Octopamine-immunoreactive neurons in the brain and subesophageal ganglion of the hawkmoth Manduca sexta

Journal of Comparative Neurology

Volumn 488, Issue 3, 2005, Pages 255-268

  Dacks, Andrew M ^a   Christensen, Thomas A ^a   Agricola, Hans J ^b   Wollweber, Leo ^c   Hildebrand, John G ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

Insect brain; Learning; Neuromodulation; Octopamine; Olfaction; VUM

Indexed keywords

MONOAMINE; MONOCLONAL ANTIBODY; NEUROHORMONE; NEUROTRANSMITTER; OCTOPAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN REGION; CONTROLLED STUDY; FEMALE; GANGLION; IMMUNOREACTIVITY; LEPIDOPTERA; MANDUCA SEXTA; MOUSE; MUSHROOM BODY; NERVE CELL; NERVE CORD; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; BRAIN; CROSS REACTIONS; GANGLIA, INVERTEBRATE; IMMUNIZATION; IMMUNOGLOBULIN ISOTYPES; IMMUNOHISTOCHEMISTRY; MANDUCA; MICE; MICE, INBRED C57BL; NEURONS; OCTOPAMINE;

EID: 21644457018     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20556     Document Type: Article

References (73)

1. Bacon JP, Thompson KSJ, Stern M. 1995. Identified octopaminergic neurons provide an arousal mechanism in the locust brain. J Neurophysiol 74:2739-2743.
2. Bell RA, Joachim FA. 1996. Techniques for rearing laboratory colonies of tobacco hornworm and pink bollworms. Ann Ent Soc Am 69:365-373.
3. Bräunig P. 1991. Suboesophageal DUM neurons in the principal neuropiles of the locust brain. Philos Trans R Soc Lond B 332:221-240.
4. Bräunig P. 1997. The peripheral branching pattern of identified dorsal unpaired median (DUM) neurones in the locust. Cell Tiss Res 290:641-654.
5. Bräunig P, Pflüger HJ. 2001. The unpaired median neurons of insects. Adv Insect Physiol 28:185-266.
6. Campbell HR, Thompson KJ, Siegler MVS. 1995. Neurons of the median neuroblast lineage of the grasshopper: a population study of the efferent DUM neurons. J Comp Neurol 358:541-551.
7. 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.
8. Christensen TA, Sherman TG, McCaman RE, Carlson, AD. 1983. Presence of octopamine in firefly photomotor neurons. Neuroscience 9:183-189.
9. Claassen DE, Kammer AE. 1986. Effects of octopamine, dopamine and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. J Neurobiol 17:1-14.
10. Cunningham JP, Moore CJ, Zalucki MP, West SA. 2004. Learning, odour preference and flower foraging in moths. J Comp Physiol A 207:87-94.
11. Daly KC, Smith BH. 2000. Associative olfactory learning in the moth Manduca sexta. J Exp Biol 203:2025-2038.
12. Daly KC, Chandra S, Durtschi ML, Smith BH. 2001a. The generalization of an olfactory-based conditioned response reveals unique but overlapping odour representations in the moth Manduca sexta. J Exp Biol 204:3085-3095.
13. Daly KC, Durtschi ML, Smith BH. 2001b. Olfactory-based discrimination learning in the moth, Manduca sexta. J Insect Physiol 47:375-384.
14. Daly KC, Christensen TA, Lei H, Smith BH, Hildebrand JG. 2004. Learning modulates the ensemble representations for odors in primary olfactory networks. Proc Natl Acad Sci U S A 101:10476-10481.
15. Davenport AP, Evans PD. 1984. Stress-induced changes in the octopamine levels of insect haemolymph. Insect Biochem 14:135-143.
16. Davenport AP, Wright DJ. 1986. Octopamine distribution in the larvae and adults of the two species of moth Spodoptera littoralis and Manduca sexta. J Insect Physiol 32:987-993.
17. Davis NT, Homberg U, Teal PE, Altstein M, Agricola HJ, Hildebrand JG. 1996. Neuroanatomy and immunocytochemistry of the median neuroendocrine cells of the subesophageal ganglion of the tobacco hawkmoth, Manduca sexta: immunoreactivities to PBAN and other neuropeptides. Microsc Res Tech 35:201-229.
18. Dolzer J, Krannich S, Fischer K, Stengl M. 2001. Oscillations of the transepithelial potential of moth olfactory sensilla are influenced by octopamine and serotonin. J Exp Biol 204:2781-2794.
19. Donini A, Agricola HJ, Lange AB. 2001. Crustacean cardioactive peptide is a modulator of oviduct contractions in Locusta migratoria. J Insect Physiol 47:277-285.
20. Dudai Y, Buxbaum J, Corfas M. 1987. Foramidines interact with Drosophila octopamine receptors, alter the flies' behavior and reduce their learning ability. J Comp Physiol A 161:739-746.
21. Eckert M, Rapus J, Nurnberger A, Penzlin H. 1992. A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol 322:1-15.
22. Essig U. 1990. Subklassentypisierung von Antikörpern der Maus mittels ELISA. In: Peters JH, Baumgarten H, editors. Monoklonale Antikörper. Herstellung und Charakteri-sierung. Berlin: Springer, p 415-420.
23. Evans PD. 1980. Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317-474.
24. Fan RJ, Hansson BS. 2001. Olfactory discrimination conditioning in the moth Spodoptera littoralis. Physiol Behav 72:159-165.
25. Fan RJ, Anderson P, Hansson B. 1997. Behavioural analysis of olfactory conditioning in the moth Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). J Exp Biol 200:2969-2976.
26. Farooqui T, Robinson K, Vaessin H, Smith BH. 2003. Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23:5370-5380.
27. Fitch GK, Kammer AE. 1986. Effects of octopamine and forskolin on excitatory junction potentials of developing and adult moth Manduca sexta muscle. J Neurobiol 17:303-316.
28. Gauglitz S, Stevensen P. 1993. Octopamine enhances responsiveness of a locust movement detector interneurone (DCMD). In: Elsner H, Heisenberg M, editors. Gene-brain-behavior. New York: Thieme. p 608.
29. Grosmaitre X, Marion-Poll F, Renou M. 2001. Biogenic amines modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem Senses 26:653-661.
30. Hammer M. 1993. An unidentified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63.
31. Hammer M, Menzel R. 1995. Learning and memory in the honeybee. J Neurosci 3:1617-1630.
32. Hammer M, Menzel R. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146-156.
33. Harlow E, Lane D. 1988. Antibodies. A laboratory manual. New York: Cold Spring Harbor Laboratory Press.
34. Hartlieb E. 1996. Olfactory conditioning in the moth Heliothis virescens. Naturwissenschaften 83:87-88.
35. Hartlieb E, Anderson P, Hansson BS. 1999. Appetitive learning of odours with different behavioural meaning in moths. Physiol Behav 67:671-677.
36. Hildebrand H, Müller U. 1995. Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J Neurobiol 27:44-50.
37. Homberg U. 1994. Distribution of neurotransmitters in the insect brain. In: Rathmayer W, editor. Progress in Zoology, 40. Stuttgart: Gustav Fischer.
38. Homberg U, Hildebrand JG. 1989. Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tiss Res 258:1-24.
39. Homberg U, Montague RA, Hildebrand JG. 1988. Anatomy of antennocerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tiss Res 254:255-281.
40. Hoyle G. 1975. Evidence that insect dorsal unpaired median (DUM) neurons are octopaminergic. J Exp Zool 193:433-439.
41. Karsten U, Rudolph M. 1985. Monoclonal antibodies against tumor-associated antigens: mycoplasma as a major technical obstacle and its possible circumvention by azaserine selection medium. Arch Geschwulst 55:305-310.
42. Kearny JF, Radbruch A, Liesegang B, Rajewski K. 1979. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J Immunol 123:1548-1550.
43. Klaassen LW, Kammer AE, Fitch GK. 1986. Effects of octopamine on miniature junction potentials from developing and adult moth Manduca sexta muscle. J Neurobiol 17:291-302.
44. Kreissl S, Eichmuller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348:583-595.
45. Lehman HE, Klukas KA, Gilchrist LS, Mesce KA. 2000a. Steroid regulation of octopamine expression during metamorphic development of the moth Manduca sexta. J Comp Neurol 424:283-296.
46. Lehman HK, Murgiuc CM, Hildebrand JG. 2000b. Characterization and development regulation of tyramine-β-hydroxylase in the CNS of the moth Manduca sexta. Insect Biochem Mol Biol 30:377-386.
47. Linn CE, Roelofs WL. 1986. 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 3:161-171.
48. Linn CE, Campbell MG, Roelofs WL. 1992. Photoperiod cues and the modulatory action if octopamine and 5-hydroxytryptamine on locomotor and pheromone response in male gypsy moths, Lymantria dispar. Arch Insect Biochem Physiol 20:265-284.
49. Linn CE Jr, Poole KR, Roelofs WL. 1994. Studies on biogenic amines and their metabolites in nervous tissue and hemolymph of adult cabbage looper moths. III. Fate of injected octopamine, 5-hydroxytryptamine, and dopamine. Comp Biochem Physiol 108C:99-106.
50. Maxwell GD, Tait JF, Hildebrand JG. 1978. Regional synthesis of neurotransmitter candidates in the CNS of the moth Manduca sexta. Comp Biochem Physiol 61C:109-119.
51. Menzel R, Heyne A, Kinzel C, Gerber B, Fiala A. 1999. Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. Behav Neurosci 113:744-754.
52. Mercer A, Menzel R. 1982. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol 145A:363-368.
53. Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnick V. 1995. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 356:275-287.
54. Muller S. 1988. Peptide carrier conjugation. Techniques in biochemistry and molecular biology. In: Burdon RH, van Knippenberg PH, editors. Synthetic polypeptides as antigens, vol. 19. Amsterdam: Elsevier. p 95-130.
55. Murphy JF, Davies DH, Smith CJ. 1992. The development of enzyme-linked immunosorbent assays (ELISA) for catecholamines as antigens. In: Burdon RH, van Knippenberg PH, editors. Laboratory techniques in biochemistry and molecular biology, vol. 19. Amsterdam: Elsevier, p 95-130.
56. Orchard I, Lange A. 1984. Cyclic AMP in locust fat body: correlation with octopamine and adipokinetic hormones during flight. J Insect Physiol 30:901-904.
57. O'Shea M, Rowell CHF. 1975. A spike-transmitting electrical synapse between visual interneurones in the locust movement detector system. J Comp Physiol 97:143-158.
58. Pflüger HJ, Witten JL, Levine RB. 1993. Fate of abdominal ventral unpaired median cells during metamorphosis of the hawkmoth, Manduca sexta. J Comp Neurol 335:508-522.
59. Pophof B. 2000. Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J Comp Physiol A 186:307-313.
60. Pophof B. 2002. Octopamine enhances moth olfactory responses to pheromones, but not those to general odorants. J Comp Neurol 188:659-662.
61. Roeder T. 1999. Octopamine in invertebrates. Prog Neurobiol 59:533-561.
62. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. 2003. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495-10502.
63. Sinakevitch I, Niwa M, Strausfeld N. 2001. Octopamine immunoreactivity reveals homologous organization in the optic lobes and brain of the fly, honey bee and cockroach. Soc Neurosci Abstr 518.19.
64. Spörhase-Eichmann U, Vullings HG, Buijs RM, Horner M, Schurmann FW. 1992. Octopamine-imnumoreactive neurons in the central nervous system of the cricket, Gryllus bimaculatus. Cell Tiss Res 268:287-304.
65. Stelinski LL, Miller JR, Ressa NE, Gut LJ. 2003. Increased EAG responses of tortricid moths after prolonged exposure to plant volatiles: evidence for octopamine-mediated sensitization. J Insect Physiol 49:845-856.
66. Stern M. 1999. Octopamine in the locust brain: cellular distribution and functional significance in an arousal mechanism. Microsc Res Tech 45:135-141.
67. Stern M, Thompson KS, Zhou P, Watson DG, Midgley JM, Gewecke M, Bacon JP. 1995. Octopaminergic neurons in the locust brain: morphological, biochemical, and electrophysiological characterization of potential modulators of the visual system. J Comp Physiol 177:611-625.
68. Stevenson PA, Meuser S. 1997. Octopaminergic innervation and modulation of a locust flight steering muscle. J Exp Biol 200:633-642.
69. Stevenson PA, Spörhase-Eichmann U. 1995. Localization of octopaminergic neurones in insects. Comp Biochem Physiol A 110:203-215.
70. Stevenson PA, Pfluger HJ, Eckert M, Rapus J. 1992. Octopamine immunoreactive cell populations in the locust thoracic-abdominal nervous system. J Comp Neurol 315:382-397.
71. Strausfeld N. 1976. Atlas of an insect brain. Berlin: Springer.
72. Watson AHD. 1984. The dorsal unpaired median neurons of the locust metathoracic ganglion: neuronal structure and diversity, and synapse distribution. J Neurocytol 13:303-327.
73. Zars T, Fischer M, Schulz R, Heisenherg M. 2000. Localization of a short-term memory in Drosophila. Science 288:672-675.