single individuals scoring even slightly better. The results showed (i) the squirrel monkey to have an unexpectedly high olfactory sensitivity, which for some substances matches or even is better than that of species such as the rat or the dog, and (ii) a significant negative correlation between perceptibility in terms of olfactory detection thresholds and carbon chain length of carboxylic acids. These findings support the assumptions that olfaction may play a significant and hitherto underestimated role in the regulation of primate behavior, and that the concept of primates as primarily visual and 'microsmatic' animals needs to be revised.     

Background odour induces adaptation and sensitization of olfactory receptors in the antennae of houseflies

The presence of background odour was found to have a small but significant effect on the sensitivity of the antennal olfactory system of houseflies, Musca domestica Linnaeus (Diptera: Muscidae), to new pulses of odour. We show that cross-adaptation and cross-sensitization between a background odour of (+/-)-1-octen-3-ol and pulses of (+/-)-1-octen-3-ol, 2-pentanone and R-(+)-limonene can occur, confirming that olfactory receptor cells are sensitive to different odours. Background odour can increase the responses to low concentration odour pulses and decrease the responses to higher concentration odour pulses. It is suggested that background odour has a larger effect on olfactory receptor cells that respond with a tonic increase of spike frequency, giving information about the level of odour concentration, i.e. the 'static' environment. Cells that respond in a phasic way only provide information on the dynamics of the olfactory environment.     

A piezoelectric biosensor as an olfactory receptor for odour detection: electronic nose

Humans can detect and differentiate the presence of different odours even at trace levels of these odorous compounds. The odour quantification of any particular samples is normally based on conventional panel decisions. Other analytical instruments could be used to detect trace levels of odorous molecules. This study presents the results of a biological sensor system subject to different odorants. The system consists of a sensor in which the isolated olfactory receptor proteins (ORPs) from bullfrogs (Rana spp.) were coated onto the surface of a piezoelectric (PZ) electrode, similar to the mechanism of human olfaction. The PZ crystal served as a signal transducer. The results indicate rapid (about 400 s), reversible, and longterm (up to 3 months) stable responses to different volatile compounds such as n-caproic acid, isoamyl acetate, n-decyl alcohol, beta-ionone, linalool, and ethyl caporate. The sensitivity of the sensor ranges from 10(-6)-10(-7) g, fully correlated with the olfactory threshold values of human noses. An array of six sensors consisting of five fractionated ORPs and one referenced phospholipid probe is able to respond to different odorants and form a typical fingerprint for each odorant.     

A quantitative structure activity analysis on the relative sensitivity of the olfactory and the nasal trigeminal chemosensory systems

We have applied a quantitative structure-activity relationship (QSAR) approach to analyze the chemical parameters that determine the relative sensitivity of olfaction and nasal chemesthesis to a common set of volatile organic compounds (VOCs). We used previously reported data on odor detection thresholds (ODTs) and nasal pungency thresholds (NPTs) from 64 VOCs belonging to 7 chemical series (acetate esters, carboxylic acids, alcohols, aliphatic aldehydes, alkylbenzenes, ketones, and terpenes). The analysis tested whether NPTs could be used to separate out "selective" chemosensory effects (i.e., those resting on the transfer of VOCs from the gas phase to the receptor phase) from "specific" chemosensory effects in ODTs. Previous work showed that selective effects overwhelmingly dominate chemesthetic potency whereas both selective and specific effects control olfactory potency. We conclude that it is indeed possible to use NPTs to separate out selective from specific effects in ODTs. Among the series studied, aldehydes and acids, except for formic acid, show clear specific effects in their olfactory potency. Furthermore, for VOCs whose odor potency rests mainly on selective effects, we have developed a QSAR equation that can predict their ODTs based on their NPTs.     

Temporal aspects of information processing in the first two stages of the frog olfactory system: influence of stimulus intensity

To understand information processing in the first two stagesof the olfactory system, neural activities were examined froma temporal point of view. The extracellular unitary activityof receptor cells and bulb neurons in response to four odorsdelivered in a range of concentrations from 1 x 10^–6 to5.62 x 10^–2 as a fraction of saturated vapor was recorded.For each population, unitary activities were pooled by 100-msbins, according to the nature and/or to the concentration ofthe stimulus. The results provided a view of the timing of activityof cell populations and allowed a comparison of the temporalstructures of the primary afferent message with that of thebulbar output message. Temporal patterns of receptor cell populationwere characterized by late and sustained discharges; thus, theprimary input volley did not coincide with the early and briefbulbar output message. In the two cell populations, the temporalresponse patterns elicited depended on the nature of the stimulus.At receptor level, interstimulus differences could be explainedin terms of binding interactions between odorants and receptorsites. In the bulb, while the input and output messages werenot strictly synchronous, some temporal characteristics relativeto the nature of the stimulus were preserved. In receptor cells,the activity occurring within 1 s following the stimulus onsetspecified stimulus intensity. By contrast, in the bulb, theevents which seemed to be involved in intensity coding werethose occurring within the first 500 ms. The convergence ofprimary afferences onto the bulb leads to an amplification ofthe earliest peripheral events setting up a sharp, earlier outputbulb message; in the processing of the input information, theolfactory bulb seems to combine an amplifying role for the earliestevents with a shutting action on later events.     

Fine structural aspects of apoptosis in the olfactory epithelium

Vertebrate olfactory receptor neurons are unique because they are continually replaced throughout life. They die by apoptosis under physiological conditions at all stages in their life cycle, and the dead olfactory neurons are replaced by the progeny of dividing basal cells. Thus, in the olfactory epithelium apoptosis is involved in tissue homeostasis and may be a direct or indirect trigger of neurogenesis. In this study, we focused on morphological changes occurring in the olfactory epithelium, i.e., degradation of DNA, condensation of nuclear chromatin, condensation of cytoplasm, blebbing of cytoplasmic fragments, and disposal of the dying and dead cells as the final phase of apoptosis. Moreover, we addressed other stages of apoptosis examining the nature of the stimulus that provokes the apoptotic response, the signal or metabolic state, and transduction of the signal that sends the message to the effector apparatus, and the effector or execution phase, which includes the activation of proteases.     

Effects of in utero odorant exposure on neuroanatomical development of the olfactory bulb and odour preferences

Human babies and other young mammals prefer food odours and flavours of their mother's diet during pregnancy as well as their mother's individually distinctive odour. Newborn mice also prefer the individual odours of more closely related--even unfamiliar--lactating females. If exposure to in utero odorants-which include metabolites from the mother's diet and the foetus's genetically determined individual odour-helps shape the neuroanatomical development of the olfactory bulb, this could influence the perception of such biologically important odours that are preferred after birth. We exposed gene-targeted mice during gestation and nursing to odorants that activate GFP-tagged olfactory receptors (ORs) and then measured the effects on the size of tagged glomeruli in the olfactory bulb where axons from olfactory sensory neurons (OSNs) coalesce by OR type. We found significantly larger tagged glomeruli in mice exposed to these activating odorants in amniotic fluid, and later in mother's milk, as well as significant preferences for the activating odour. Larger glomeruli comprising OSNs that respond to consistently encountered odorants should enhance detection and discrimination of these subsequently preferred odours, which in nature would facilitate selection of palatable foods and kin recognition, through similarities in individual odours of relatives.     

The influence of early odour experience on the neural response of the olfactory bulb in laboratory mice

Summary In mice (strain NMRI) the influence of olfactory rearing conditions on the ontogenetic development of the bulbar electroencephalogram (EEG) was investigated.The cages of control animals were perfused continually with filtered air, whereas in the three experimental groups geraniol was added to the atmosphere at different times (group G_0–13, from birth till day 13; group G_0–6, from birth till day 6; group G_6–12, from day 6 till day 12). At various ages the EEG of the bulbus olfactorius was studied by means of permanently implanted tungsten electrodes, and the neural response to nest odour and geraniol (10^–2 vol. %) was recorded.No differences were found between the groups regarding the overall development of the bulbar EEG, nor did the raising conditions affect the neural response to nest odour. However, in groups G_0–13 and G_6–12 a marked response to the odour of geraniol was recorded, while in the controls and the individuals that had experienced geraniol only during their first week of life, the bulbar response to this odourant did not differ from that obtained following stimulation with clean air. In the animals of group g_0–13, which were investigated as adults (day 70), the prominent geraniol response was still recordable 2 months after the last contact with the odour.These results indicate that odours experienced during a sensitive period in the nest evoke neuronal alterations in the olfactory system of the mouse that facilitate processing of a known odourant.     

Differential interactions of sex pheromone and plant odour in the olfactory pathway of a male moth

Most animals rely on olfaction to find sexual partners, food or a habitat. The olfactory system faces the challenge of extracting meaningful information from a noisy odorous environment. In most moth species, males respond to sex pheromone emitted by females in an environment with abundant plant volatiles. Plant odours could either facilitate the localization of females (females calling on host plants), mask the female pheromone or they could be neutral without any effect on the pheromone. Here we studied how mixtures of a behaviourally-attractive floral odour, heptanal, and the sex pheromone are encoded at different levels of the olfactory pathway in males of the noctuid moth Agrotis ipsilon. In addition, we asked how interactions between the two odorants change as a function of the males' mating status. We investigated mixture detection in both the pheromone-specific and in the general odorant pathway. We used a) recordings from individual sensilla to study responses of olfactory receptor neurons, b) in vivo calcium imaging with a bath-applied dye to characterize the global input response in the primary olfactory centre, the antennal lobe and c) intracellular recordings of antennal lobe output neurons, projection neurons, in virgin and newly-mated males. Our results show that heptanal reduces pheromone sensitivity at the peripheral and central olfactory level independently of the mating status. Contrarily, heptanal-responding olfactory receptor neurons are not influenced by pheromone in a mixture, although some post-mating modulation occurs at the input of the sexually isomorphic ordinary glomeruli, where general odours are processed within the antennal lobe. The results are discussed in the context of mate localization.     

Computation in the olfactory system

Computational models are increasingly essential to systems neuroscience. Models serve as proofs of concept, tests of sufficiency, and as quantitative embodiments of working hypotheses and are important tools for understanding and interpreting complex data sets. In the olfactory system, models have played a particularly prominent role in framing contemporary theories and presenting novel hypotheses, a role that will only grow as the complexity and intricacy of experimental data continue to increase. This review will attempt to provide a comprehensive, functional overview of computational ideas in olfaction and outline a computational framework for olfactory processing based on the insights provided by these diverse models and their supporting data.