Identification of distinct tyraminergic and octopaminergic neurons innervating the central complex of the desert locust, Schistocerca gregaria

Journal of Comparative Neurology

Volumn 521, Issue 9, 2013, Pages 2025-2041

  Homberg, Uwe ^a,b   Seyfarth, Jutta ^a   Binkle, Ulrike ^b   Monastirioti, Maria ^c   Alkema, Mark J ^d  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Biogenic amines; Central complex; Immunocytochemistry; Insect brain; Neuroanatomy; Neuromodulation

Indexed keywords

ANTISERUM; OCTOPAMINE; TYRAMINE; TYRAMINE BETA HYDROXYLASE; TYROSINE DECARBOXYLASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; BRAIN NERVE CELL; CCTOPAMINERGIC NEURON; CENTRAL COMPLEX; CONTROLLED STUDY; FEMALE; HEMISPHERE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INNERVATION; MALE; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; SCHISTOCERCA GREGARIA; SYNTHESIS; TYRAMINERGIC NEURON;

ANIMALS; BRAIN; GRASSHOPPERS; IMAGE PROCESSING, COMPUTER-ASSISTED; MIXED FUNCTION OXYGENASES; NEUROIMAGING; NEURONS; NEUROPIL; OCTOPAMINE; TYRAMINE; TYROSINE DECARBOXYLASE;

EID: 84876483434     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23269     Document Type: Article

References (68)

1. Agricola H, Hertel W, Penzlin H. 1988. Octopamin-neurotransmitter, neuromodulator, neurohormone. Zool Jb Physiol 92: 1-45.
2. Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR. 2005. Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46: 247-260.
3. Bacon JP, Thompson KSJ, Stern M. 1995. Identified octopaminergic neurons provide an arousal mechanism in the locust brain. J Neurophysiol 74: 2739-2743.
4. Bräunig P. 1991. Suboesophageal DUM neurons innervate the principal neuropiles of the locust brain. Philos Trans R Soc Lond B Biol Sci 332: 221-240.
5. Brembs B Christiansen F, Pflüger HJ, Duch C. 2007. Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J Neurosci 27: 11122-11131.
6. Busch S, Selcho M, Ito K, Tanimoto H. 2009. A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513: 643-667.
7. Cazzamali G, Klaerke DA, Grimmelikhuijzen CJP. 2005. A new family of insect tyramine receptors. Biochem Biophys Res Commun 338: 1189-1196.
8. Certel SJ, Savella MG, Schlegel DCF, Kravitz EA. 2007. Modulation of Drosophila male behavioral choice. Proc Natl Acad Sci U S A 104: 4706-4711.
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. Cole SH, Carney GE, McClungi CA, Willard SS, Taylor BJ, Hirsh J. 2005. Two functional but noncomplementing Drosophila tyrosine decarboxylase genes. J Biol Chem 280: 14948-14955.
11. Crocker A, Shahidullah M, Levitan IB, Sehgal A. 2010. Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behaviour. Neuron 65: 670-681.
12. Downer RGH, Hiripi L, Juhohs S. 1993. Characterization of the tyraminergic system in the central nervous system of the locust, Locusta migratoria migratorioides. Neurochem Res 18: 1245-1248.
13. Eckert M, Rapus J, Nürnberger A, Penzlin H. 1992. A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol 322: 1-15.
14. Evans PD. 1985. Octopamine. In: Kerkut GA, Gilbert L, editors. Comprehensive insect biochemistry, physiology and pharmacology. Oxford: Pergamon Press. p 499-529.
15. Farooqui T. 2007. Octopamine-mediated neuromodulation of insect senses. Neurochem Res 32: 1511-1529.
16. Fussnecker BL, Smith BH, Mustard JA. 2006. Octopamine and tyramine influence the behavioral profile of locomotor activity in the honey bee (Apis mellifera). J Insect Physiol 52: 1083-1092.
17. Gebhardt S, Homberg U. 2004. Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell Tissue Res 317: 195-205.
18. Giurfa M. 2006. Associative learning: the instructive function of biogenic amines. Curr Biol 16: R892-895.
19. Heinze S, Homberg U. 2007. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315: 995-997.
20. Heinze S, Homberg U. 2008. Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511: 454-478.
21. Heinze S, Homberg U. 2009. Linking the input to the output: new sets of neurons complement the polarization vision network in the locust central complex. J Neurosci 29: 4911-4921.
22. Heinze S, Gotthardt S, Homberg U. 2009. Transformation of polarized light information in the central complex of the locust. J Neurosci 29: 11783-11793.
23. Hirashima A, Yamaji H, Yoshizawa T, Kuwano E, Eto M. 2007. Effect of tyramine and stress on sex-pheromone production in the pre- and post-mating silkworm moth, Bombyx mori. J Insect Physiol 53: 1242-1249.
24. Homberg U. 1991. Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303: 245-254.
25. Homberg U. 2008. Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37: 347-362.
26. Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B. 2011. Central neural coding of sky polarization in insects. Philos Trans R Soc Lond B Biol Sci 366: 680-687.
27. Hoyer SC, Eckart A, Herrel A, Zars T, Fisher SA, Hirsh J, Heisenberg M. 2008. Octopamine in male aggression of Drosophila. Curr Biol 18: 159-167.
28. Kloppenburg P, Erber J. 1995. The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). II. Electrophysiological analysis of motion-sensitive neurons in the lobula. J Comp Physiol A176: 119-129.
29. Konings PN, Vullings HG, Geffard M, Buijs RM, Diederen JH, Jansen WF. 1988. Immunocytochemical demonstration of octopamine immunoreactive cells in the nervous system of Locusta migratoria and Schistocerca gregaria. Cell Tissue Res 251: 371-379.
30. Kononenko NL, Wolfenberg H, Pflüger H-J. 2009. Tyramine as an independent transmitter and a precursor of octopamine in the locust central nervous system: an immunocytochemical study. J Comp Neurol 512: 433-452.
31. Koon AC, Ashley J, Barria R, DasGupta S, Brain R, Waddell S, Alkema MJ, Budnik V. 2011. Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat Neurosci 14: 190-199.
32. Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 348: 583-595.
33. Lange AB. 2009. Tyramine: from octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162: 18-26.
34. Lehman HK, Murgiuc CM, Hildebrand JG. 2000. Characterization and developmental regulation of tyramine-β-hydroxylase in the CNS of the moth, Manduca sexta. Insect Biochem Mol Biol 30: 377-386.
35. Lehman HK, Schulz DJ, Barron AB, Wraight L, Hardison C, Whitney S, Takeuchi H, Paul RK, Robinson GE. 2006. Division of labor in the honey bee (Apis mellifera): the role of tyramine β-hydroxylase. J Exp Biol 209: 2774-2784.
36. Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf R, Heisenberg M, Liu L. 2006. Distinct memory traces for two visual features in the Drosophila brain. Nature 439: 551-556.
37. Longden KD, Krapp HG. 2009. State-dependent performance of optic-flow processing interneurons. J Neurophysiol 102: 3606-3618.
38. Merlin C, Heinze S, Reppert SM. 2012. Unraveling navigational strategies in migratory insects. Curr Opin Neurobiol 22: 353-361.
39. Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik K. 1995. Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 356: 275-287.
40. Monastirioti M, Linn, CE, White, K. 1996. Characterization of Drosophila tyramine β-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 16: 3900-3911.
41. Müller M, Homberg U, Kühn A. 1997. Neuroarchitecture of the lower division of the central body in the brain of the locust Schistocerca gregaria. Cell Tissue Res 288: 159-176.
42. Nagaya Y, Kutsukake M, Chigusa SI, Komatsu A. 2002. A trace amine, tyramine, functions as a neuromodulator in Drosophila melanogaster. Neurosci Lett 329: 324-328.
43. Pflüger H-J, Stevenson PA. 2005. Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34: 379-396.
44. Pirri, JK, McPherson AD, Donnelly JL, Francis MM, Alkema MJ. 2009. A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response. Neuron 62: 526-538.
45. Potter CJ, Luo L. 2008. Octopamine fuels fighting flies. Nat Neurosci 11: 889-890.
46. Rillich J, Stevenson PA. 2011. Winning fights induces hyperaggression via the action of the biogenic amine octopamine in crickets. PLoS One 6: e28891.
47. Roeder T. 1999. Octopamine in invertebrates. Prog Neurobiol 59: 533-561.
48. Roeder T. 2005. Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50: 447-477.
49. Sakura M, Lambrinos D, Labhart T. 2007. Polarized skylight navigation in insects: model and electrophysiology of e-vector coding by neurons in the central complex. J Neurophysiol 99: 667-682.
50. Saraswati S, Fox LE, Soll DR, Wu C-F. 2003. Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58: 425-441.
51. Sinakevitch I, Strausfeld NJ. 2006. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol 494: 460-475.
52. Sinakevitch I, Niwa M, Strausfeld NJ. 2005. Octopamine-like immunoreactivity in the honeybee and cockroach: comparable organization in the brain and suboesophageal ganglion. J Comp Neurol 488: 233-254.
53. Sombati S, Hoyle G. 1984. Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J Neurobiol 15: 481-506.
54. Spörhase-Eichmann U, Vullings HGB, Buijs RM, Hörner M, Schürmann F-W. 1992. Octopamine-immunoreactive neurons in the central nervous system of the cricket, Gryllus bimaculatus. Cell Tissue Res 268: 287-304.
55. Stern M. 1999. Octopamine in the locust brain: cellular distribution and functional significance in an arousal mechanism. Microsc Res Tech 45: 135-141.
56. Stern M, Thompson KSJ, Zhou P, Watson DG, Midgley JM, Gewecke M, Bacon JP. 1995. Octopaminergic neurons in the locust brain: morphological, biochemical, and electrophysiological characterisation of potential modulators of the visual system. J Comp Physiol A 177: 611-625.
57. Sternberger LA. 1979. Immunocytochemistry. New York: John Wiley & Sons.
58. Stevenson PA, Spörhase-Eichmann U. 1995. Localization of octopaminergic neurons in insects. Comp Biochem Physiol A Physiol 110: 203-215.
59. Stevenson PA, Hofmann HA, Schoch K, Schildberger K. 2000. The fight and flight responses of crickets depleted of biogenic amines. J Neurobiol 43: 107-120.
60. Stevenson PA, Dyakonova V, Rillich J, Schildberger K. 2005. Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25: 1431-1441.
61. Strauss R. 2002. The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12: 633-638.
62. Triphan T, Poeck B, Neuser K, Strauss R. 2010. Visual targeting of motor actions in climbing Drosophila. Curr Biol 20: 663-668.
63. Unoki S, Matsumoto Y, Mizunami M. 2006. Roles of octopaminergic and dopaminergic neurons in mediating reward and punishment signals in insect visual learning. Eur J Neurosci 24: 2031-2038.
64. Verlinden H, Vleugels R, Marchal E, Badisco L, Pflüger H-J, Blenau W, Vanden Broeck J. 2010. The role of octopamine in locusts and other arthropods. J Insect Physiol 56: 854-867.
65. Vierk R, Pflüger HJ, Duch C. 2009. Differential effects of octopamine and tyramine on the central pattern generator for Manduca flight. J Comp Physiol A 195: 265-277.
66. Wendt B, Homberg U. 1992. Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol 321: 387-403.
67. Williams JLD. 1975. Anatomical studies of the insect central nervous system: a ground plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool Lond 176: 67-86.
68. Zhou C, Rao Y, Rao Y. 2008. A subset of octopaminergic neurons are important for Drosophila aggression. Nat Neurosci 11: 1059-1067.