Abstract
Recordings were made from single sensilla placodea of the worker honeybee (Apis mellifera). The sensilla were stimulated with one of two sets of four compounds and their binary mixtures, at two dosage levels. Aromatic compounds comprised one set, and saturated n-octane derivatives comprised the other set. Correlation, principal component, and cluster analyses indicate that responses to binary mixtures are not linear combinations of responses to the component compounds. The first principal component indicated that neuronal units had either more excitatory or more inhibitory responses to all odorants than would be expected from a model where inhibitory and excitatory responses are randomly distributed among the neuronal units. When compared to the responses to the component odorants, synergistic responses to binary odors occurred more often than would be expected by chance. Clear inhibitory responses to binary odors were less prevalent. This study agrees with an earlier study employing aromatic odorants in that most of the aromatic odorants each had groups of receptor neurons that were relatively selective for it, and each odorant had a distinctly different number of receptor neurons selective for it. Among the octane derivatives, receptor neurons were selective for the level of oxidation of the functional group or its site of attachment, rather than specific compounds.
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References
Ache BW (1989) Central and peripheral bases for mixture suppression in olfaction: a crustacean model. In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 101–114
Akers RP, Getz WM (1992) A test of identified response classes among olfactory receptor neurons in the honeybee worker. Chem Senses 17:191–209
Akers RP, O'Connell RJ (1988) The contribution of olfactory receptor neurons to the perception of pheromone component ratios in male redbanded leafroller moths. J Comp Physiol A 163:641–650
Akers RP, O'Connell RJ (1991) Response specificity of male olfactory receptor neurones for the major and minor components of a female pheromone blend. Physiol Entomol 16:1–17
Atema J, Borroni P, Johnson B, Voigt R, Handrich L (1989) Adaptation and mixture interactions in chemoreceptor cells: mechanisms for diversity and contrast enhancement. In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 83–100
Baker TC, Card RT, Roelofs WL (1976) Behavioral responses of male Argyrotaenia velutinana (Lepidoptera: Tortricidae) to components of its sex pheromone. J Chem Ecol 12:1239–1245
Beidler LM (1954) A theory of taste stimulation. J Gen Physiol 38:133–139
Beidler LM (1962) Taste receptor stimulation. Prog Biophys Chem 12:107–151
Bieber SL, Smith DV (1986) Multivariate analysis of sensory data: a comparison of methods. Chem Senses 11:19–47
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees Apis mellifera. J Comp Psychol 97:107–119
Boeckh J (1976) Aspects of nervous coding of sensory quality in the olfactory pathway of insects. Proc XV International Congr Entomol, Entomol Soc Am, pp 308–322
Boeckh J, Ernst KD (1987) Contribution of single unit analysis in insects to an understanding of olfactory function. J Comp Physiol A 161:549–565
Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurones in the central antennal pathway of insects. J Insect Physiol 30:15–26
Caprio J, Dudek J, Robinson II JJ (1989) Electro-olfactogram and multiunit olfactory receptor responses to binary and trinary mixtures of amino acids in the channel catfish, Ictalurus punctatus. J Gen Physiol 93:245–262
Carr WES, Derby CD (1986a) Behavioral chemoattractants for the shrimp, Palaemonetes pugio: Identification of active component in food extracts and evidence of synergistic mixture interactions. Chem Senses 11:49–64
Carr WES, Derby CD (1986b) Chemically stimulated feeding behavior in marine animals: the importance of chemical mixtures and the involvement of mixture interactions. J Chem Ecol 12:987–1009
Christensen TA, Hildebrand JG (1987) Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 160:553–569
Daniel PC, Derby CD (1988) Behavioral olfactory discrimination of mixtures by the spiny lobster (Panulirus argus) based on a habituation paradigm. Chem Senses 13:385–395
De Jong R, Visser JH (1988) Specificity-related suppression of responses to binary mixtures in olfactory receptors of the Colorado potato beetle. Brain Res 447:18–24
Den Otter CJ (1977) Single sensillum responses in the male moth Adoxophyes orana (F.v.R) to female sex pheromone components and their geometrical isomers. J Comp Physiol 121:205–222
Derby CD, Ache BW (1984) Quality coding of a complex odorant in an invertebrate. J Neurophysiol 51:906–924
Derby CD, Ache BW, Kennel EW (1985) Mixture suppression in olfaction: electrophysiological evaluation of the contribution of peripheral and central neural components. Chem Senses 10:301–316
Derby CD, Girardot MN, Daniel PC, Fine-Levy JB (1989) Olfactory discrimination of mixtures: Behavioral, electrophysiological and theoretical studies using the spiny lobster Panulirus argus. In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 65–82
Derby CD, Girardot MN, Daniel PC (1991a) Responses of olfactory receptor cells of spiny lobsters to binary mixtures. I. Intensity mixture interactions. J Neurophysiol 66:112–130
Derby CD, Girardot MN, Daniel PC (1991b) Responses of olfactory receptor cells of spiny lobsters to binary mixtures. II. Pattern mixture interactions. J Neurophysiol 66:131–139
Duchamp A, Revial MF, Holley A, MacLeod P (1974) Odor discrimination by frog olfactory receptors. Chem Senses and Flavor 1:213–233
Duchamp-Viret P, Duchamp A, Sicard G (1990) Olfactory discrimination over a wide concentration range: Comparison of receptor cell and bulb neuron abilities. Brain Res 517:256–262
Fine-Levy JB, Derby CD (1992) Behavioral discrimination of binary mixtures and their components: effects of mixture interactions on coding of stimulus intensity and quality. Chem Senses 17:307–323
Flanagan D, Mercer AR (1989) Morphology and response characteristics of neurones in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 164:483–494
Frank ME (1989) Processing of mixtures of stimuli with different tastes by primary mammalian taste neurons. In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 127–148
Free JB (1987) Pheromones in social bees. Cornell Univ Press Ithaca, New York
Frisch K von (1967) The dance language and orientation of bees. Harvard Univ Press, Cambridge, MA
Fujimura F, Yokohari F, Tateda H (1991) Classification of antennal olfactory receptors of the cockroach, Periplaneta americana L. Zool Sci 8:243–255
Gesteland RC, Lettvin JY, Pitts WH (1965) Chemical transmission in the nose of the frog. J Physiol (Lond) 181:525–559
Getz WM (1991) A neural network for processing olfactory-like stimuli. Bull Math Biol 53:805–823
Getz WM, Chapman R (1987) An odor perception model with application to kin discrimination in the social insects. Int J Neurosci 32:963–978
Getz WM, Smith KB (1987) Olfactory sensitivity and discrimination of mixtures in honeybees. J Comp Physiol A 160:239–246
Getz WM, Smith KB (1990) Odorant moiety and odor mixture perception in free-flying honey bees (Apis mellifera). Chem Senses 15:111–128
Getz WM, Smith KB (1991) Olfactory perception in honey bees: concatenated and mixed odorant stimuli, concentration, and exposure effects. J Comp Physiol A 169:215–230
Getz WM, Brückner D, Smith KB (1986) Conditioning honey bees to discriminate between heritable odors from full and half sisters. J Comp Physiol A 159:251–256
Getz WM, Brückner D, Smith KB (1988) Variability of chemosensory stimuli within honeybee (Apis mellifera) colonies: a differential conditioning assay for discrimination cues. J Chem Ecol 14:249–260
Getz WM, Brückner D, Smith KB (1989) Ontogeny of chemosensory cues in the worker honeybee Apis mellifera. Apidology 20:105–113
Gleeson RA, Ache BW (1985) Aminoacid suppression of taurine-sensitive chemosensory neurons. Br Res 335:99–107
Grant AJ, O'Connell RJ (1986) Neurophysiological and morphological investigations of pheromone-sensitive sensilla on the antenna of male Trichoplusia ni. J Insect Physiol 32:503–515
Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154:825–836
Jackson JE (1991) A user's guide to principal components. J Wiley and Sons, New York
Johnson BR, Borroni P, Atema J (1985) Response properties of lobster chemoreceptors: Tuning of primary taste neurons in walking legs. J Comp Physiol A 155:593–604
Johnson BR, Voigt R, Atema J (1989) Response properties of lobster chemoreceptor cells: response modulation by stimulus mixtures. Physiol Zool 62:559–579
Kaissling KE (1986) Insect olfactory receptors. Annu Rev Neurosci 9:121–145
Kaissling KE 1987 Wright lectures on insect olfaction. Colbow K (ed) Simon Fraser Univ, Burnaby, Br Columbia, Canada
Kang J, Caprio J (1991) Electro-olfactogram and multiunit olfactory receptor responses to complex mixtures of amino acids in the channel catfish, Ictalurus punctatus. J Gen Physiol 98:699–721
Klun JA, Chapman OL, Mattes KC, Wojkowski PW, Beroza M, Sonnet PE (1973) Insect sex pheromones: Minor amounts of opposite geometrical isomer critical to attraction. Science 181:661–663
Kroeze JH (1989) Is taste mixture suppression a peripheral or central event? In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 225–244
Lacher V (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, Kohlendioxyd, Lufteuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne (Apis mellifica L). Z Vergl Physiol 48:587–623
Lettvin JY, Gesteland RC (1965) Speculations on smell. Cold Spring Harbor Symp Quant Biol 30:217–225
Ma WC, Visser JH (1978) Single unit analysis of odour quality coding by the olfactory antennal receptor system of the Colorado beetle. Entomol Exp Appl 25:520–533
Masson C, Mustaparta H (1990) Chemical information processing in the olfactory system of insects. Physiol Rev 70:199–245
Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the moth Manduca sexta: Response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond B 213:249–277
Menzel R (1990) Learning, memory, and “cognition” in honey bees. In: Kesner RP (ed) Neurobiology of comparative cognition. Lawrence Erlbaum Associates, Hillsdale, NJ, pp 247–292
Menzel R, Erber J, Masuhr T (1974) Learning and memory in the honey bee. In: Barton-Browne L (ed) Experimental analysis of insect behavior. Springer, Berlin, pp 195–217
Mobbs PG (1982) The brain of the honeybee, Apis mellifera: I. The connections and spatial organization of the mushroom bodies. Phil Trans R Soc Lond B 298:309–354
Mustaparta H, Angst ME, Lanier GN (1977) Responses of single receptor cells in the pine engraver beetle, Ips pini (Say) (Coleoptera: Scolytidae) to its aggregation pheromone, ipsdienol, and the aggregation inhibitor, ipsenol. J Comp Physiol 121:343–347
Mustaparta H, Angst ME, Lanier GN (1980) Receptor dicrimination of enantiomers of the aggregation pheromone ipsdienol, in two species of Ips. J Chem Ecol 6:689–701
O'Connell RJ (1972) Response of olfactory receptors to the sex attractant, its Synergist and inhibitor in the red-banded leaf roller, Argyrotaenia velutinana. In: Schneider D (ed) Olfaction and taste IV. Wiss Verlagsges, Stuttgart, pp 180–186
O'Connell RJ (1975) Olfactory receptor responses to sex pheromone components in the redbanded leafroller moth. J Gen Physiol 65:179–205
O'Connell RJ (1985) Response to pheromone blends in insect olfactory receptor neurons. J Comp Physiol A 156:747–761
O'Connell RJ, Mozell MM (1969) Quantitative stimulation of frog olfactory receptors. J Neurophysiol 32:51–63
O'Connell RJ, Beuchamp JT, Grant AJ (1986) Insect olfactory receptor responses to components of pheromone blends. J Chem Ecol 12:451–467
Olberg RM (1983) Interneurons sensitive to female pheromone of the male silkworm moth, Bombyx mori. Physiol Entomol 8:419–428
Pers JNC van der, Thomas G, Otter CJ den (1980) Interactions between plant odours and pheromone reception in small ermine moths (Lepidoptera: Yponomeutidae). Chem Senses 5:367–371
Rabin MD, Cain WS (1989) Attention and learning in the perception of odor mixtures. In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 173–188
Revial MF, Duchamp A, Holley A (1978a) Odour discrimination by frog olfactory receptors: A second study. Chem Senses and Flavor 3:7–21
Revial MF, Duchamp A, Holley A, MacLeod P (1978b) Frog olfaction: Odour groups, acceptor distribution, and receptor categories. Chem Senses and Flavor 3:23–33
Revial MF, Sicard G, Duchamp A, Holley A (1982) New studies on odour discrimination in the frog's olfactory receptor cells: I. Experimental results. Chem Senses 7:175–190
Romesburg HC (1990) Cluster analysis for researchers. RE Krieger Co., Fla
Sass H (1976) Zur nervösen Codierung von Geruchsreizen bei Periplaneta americana. J Comp Physiol 107:49–65
Sass H (1978) Olfactory receptors on the antenna of Periplaneta: Response constellations that encode food odors. J Comp Physiol 128:227–233
Selzer R (1979) Morphological and physiological identification of food odor specific neurons in the deutocerebrum of Periplaneta americana. J Comp Physiol 134:159–163
Selzer R (1984) On the specificities of antennal olfactory receptor cells of Periplaneta americana. Chem Senses 8:375–395
Slifer EH, Sekhon SS (1961) Fine structure of the sense organs on the antennal flagellum of the honey bee Apis mellifera. J Morphol 109:351–381
Smith BH (1991) The olfactory memory of honey bee, Apis melliferea. I. Odorant modulation of short- and intermediate-term memory after single-trial conditioning. J Exp Biol 161:367–382
Smith BH, Menzel R (1989) A neuroethological analysis of variability in the feeding motor program of the honey bee Apis mellifera (Hymenoptera: Apidae). Ethology 82:68–81
Smith DV (1989) Neural and behavioral mechanisms of taste mixture perception in mammals. In: Laing DG, Cain WS, McBride RL, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, Australia, pp 149–172
Smith JJB, Mitchell DK, Rolseth BM, Whitehead AT, Albert PJ (1990) SAPID Tools: Microcomputer programs for analysis of multi-unit nerve recordings. Chem Senses 15:253–270
Suzuki H (1975) Antennal movements induced by odour and central projection of antennal neurons in the honeybee. J Insect Physiol 21:831–847
Suzuki H, Tateda H (1974) An electrophysiological study of olfactory interneurones in the brain of the honey-bee. J Insect Physiol 20:2287–2299
Vareschi E (1971) Duftunterscheidung bei der Honigbiene. Einzelzell-Ableitungen und Verhaltensreaktionen. Z Vergl Physiol 75:143–173
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Akers, R.P., Getz, W.M. Response of olfactory receptor neurons in honeybees to odorants and their binary mixtures. J Comp Physiol A 173, 169–185 (1993). https://doi.org/10.1007/BF00192976
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DOI: https://doi.org/10.1007/BF00192976