Abstract
Pheromone-source orientation behavior can be modified by coexisting plant volatiles. Some host plant volatiles enhance the pheromonal responses of olfactory receptor neurons and increase the sensitivity of orientation behavior in the Lepidoptera species. Although many electrophysiological studies have focused on the pheromonal response of olfactory interneurons, the response to the mixture of pheromone and plant odor is not yet known. Using the silkmoth, Bombyx mori, we investigated the physiology of interneurons in the antennal lobe (AL), the primary olfactory center in the insect brain, in response to a mixture of the primary pheromone component bombykol and cis-3-hexen-1-ol, a mulberry leaf volatile. Application of the mixture enhanced the pheromonal responses of projection neurons innervating the macroglomerular complex in the AL. In contrast, the mixture of pheromone and cis-3-hexen-1-ol had little influence on the responses of projection neurons innervating the ordinary glomeruli whereas other plant odors dynamically modified the response. Together this suggests moths can process plant odor information under conditions of simultaneous exposure to sex pheromone.
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Abbreviations
- ΔILPC:
-
Delta area of the inferior lateral protocerebrum
- AL:
-
Antennal lobe
- Bol:
-
Bombykol
- Ca:
-
Calyx of the mushroom body
- D:
-
Dorsal
- Hex:
-
cis-3-Hexen-1-ol
- L:
-
Lateral
- LH:
-
Lateral horn
- LN:
-
Local interneuron
- LNs:
-
Local interneurons
- LY:
-
Lucifer Yellow CH
- M:
-
Medial
- MGC:
-
Macroglomerular complex
- Oe:
-
Oesophagus
- OG:
-
Ordinary glomeruli
- OL:
-
Optic lobe
- ORNs:
-
Olfactory receptor neurons
- PN:
-
Projection neuron
- PNs:
-
Projection neurons
References
Ai H, Kanzaki R (2004) Modular organization of the silkmoth antennal lobe macroglomerular complex revealed by voltage-sensitive dye imaging. J Exp Biol 207:633–644. doi:10.1242/jeb.00784
Anton S, Dufour MC, Gadenne C (2007) Plasticity of olfactory-guided behavior and its neurobiological basis: lessons from moths and locusts. Entomol Exp Appl 123:1–11. doi:10.1111/j.1570-7458.2006.00516.x
Anton S, Hansson BS (1994) Central processing of sex pheromone, host odour, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Neurol 350:199–214. doi:10.1002/cne.903500205
Anton S, Hansson BS (1995) Sex pheromone and plant-associated odour processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae). J Comp Physiol A 176:773–789. doi:10.1007/BF00192625
Anton S, Hansson BS (1999) Physiological mismatching between neurons innervating olfactory glomeruli in a moth. Proc R Soc Lond B Biol Sci 266:1813–1820. doi:10.1098/rspb.1999.0851
Berg BG, Almass TJ, Biaalie JG, Mustaparta H (1998) The macroglomerular complex of the antennal lobe in the tobacco budworm Heliothis virescens: specified subdivision in four compartments according to information about biologically significant compounds. J Comp Physiol A 183:669–682. doi:10.1007/s003590050290
Broome BM, Jayaraman V, Laurent G (2006) Encoding and decoding of overlapping odor sequences. Neuron 51:467–482. doi:10.1016/j.neuron.2006.07.018
Butenandt A, Beckermann R, Stamm D, Hecker E (1959) Über den Sexual-lockstoff des Seidenspinners Bombyx mori. Reindars-tellung udn Konstitution. Z Naturforsch 14:283–284
Byers JA, Birgersson G, Lofqvist J, Appelgren M, Bergstrom G (1990) Isolation of pheromone synergists of bark beetle, Pityogenes chalcographus, from complex insect-plant odors by fractionation and subtractive-combination bioassay. J Chem Ecol 16:861–876. doi:10.1007/BF01016496
Carlsson MA, Chong KY, Daniels W, Hansson BS, Pearce TC (2007) Component information is preserved in glomerular responses to binary odor mixtures in the moth Spodoptera littoralis. Chem Senses 32:433–443. doi:10.1093/chemse/bjm009
Christensen TA, Mustaparta H, Hildebrand JG (1989) Discrimination of sex pheromone blends in the olfactory system of the moth. Chem Senses 14:463–477. doi:10.1093/chemse/14.3.463
Christensen TA, Mustaparta H, Hildebrand JG (1991) Chemical communication in heliothine moths. II. Central processing of intra- and interspecific olfactory messages in the male corn earworm moth Helicoverpa zea. J Comp Physiol A 169:259–274. doi:10.1007/BF00206990
Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG (1993) Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A 173:385–399. doi:10.1007/BF00193512
De Jong R, Visser JH (1988) Integration of olfactory information in the Colorado potato beetle brain. Brain Res 447:10–17. doi:10.1016/0006-8993(88)90960-2
Deng JY, Wei HY, Huang YP, Du JW (2004) Enhancement of attraction to sex pheromones of Spodoptera exigua by volatile compounds produced by host plants. J Chem Ecol 30:2037–2045. doi:10.1023/B:JOEC.0000045593.62422.73
Deisig N, Giurfa M, Lachnit H, Sandoz JC (2006) Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24:1161–1174. doi:10.1111/j.1460–9568.2006.04959.x
Dickens JC, Jang EB, Light DM, Alford AR (1990) Enhancement of insect pheromone responses by green leaf volatiles. Naturwissenschaften 77:29–31. doi:10.1007/BF01131792
Dickens JC, Smith JW, Light DM (1993a) Green leaf volatiles enhance sex attractant pheromone of the tobacco budworm, Heliothis virescens (Lep.: Noctuidae). Chemoecology 4:175–177. doi:10.1007/BF01256553
Dickens JC, Visser JH, van der Pers JMC (1993b) Detection and deactivation of pheromone and plant odor components by the beet armyworm, Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). J Insect Physiol 39:503–516. doi:10.1016/0022-1910(93)90083-4
Distler PG, Boeckh J (1997) Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. Local multiglomerular interneurons. J Comp Neurol 383:529–540. doi:10.1002/(SICI)1096-9861(19970714)383:4<529::AID-CNE9>3.0.CO;2-4
Distler PG, Gruber C, Boeckh J (1998) Synaptic connections between GABA-immunoreactive neurons and uniglomerular projection neurons within the antennal lobe of the cockroach, Periplaneta americana. Synapse 29:1–13. doi:10.1002/(SICI)1098-2396(199805)29:1<1::AID-SYN1>3.0.CO;2-C
Duchamp-Viret P, Duchamp A, Chaput MA (2003) Single olfactory sensory neurons simultaneously integrate the components of an odour mixture. Eur J Neurosci 18:2690–2696. doi:10.1111/j.1460-9568.2003.03001.x
Edwards LK (ed) (1993) Applied anaysis of variance in behavioral science. M Dekker, New York
Gao Q, Yuan B, Chess A (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3:780–785. doi:10.1038/77680
Gattellier L, Nagao T, Kanzaki R (2004) Serotonin modifies the sensitivity of the male silkmoth to pheromone. J Exp Biol 207:2487–2496. doi:10.1242/jeb.01035
Getz WM, Akers RP (1997) Responses of American cockroach (Periplaneta americana) olfactory recetpors to selected alcohol odorants and their binary combinations. J Comp Physiol A 180:701–709. doi:10.1007/s003590050084
Ginzel MD, Hanks LM (2005) Role of host plant volatiles in mate location for three species of longhorned beetles. J Chem Ecol 31:213–217. doi:10.1007/s10886-005-6735-6
Hamamura Y, Hayashiya K, Naito K (1961) Food selection by silkworm larvae, Bombyx mori. Nature 190:879–881. doi:10.1038/190880a0
Hansson BS, Anton S (2000) Funciton and morphology of the antennal lobe: new developments. Annu Rev Entomol 45:203–231. doi:10.1146/annurev.ento.45.1.203
Hansson BS, Anton S, Christensen TA (1994) Structure and functions of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera: Noctuidae). J Comp Physiol A 175:547–562. doi:10.1007/BF00199476
Hansson BS, Ljungberg H, Hallberg E, Lofstedt C (1992) Functional specialization of olfactory glomeruli in a moth. Science 256:1313–1315. doi:10.1126/science.1598574
Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501. doi:10.1146/annurev.en.34.010189.002401
Iwano M, Kanzaki R (2005) Immunocytochemical identification of neuroactive substances in the antennal lobe of the male silkworm moth Bombyx mori. Zoolog Sci 22:199–211. doi:10.2108/zsj.22.199
Joerges J, Kuttner A, Galizia CG, Menzel R (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature 387:282–288. doi:10.1038/387285a0
Kaissling KE, Zack Strausfeld C, Rumbo ER (1987) Adaptation processes in insect olfactory receptors. Mechanisms and behavioral significance. Ann NY Acad Sci 510:104–112
Kang J, Caprio J (1997) In vivo responses of single olfactory receptor neurons of channel catfish to binary mixtures of amino acids. J Neurophysiol 77:1–8
Kanzaki R (1998) Coordination of wing motion and walking suggests common control of zigzag motor program in a male silkworm moth. J Comp Phsyiol A 182:267–276. doi:10.1007/s003590050177
Kanzaki R, Ikeda A, Shibuya T (1994) Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori. J Comp Physiol A 175:1–14. doi:10.1007/BF00217431
Kanzaki R, Shibuya T (1986) Identification of the deutocerebral neurons responding to the sexual pheromone in the male silkworm moth brain. Zoolog Sci 3:409–418
Kanzaki R, Shibuya T (1992) Long-lasting excitation of protocerebral bilateral neurons in the pheromone-processing pathways of the male moth Bombyx mori. Brain Res 587:212–215. doi:10.1016/0006-8993(92)90999-P
Kanzaki R, Sugi N, Shibuya T (1992) Self-generated zigzag turning of Bombyx mori males during pheromone-mediated upwind walking. Zoolog Sci 9:515–527
Kanzaki R, Arbas EA, Strausfeld NL, Hildebrand JG (1989) Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165:427–453. doi:10.1007/BF00611233
Kanzaki R, Soo K, Seki Y, Wada S (2003) Projections to higher olfactory centers from subdivisions of the antennal lobe macroglomerular complex of the male silkmoth. Chem Senses 28:113–130. doi:10.1093/chemse/28.2.113
Kloppenburg P, Mercer AR (2008) Serotonin modulation of moth central olfactory neurons. Annu Rev Entomol 53:179–190. doi:10.1146/annurev.ento.53.103106.093408
Koontz MA, Schneider D (1987) Sexual dimorphism in neuronal projections from the antennae of silkmoths (Bombyx mori, Antheraea polyphemus) and the gypsy moth (Lymantria dispar). Cell Tissue Res 249:39–50. doi:10.1007/BF00215416
Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioral responses to a Drosophila sex pheromone. Nature 446:542–546. doi:10.1038/nature05672
Landolt PJ, Reed HC, Heath RR (1992) Attraction of female papaya fruit fly (Diptera: Tephritidae) to male pheromone and host fruit. Environ Entomol 21:1154–1159
Lei H, Christensen TA, Hildebrand JG (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5:557–565. doi:10.1038/nn859
Lei H, Christensen TA, Hildebrand JG (2004) Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J Neurosci 24:11108–11119. doi:10.1523/JNEUROSCI.3677-04.2004
Light DM, Flath RA, Buttery RG, Zalom FG, Rice RE, Dickens JC, Jang EB (1993) Host-plant green-leaf volatiles synergize the synthetic sex pheromones of the corn earworm and codling moth (Lepidoptera). Chemoecology 4:145–152. doi:10.1007/BF01256549
Loudon C, Koehl MAR (2000) Sniffing by a silkworm moth: wing fanning enhances air penetration through and pheromone interception by antennae. J Exp Biol 203:2977–2990
Maida R, Mameli M, Müller B, Krieger J, Steinbrecht RA (2005) The expression pattern of four odorant-binding proteins in male and female silk moths, Bombyx mori. J Neurocytol 34:149–163. doi:10.1007/s11068-005-5054-8
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
Minor AV, Kaissling KE (2003) Cell responses to single pheromone molecules may reflect the activation kinetics of olfactory receptor molecules. J Comp Physiol A 189:221–230. doi:10.1007/s00359-003-0394-2
Mishima T, Kanzaki R (1998) Coordination of flipflopping neural signals and head turning during pheromone-mediated walking in a male silkworm moth Bombyx mori. J Comp Physiol A 183:273–282. doi:10.1007/s003590050255
Mishima T, Kanzaki R (1999) Physiological and morphological characterization of olfactory descending interneurons of the male silkworm moth, Bombyx mori. J Comp Physiol A 184:143–160. doi:10.1007/s003590050314
Mita K, Kasahara M, Sasaki S, Nagayasu Y, Yamada T, Kanamori H, Namiki N, Kitagawa M, Yamashita H, Yasukochi Y et al (2004) The genome sequence of silkworm, Bombyx mori. DNA Res 11:27–35. doi:10.1093/dnares/11.1.27
Moto K, Abdel Salam SE, Sakurai S, Iwami M (1999) Gene transfer into insect brain and cell-specific expression of bombyxin gene. Dev Genes Evol 209:447–450. doi:10.1007/s004270050277
Mustaparta H (1990) Chemical information processing in the olfactory system of insects. Physiol Rev 70:199–245
Nakagawa T, Sakurai T, Nishioka T, Touhara K (2005) Insect sex-pheromone signals mediated by specific combinations of olfactory receptors. Science 307:1638–1642. doi:10.1126/science.1106267
Nakamuta K, Leal WS, Nakashima T, Tokoro M, Ono M, Nakanishi M (1997) Increase of trap catches by a combination of male sex pheromones and floral attractant in longhorn beetle, Anaglyptus subfasciatus. J Chem Ecol 26:823–840. doi:10.1023/B:JOEC.0000006427.56337.6c
Namiki S, Kanzaki R (2006) Spatial and temporal organization of odor representation by uniglomerular projection neurons in the moth antennal lobe. Chem Senses 31:A80. doi:10.1093/chemse/bjj055
Nishino H, Mizunami M (2007) Sensilla position on antennae influences afferent terminal location in glomeruli. Neuroreport 18:1765–1769. doi:10.1097/WNR.0b013e3282f16d71
Ochieng SA, Park KC, Baker TC (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J Comp Physiol A 188:325–333. doi:10.1023/B:JOEC.0000018633.94002.af
Oka Y, Omura M, Kataoka H, Touhara K (2004) Olfactory receptor antagonism between odorants. EMBO J 23:120–126. doi:10.1038/sj.emboj.76000
Olberg RM (1983) Pheromone-triggered flip-flopping interneurons in the ventral nerve cord of the silkworm moth, Bombyx mori. J Comp Physiol A 152:297–307. doi:10.1007/BF00606236
Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89–103. doi:10.1016/j.neuron.2007.03.010
Phillips TW, West JR, Foltz JL, Silverstein RM, Lanier GN (1984) Aggregation pheromone of the deodar weevil, Pissodes nemeorensis (Coleoptera: Curculionidae): isolation and activity of grandisol and grandisal. J Chem Ecol 10:1417–1423. doi:10.1007/BF00990312
Reddy GVP, Guerrero A (2000) Behavioral responses of the diamondback moth, Plutella xylostella, to green leaf volatiles of Brassica oleracea subsp. capitata. J Agric Food Chem 48:6025–6029. doi:10.1021/jf0008689
Reddy GVP, Guerrero A (2004) Interactions of insect pheromones and plant semiochemicals. Trends Plant Sci 9:253–261. doi:10.1016/j.tplants.2004.03.009
Reisenman CE, Christensen TA, Hildebrand JG (2005) Chemosensory selectivity of output neurons innervating an identified, sexually isomorphic olfactory glomerulus. J Neurosci 25:8017–8026. doi:10.1523/JNEUROSCI.1314-05.2005
Sadek MM, Hansson BS, Rospars JP, Anton S (2002) Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J Exp Biol 205:1363–1376
Said I, Renou M, Morin JP, Ferreira JMS, Rochat D (2005) Interactions between acetoin, a plant volatile, and pheromone in Rhynchophorus palmarum: behavioral and olfactory neuron responses. J Chem Ecol 31:1789–1805. doi:10.1007/s10886-005-5927-4
Sakurai T, Nakagawaga T, Mitsuno H, Mori H, Endo Y, Tanoue S, Yasukochi Y, Touhara K, Nishioka T (2004) Identification and functional characterization of a sex pheromone receptor in the silkmoth Bombyx mori. Proc Natl Acad Sci USA 101:16653–16658. doi:10.1073/pnas.0407596101
Sandoz JC (2006) Odour-evoked responses to queen pheromone components and to plant odours using optical imaging in the antennal lobe of the honey bee drone Apis mellifera L. J Exp Biol 209:3587–3598. doi:10.1242/jeb.02423
Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea+Hexapoda). Arthropod Struct Dev 34:257–299. doi:10.1016/j.asd.2005.04.003
Schlief ML, Wilson RI (2007) Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci 10:623–630. doi:10.1038/nn1881
Seki Y, Aonuma H, Kanzaki R (2005) Pheromone processing center in the protocerebrum of Bombyx mori revealed by nitric oxide-induced anti-cGMP immunocytochemistry. J Comp Neurol 481:340–351. doi:10.1002/cne.20392
Seki Y, Kanzaki R (2008) Comprehensive morphological identification and GABA immunocytochemistry of antennal lobe local interneurons in Bombyx mori. J Comp Neurol 506:93–107. doi:10.1002/cne.21528
Shang Y, Claridge-Chang A, Sjulson L, Pyparet M, Miesenbock G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601–612. doi:10.1016/j.cell.2006.12.034
Shiomi K, Fujiwara Y, Atsumi T, Kajiura Z, Nakagaki M, Tanaka Y, Mizoguchi A, Yaginuma T, Yamashita O (2005) Myocyte enhancer factor 2 (MEF2) is a key modulator of the expression of the prothoracicotropic hormone gene in the silkworm, Bombyx mori. FEBS J 272:3853–3862. doi:10.1111/j.1742-4658.2005.04799.x
Stopfer M, Laurent G (1999) Short-term memory in olfactory network dynamics. Nature 402:664–668. doi:10.1038/45244
Tabor R, Yaksi E, Weislogel JM, Friedrich RW (2004) Processing of odor mixtures in the zebrafish olfactory bulb. J Neurosci 24:6611–6620. doi:10.1523/JNEUROSCI.1834-04.2004
Topazzini A, Mazza M, Pelosi P (1990) Electroantennogram responses of five Lepidopatera species to 26 general odourants. J Insect Physiol 36:619–624. doi:10.1016/0022-1910(90)90065-N
Vickers NJ, Christensen TA, Hildebrand JG (1998) Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combination of uniquely identifiable glomeruli. J Comp Neurol 400:35–56. doi:10.1002/(SICI)1096-9861(19981012)400:1<35::AID-CNE3>3.0.CO;2-U
Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159. doi:10.1016/S0092-8674(00)00021-0
Wada S, Kanzaki R (2005) Neural control mechanisms of the pheromone-triggered programmed behavior in male silkmoths revealed by double-labeling of descending interneurons and a motor neuron. J Comp Neurol 484:168–182. doi:10.1002/cne.20452
Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25:9069–9079. doi:10.1523/JNEUROSCI.2070-05.2005
Wu W, Anton S, Lofstedt C, Hansson BS (1996) Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth, Agrotis segetum. Proc Natl Acad Sci U S A 93:8022–8027
Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, Zhao P, Zha X, Cheng T, Chai C et al (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–1940. doi:10.1126/science.1102210
Xu F, Shaefer M, Kida I, Shafer J, Liu N, Rothman DL, Hyder F, Restrepo D, Shepherd GM (2005) Simultaneous activation of mouse main and accessory olfactory bulbs by odors or pheromones. J Comp Neurol 489:491–500. doi:10.1002/cne.20652
Yamada M (1971) A search for odour encoding in the olfactory lobe. J Physiol 214:127–143
Yang Z, Bengtsson M, Witzgall P (2004) Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella. J Chem Ecol 30:619–629. doi:10.1023/B:JOEC.0000018633.94002.af
Zhang QH, Schlyter F (2003) Redundancy, synergism, and active inhibitory range of non-host volatiles in reducing pheromone attraction in European spruce bark beetle Ips typographus. Oikos 101:299–310. doi:10.1034/j.1600-0706.2003.111595.x
Acknowledgments
The authors thank Dr Shigeru Matsuyama (University of Tsukuba) for purification of bombykol, and Drs. Hidefumi Mitsuno, Evan S. Hill and Shuichi S. Haupt for insightful discussion and critical comments on this manuscript. This research was supported by the Japanese Ministry of Education, Culture, Sports, Science, and Technology; Grant numbers: Grant-in-Aid for Scientific Research on Priority Areas (Area No. 454) and Grant-in-Aid for Scientific Research (B).
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Namiki, S., Iwabuchi, S. & Kanzaki, R. Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori . J Comp Physiol A 194, 501–515 (2008). https://doi.org/10.1007/s00359-008-0325-3
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DOI: https://doi.org/10.1007/s00359-008-0325-3