Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: Combined effects of octopamine and juvenile hormone

Hormones and Behavior

Volumn 56, Issue 1, 2009, Pages 185-191

  Jarriault, David ^a   Barrozo, Romina B ^a   de Carvalho Pinto, Carlos J ^b,c   Greiner, Birgit ^d   Dufour, Marie Cécile ^b   Masante Roca, Ingwild ^b   Gramsbergen, Jan B ^e   Anton, Sylvia ^a   Gadenne, Christophe ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b BORDEAUX SCIENCES AGRO   (France)

^c FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Antennal lobe; Juvenile hormone; Maturation; Octopamine; Pheromone response; Plasticity

Indexed keywords

JUVENILE HORMONE; MIANSERIN; OCTOPAMINE; SEX PHEROMONE;

AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA; ARTICLE; CONTROLLED STUDY; HORMONE SYNTHESIS; MALE; MATING; MATURATION; MOTH; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY TRACT; PRIORITY JOURNAL; SEXUAL BEHAVIOR; STIMULUS RESPONSE;

ACTION POTENTIALS; AGING; ANIMALS; BEHAVIOR, ANIMAL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; JUVENILE HORMONES; MALE; MIANSERIN; MICROELECTRODES; MOTHS; MOTOR ACTIVITY; NEURONS; OCTOPAMINE; PHENYLCARBAMATES; PHYSICAL STIMULATION; RECEPTORS, BIOGENIC AMINE; SENSORY THRESHOLDS; SEX ATTRACTANTS;

EID: 65849276129     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2009.04.005     Document Type: Article

References (65)

1. Andersen J.P., Schwartz A., Gramsbergen J.B., and Loeschcke V. Dopamine levels in the mosquito Aedes aegypti during adult development, following blood feeding and in response to heat stress. J. Insect Physiol. 52 (2006) 1163-1170
2. Anton S., and Gadenne C. Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5764-5767
3. Barron A.B., Schultz D.J., and Robinson G.E. Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J. Comp. Physiol. A. 188 (2002) 603-610
4. Bleeker M.A.K., Van der Zee B., and Smid H.M. Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of two parasitic wasps, Cotesia glomerulata and Cotesia rubeluca. Anim. Biol. 56 (2006) 247-257
5. Bloch G., and Meshi A. Influences of octopamine and juvenile hormone on locomotor behavior and period gene expression in the honeybee, Apis mellifera. J. Comp. Physiol. A. 193 (2007) 181-199
6. Causse R., Buès R., Barthes J., and Toubon J. Mise en évidence expérimentale de nouveaux constituants des phéromones sexuelles de Scotia ipsilon et Mamestra suasa. Médiateurs chimiques: comportement et systématique des lépidoptères. Coll. INRA 46 (1988) 75-82
7. Cayre M., Malaterre J., Scotto-Lomassese S., Aouane A., Strambi C., and Strambi A. Hormonal and sensory inputs regulate distinct neuroblast cell cycle properties in adult cricket brain. J. Neurosci. Res. 82 (2005) 659-664
8. Christensen T.A., and Hildebrand J.G. Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth, Manduca sexta. J. Comp. Physiol. 160 (1987) 553-569
9. Cologer-Clifford A., Simon N.G., Richter M.L., Smoluk S.A., and Lu S. Androgens and estrogens modulate 5-HT1A and 5-HT-1B agonist effects on aggression. Physiol. Behav. 65 (1999) 823-828
10. Dacks A.M., Christensen T.A., Agricola H.-J., Wollweber L., and Hildebrand J.G. Octopamine-immunoreactive neurons in the brain and suboesophageal ganglion of the hawkmoth Manduca sexta. J. Comp. Neurol. 488 (2005) 255-268
11. Davenport A.P., and Wright D.J. Octopamine distribution in the larvae and adults of two species of moth, Spodoptera littoralis and Manduca sexta. J. Insect Physiol. 32 (1986) 987-993
12. Dolzer J., Krannich S., Fischer K., and Stengl M. Oscillations of the transepithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J. Exp. Biol. 204 (2001) 2781-2794
13. Dorn S., Frischknecht M.L., Martinez V., Zurflüh R., and Fischer U. A novel non-neurotoxic insecticide with a broad activity spectrum. Zeit. Pflkr. Pflsch. 88 (1981) 269-275
14. Doucette W., Milder J., and Restrepo D. Adrenergic modulation of olfactory bulb circuitry affects odor discrimination. Learn Mem. 14 (2007) 539-547
15. Duportets L., Dufour M.C., Bécard J.M., Gadenne C., and Couillaud F. Inhibition of male corpora allata activity and sexual pheromone responsiveness in the black cutworm, Agrotis ipsilon, by the hypocholesterolemic agent, fluvastatin. Arch. Insect Biochem. Physiol. 32 (1996) 601-611
16. Duportets L., Dufour M.C., Couillaud F., and Gadenne C. Biosynthetic activity of corpora allata, growth of sex accessory glands and mating of the male moth Agrotis ipsilon. J. Exp. Biol. 201 (1998) 2425-2432
17. Farooqui T. Octopamine-mediated neuromodulation of insect senses. Neurochem. Res. 32 (2007) 1511-1529
18. Farooqui T., Robinson K.O., Vaessin H., and Smith B.H. Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J. Neuroscience 23 (2003) 5370-5380
19. Farooqui T., Vaessin H., and Smith B.H. Octopamine receptors in the honeybee (Apis mellifera) brain and their distribution by RNA-mediated interference. J. Insect Physiol. 50 (2004) 701-713
20. Gadenne C. Effects of fenoxycarb, JH mimetic, on female sexual behaviour of the black cutworm, Agrotis ipsilon (Lep:Noctuidae). J. Insect Physiol. 39 (1993) 25-29
21. Gadenne C., Renou M., and Sreng L. Hormonal control of sex pheromone responsiveness in the male black cutworm, Agrotis ipsilon. Experientia 49 (1993) 721-724
22. Gadenne C., and Anton S. Central processing of sex pheromone stimuli is differentially regulated by juvenile hormone in a male moth. J. Insect Physiol. 46 (2000) 1195-1206
23. Gadenne C., Dufour M.C., and Anton S. Transient post-mating inhibition of behavioural and central nervous responses to sex pheromone in an insect. Proc. Royal Soc. London B 268 (2001) 1631-1635
24. Gemeno C., and Haynes K.F. Chemical and behavioral evidence for a third pheromone component in a north American population of the black cutworm moth, Agrotis ipsilon. J. Chem. Ecol. 24 (1998) 999-1011
25. Giurfa M. Associative learning: the instructive function of biogenic amines. Curr. Biol. 16 (2006) R892-R895
26. Gramsbergen J.B., Sandberg M., Moller Dall A., Kornblit B., and Zimmer J. Gluthatione depletion in nigrostriatal slice cultures: GABA loss, dopamine resistance and protection by the tetrahydrobiopterin precursor sepiapterin. Brain Res. 935 (2002) 47-58
27. Greiner B., Gadenne C., and Anton S. Central processing of plant volatiles in Agrotis ipsilon males is age independent in contrast to sex pheromone processing. Chem. Senses 27 (2002) 45-48
28. Grosmaître X., Marion-Poll F., and Renou M. Biogenic amines modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem. Senses. 26 (2001) 653-661
29. Gruntenko N.E., Karpova E.K., Alekseev A.A., Chentsova N.A., Bogomolova E.V., Bownes M., and Rauschenbach I.Y. Effects of octopamine on reproduction, juvenile hormone metabolism, dopamine, and 20-hydroxyecdysone contents in Drosophila. Arch. Insect Biochem. Physiol. 65 (2007) 85-94
30. Hammer M., and Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem. 5 (1998) 146-156
31. Hardie S.L., and Hirsh J. An improved method for the separation and detection of biogenic amines in adult Drosophila brain extracts by high performance liquid chromatography. J. Neurosci. Met. 153 (2006) 243-249
32. Hirashima A., Hirokado S., Ohta H., Suetsugu T., Sakaguichi M., Kuwano E., Taniguchi E., and Eto M. Titres of biogenic amines and ecdysteroids: effect of octopamine on the production of ecdysteroids in the silkworm Bombyx mori. J. Insect Physiol. 45 (1999) 843-851
33. Huetteroth W., and Schachtner J. Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study developmental and adult neuronal plasticity. Cell Tissue Res. 319 (2005) 513-524
34. Hull E.M., Lorrain D.S., Du J., Matuszewich L., Lumley L.A., Putnam S.K., and Moses J. Hormone-neurotransmitter interactions in the control of sexual behavior. Behav. Brain Res. 105 (1999) 105-116
35. Hull E.M., Muschamp J.W., and Sato S. Dopamine and serotonin: influences on male sexual behavior. Physiol. Behav. 83 (2004) 291-307
36. Jarriault D., Gadenne C., Rospars J.P., and Anton S. Quantitative analysis of sex-pheromone coding in the antennal lobe of the moth Agrotis ipsilon: a tool to study network plasticity. J. Exp. Biol. 212 (2009) 1191-1201
37. Kaatz H., Eichmuller S., and Kreissl S. Stimulatory effect of octopamine on juvenile hormone biosynthesis in honey bees (Apis mellifera): physiological and immunocytochemical evidence. J. Insect Physiol. 40 (1994) 856-872
38. Kawai F., Kurahashi T., and Kaneko A. Adrenaline enhances odorant contrast by modulating signal encoding in olfactory receptor cells. Nature Neuroscience 2 (1999) 133-138
39. Kravitz E.A. Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J. Comp. Physiol. 186 (2000) 221-238
40. Lafon-Cazal M., and Baehr J.C. Octopaminergic control of corpora allata activity in an insect. Experientia 44 (1988) 895-896
41. Lehman K.K., Klukas K.A., Gilchrist L.S., and Mesce K.A. Steroid regulation of octopamine expression during metamorphic development of the moth Manduca sexta. J. Comp. Neurol. 424 (2000) 283-296
42. Linn C.E., and Roelofs W. Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromone in the cabbage looper moth Trichoplusia ni. Arch. Insect Biochem. Physiol. 3 (1986) 161-172
43. Linn C.E., and Roelofs W. Role of photoperiod cues in regulating the modulatory action of octopamine on pheromone-reponse thresholds in the cabbage looper moth. Arch. Insect Biochem. Physiol. 20 (1992) 285-302
44. Linn C.E., Campbell M.G., and Roelofs W.L. Photoperiod cues and the modulatory action of octopamine and 5-hydroxytryptamine on locomotor and pheromone in male gypsy moths, Lymantria dispar. Arch. Insect Biochem. Physiol. 20 (1992) 265-284
45. Linn C.E., Campbell M.G., Poole K.R., Wu W.-Q., and Roelofs W.L. Effects of photoperiod on the circadian timing of pheromone response in male Trichoplusia ni: relationship to the modulatory action of octopamine. J. Insect Physiol. 42 (1996) 881-891
46. Mani S.K., Allen J.M.C., Clark J.H., Blaustein J.D., and O'Malley B.W. Convergent pathways for steroid hormone- and neurotransmitter-induced rat sexual behavior. Science 265 (1994) 1246-1248
47. Mesce K.A. Metamodulation of the biogenic amines: second-order modulation by steroid hormones and amine cocktails. Brain Behav. Evol. 60 (2002) 339-349
48. Monastirioti M., Gorczyca M., Rapus J., Eckert M., White K., and Budnik V. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J. Comp. Neurol. 356 (1995) 275-287
49. Orr N., Orr G.L., and Hollingworth R.M. Characterization of a potent agonist of the insect octopamine-receptor-coupled adenylate cyclase. Insect Biochem. 21 (1991) 335-340
50. Orr N., Orr G.L., and Hollingworth R.M. The Sf9 cell line as a model for study in insect octopamine-receptors. Insect Biochem. Molec. Biol. 22 (1992) 591-597
51. Picimbon J.F., Gadenne C., Bécard J.M., Clément J.L., and Sreng L. Sex pheromone of the french black cutworm moth, Agrotis ipsilon (Lepidoptera:Noctuidae): identification and regulation of a multicomponent blend. J. Chem. Ecol. 23 (1997) 211-230
52. Poitout S., and Buès R. Elevage de plusieurs espèces de lépidoptères sur milieu artificiel simplifié. Ann. Zool. Ecol. Anim. 2 (1974) 79-91
53. Pophof B. Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J. Comp. Physiol. 186 (2000) 307-313
54. Pophof B. Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J. Comp. Physiol. 188 (2002) 659-662
55. Robinson G.E., Heuser L.M., Le Conte Y., Lenquette F., and Hollingworth R.M. Neurochemicals aid bee nestmate recognition. Nature. 399 (1999) 534-535
56. Roeder T. Tyramine and octopamine: ruling behavior and metabolism. Annu. Rev. Entomol. 50 (2005) 447-477
57. Roelofs W.L., and Linn C.E. Neuroactive substances as probes of central thresholds in sex pheromone perception. Mol. Entomol. 10 (1987) 67-77
58. Schulz D.J., and Robinson G.E. Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J. Comp. Physiol. 184 (1999) 481-488
59. Schulz D.J., Sullivan J.P., and Robinson G.E. Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm. Behav. 42 (2002) 222-231
60. Schwaerzel M., Monastirioti M., Scholz H., Friggi-Grelin F., Birman S., and Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neuroscience 23 (2003) 10495-10502
61. Sigg D., Thompson C.M., and Mercer A.R. Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera. J. Neuroscience 17 (1997) 7148-7156
62. Sinakevitch I., and Strausfeld N.J. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J. Comp. Neurol. 494 (2006) 460-475
63. Wagener-Hulme C., Kuehn J.C., Schulz D.J., and Robinson G.E. Biogenic amines and division of labor in honey bee colonies. J. Comp. Physiol., A 184 (1999) 471-479
64. Walikonis R., Schoun D., Zacharias D., Henley J., Coburn P., and Stout J. Attractiveness of the male Acheta domesticus calling song to females. III. The relation of age-correlated changes in syllable period recognition and phonotactic threshold to juvenile hormone III biosynthesis. J. Comp. Physiol. 169 (1991) 751-764
65. Woodring J., and Hoffmann K.H. The effects of octopamine, dopamine and serotonin on juvenile hormone synthesis, in vitro, in the cricket, Gryllus bimaculatus. J. Insect Physiol. 40 (1994) 797-802