Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 199, Issue 11, 2013, Pages 997-1014

  Lei, Hong ^a   Chiu, Hong Yan ^a   Hildebrand, John G ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Mixture; Moth; Pheromone; Protocerebrum; Ratio

Indexed keywords

FLUORESCENT DYE; SEX PHEROMONE;

ACTION POTENTIAL; ANIMAL; ARTICLE; BRAIN; BRAIN MAPPING; CYTOLOGY; DOSE RESPONSE; DRUG COMBINATION; DRUG EFFECT; ELECTROSTIMULATION; HEMISPHERIC DOMINANCE; MALE; MANDUCA; METABOLISM; NERVE CELL; NONPARAMETRIC TEST; ODOR; OLFACTORY SYSTEM;

ACTION POTENTIALS; ANIMALS; BRAIN; BRAIN MAPPING; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; ELECTRIC STIMULATION; FLUORESCENT DYES; FUNCTIONAL LATERALITY; MALE; MANDUCA; NEURONS; ODORS; OLFACTORY PATHWAYS; SEX ATTRACTANTS; STATISTICS, NONPARAMETRIC;

EID: 84885955272     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-013-0844-4     Document Type: Article

References (72)

1. Aertsen A, Diesmann M, Gewaltig MO (1996) Propagation of synchronous spiking activity in feedforward neural networks. J Physiol 90: 243-247.
2. Anton S, Hansson BS (1995) Sex-pheromone and plant-associated odor processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera, Noctuidae). J Comp Physiol A 176(6): 773-789.
3. Anton S, Löfstedt C, Hansson BS (1997) Central nervous processing of sex pheromones in two strains of the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). J Exp Biol 200: 1073-1087.
4. Bell RA, Joachim FG (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms (Lepidoptera-Sphingidae-Gelechiidae). Ann Entomol Soc Am 69: 365-373.
5. Brévault T, Quilici S (2010) Interaction between visual and olfactory cues during host finding in the tomato fruit fly Neoceratitis cyanescens. J Chem Ecol 36(3): 249-259.
6. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10: 269-274.
7. 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.
8. Cha DH, Nojima S, Hesler SP, Zhang A, Linn CE, Roelofs WL, Loeb GM (2008) Identification and field evaluation of grape shoot volatiles attractive to female grape berry moth (Paralobesia viteana). J Chem Ecol 34: 1180-1189.
9. Cha DH, Linn CE, Teal PEA, Zhang A, Roelofs WL, Loeb GM (2011) Eavesdropping on plant volatiles by a specialist moth: significance of ratio and concentration. PLoS One 6(2): e17033.
10. Chapin JK, Nicolelis MAL (1999) Principal component analysis of neuronal ensemble activity reveals multidimensional somatosensory representations. J Neurosci Methods 94: 121-140.
11. Chelaru MI, Dragoi V (2008) Efficient coding in heterogeneous neuronal populations. Proc Natl Acad Sci USA 105: 16344-16349.
12. Chow DM, Theobald JC, Frye MA (2011) An olfactory circuit increases the fidelity of visual behavior. J Neurosci 31(42): 15035-15047.
13. 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.
14. Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15: 1535-1547.
15. Domingue MJ, Musto CJ, Linn CE Jr, Roelofs WL, Baker TC (2007) Evidence of olfactory antagonistic imposition as a facilitator of evolutionary shifts in pheromone blend usage in Ostrinia spp. (Lepidoptera: Crambidae). J Insect Physiol 53: 488-496.
16. Domingue MJ, Musto CJ, Linn J, Roelofs WL, Baker TC (2008) Olfactory neuron responsiveness and pheromone blend preference in hybrids between Ostrinia furnacalis and Ostrinia nubilalis (Lepidoptera: Crambidae). J Insect Physiol 54: 1261-1270.
17. El-Sayed AM, Mitchell VJ, Manning LA, Suckling DM (2011) New sex pheromone blend for the lightbrown apple moth, Epiphyas postvittana. J Chem Ecol 37: 640-646.
18. Fang N, Teal PEA, Doolittle RE, Tumlinson JH (1995) Biosynthesis of conjugated olefinic systems in the sex pheromone gland of female tobacco hornworm moths, Manduca sexta (L.). Insect Biochem 25: 39-48.
19. 2+ imaging of identifiable neurons labeled by electroporation in insect brains. NeuroReport 20: 1061-1065.
20. 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.
21. Goyret J, Markwell PM, Raguso RA (2007) The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J Exp Biol 210(8): 1398-1405.
22. Haddad R, Weiss T, Khan R, Nadler B, Mandairon N, Bensafi M, Schneidman E, Sobel N (2010) Global features of neural activity in the olfactory system form a parallel code that predicts olfactory behavior and perception. J Neurosci 30: 9017-9026.
23. Hagström ÅK, Liénard MA, Groot AT, Hedenström E, Löfstedt C (2012) Semi-selective fatty acyl reductases from four heliothine moths influence the specific pheromone. PLoS One 7(5): e37230.
24. Han Q, Hansson BS, Anton S (2005) Interactions of mechanical stimuli and sex pheromone information in antennal lobe neurons of a male moth Spodoptera littoralis. J Comp Physiol A 191(6): 521-528.
25. Hillier NK, Vickers NJ (2011) Mixture interactions in moth olfactory physiology: examining the effects of odorant mixture, concentration, distal stimulation, and antennal nerve transection on sensillar responses. Chem Senses 36: 93-108.
26. Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254(2): 255-281.
27. Iwano M, Hill ES, Mori A, Mishima T, Mishima T, Ito K, Kanzaki R (2010) Neurons associated with the flip-flop activity in the lateral accessory lobe and ventral protocerebrum of the silkworm moth brain. J Comp Neurol 518(3): 366-388.
28. Jefferis GSXE, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187-1203.
29. Kanno H, Kuenen LPS, Klingler KA, Millar JG, Cardé RT (2010) Attractiveness of a four-component pheromone blend to male navel orangeworm moths. J Chem Ecol 36: 584-591.
30. 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(2): 211-215.
31. Kanzaki R, Arbas EA, Strausfeld NJ, Hildebrand JG (1989) Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165(4): 427-453.
32. 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): 1-14.
33. 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.
34. Kay LM, Lowry CA, Jacobs HA (2003) Receptor contributions to configural and elemental odor mixture perception. Behav Neurosci 117: 1108-1114.
35. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grunewald B, Rossler W (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499(6): 933-952.
36. Kisley MA, Gerstein GL (1999) The continuum of operating modes for a passive model neuron. Neural Comput 11: 1139-1154.
37. Leary GP, Allen JE, Bunger PL, Luginbill JB, Linn CE Jr, Macallister IE, Kavanaugh MP, Wanner KW (2012) Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species. Proc Natl Acad Sci USA 109: 14081-14086.
38. Lei H, Vickers N (2008) Central processing of natural odor mixtures in insects. J Chem Ecol 34: 915-927.
39. Lei H, Anton S, Hansson BS (2001) Olfactory protocerebral pathways processing sex pheromone and plant odor information in the male moth Agrotis segetum. J Comp Neurol 432: 356-370.
40. Lei H, Christensen TA, Hildebrand JG (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5: 557-565.
41. 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.
42. Løfaldli BB, Kvello P, Kirkerud N, Mustaparta H (2012) Activity in neurons of a putative protocerebral circuit representing information about a 10 component plant odor blend in Heliothis virescens. Front Syst Neurosci 6: 64.
43. Martin JP, Lei H, Riffell JA, Hildebrand JG (2013) Synchronous firing of antennal-lobe neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta. J Comp Physiol A. doi: 10. 1007/s00359-013-0849-z.
44. Matoušková P, Pichová I, Svatoš A (2007) Functional characterization of a desaturase from the tobacco hornworm moth (Manduca sexta) with bifunctional Z11- and 10, 12-desaturase activity. Insect Biochem 37: 601-610.
45. Najar-Rodriguez AJ, Galizia CG, Stierle J, Dorn S (2010) Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures. J Exp Biol 213: 3388-3397.
46. Nikonov A, Leal W (2002) Peripheral coding of sex pheromone and a behavioral antagonist in the Japanese beetle, Popillia japonica. J Chem Ecol 28: 1075-1089.
47. Nojima S, Linn C Jr, Morris B, Zhang A, Roelofs W (2003) Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. J Chem Ecol 29: 321-336.
48. Ochieng SA, Park KC, Baker TC (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptors neurons in male Helicoverpa zea. J Comp Physiol A 188: 325-333.
49. Person AL, Raman IM (2012) Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature 481: 502-505.
50. Pickett J, Bruce T, Chamberlain K, Hassanali A, Khan Z, Napier JA, Smart LE, Wadhams LJ, Woodcock CM (2006) Plant volatiles yielding new ways to exploit plant defence. In: Dicke M, Takken W (eds) Chemical ecology: from gene to ecosystem. Springer, Wageningen, pp 161-173.
51. Piñero JC, Dorn S (2007) Synergism between aromatic compounds and green leaf volatiles derived from the host plant underlies female attraction in the oriental fruit moth. Entomol Exp Appl 125: 185-194.
52. Pregitzer P, Schubert M, Breer H, Hansson BS, Sachse S, Krieger J (2012) Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens. Front Cell Neurosci 6 (article 42): 1-12.
53. Riffell JA, Lei H, Hildebrand JG (2009a) Neural correlates of behavior in the moth Manduca sexta in response to complex odors. Proc Natl Acad Sci USA 106: 19219-19226.
54. Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009b) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19: 335-340.
55. Rudolph M, Destexhe A (2003) Tuning neocortical pyramidal neurons between Integrators and coincidence detectors. J Comput Neurosci 14: 239-251.
56. Sakurai Y (1999) How do cell assemblies encode information in the brain? Neurosci Biobehav Rev 23: 785-796.
57. Sanes JR, Hildebrand JG (1976) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51: 282-299.
58. 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(4): 340-351.
59. Shields VDC, Hildebrand JG (2001) Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds. J Comp Physiol A 186: 1135-1151.
60. Stocker RF, Lienhard MC, Borst A, Fischbach KF (1990) Neural architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262: 9-34.
61. Sun XJ, Tolbert LP, Hildebrand JG (1997) Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 379(1): 2-20.
62. Tanaka NK, Suzuki E, Dye L, Ejima A, Stopfer M (2012) Dye fills reveal additional olfactory tracts in the protocerebrum of wild-type Drosophila. J Comp Neurol 520(18): 4131-4140.
63. Tasin M, Backman AC, Bengtsson M, Ioriatti C, Witzgall P (2006) Essential host plant cues in the grapevine moth. Naturwiss 93: 141-144.
64. Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones-an overview of biosynthesis and endocrine regulation. Insect Biochem 29: 481-514.
65. Tolbert LP, Matsumoto SG, Hildebrand JG (1983) Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3: 1158-1175.
66. Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, Mazomenos BE, Baumhover AH, Jackson DM (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10: 255-271.
67. Tumlinson JH, Mitchell ER, Doolittle RE, Jackson DM (1994) Field tests of synthetic Manduca sexta sex pheromone. J Chem Ecol 20: 579-591.
68. Vickers NJ, Poole K, Linn CE (2003) Consequences of interspecies antennal imaginal disc transplantation on organization of olfactory glomeruli and pheromone blend discrimination. J Comp Neurol 466: 377-388.
69. Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102: 147-159.
70. Webster B, Bruce T, Dufour S, Birkemeyer C, Birkett M, Hardie J, Pickett J (2008) Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae. J Chem Ecol 34: 1153-1161.
71. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109: 229-241.
72. Yao CA, Ignell R, Carlson JR (2005) Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25(37): 8359-8367.