Neuropeptides in insect mushroom bodies

Arthropod Structure and Development

Volumn 41, Issue 3, 2012, Pages 199-226

  Heuer, Carsten M ^a   Kollmann, Martin ^a   Binzer, Marlene ^a   Schachtner, Joachim ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Evolution; Mushroom body; Network; Neuropeptides; Neuropil

Indexed keywords

ALLATOSTATIN; ALLATOSTATIN A; ALLATOTROPIN; ALLOSTATIN B; FMRFAMIDE RELATED PEPTIDE; INSECT PROTEIN; MYOINHIBITORY PEPTIDE; NEUROPEPTIDE; ORCOKININ; SHORT NEUROPEPTIDE F; SIFAMIDE PROTEIN; TACHYKININ; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INSECT; MUSHROOM BODY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW;

ANIMALS; FEMALE; IMMUNOHISTOCHEMISTRY; INSECT PROTEINS; INSECTS; MALE; MICROSCOPY, CONFOCAL; MUSHROOM BODIES; NEURONS; NEUROPEPTIDES; SEQUENCE ANALYSIS, PROTEIN;

BASIDIOMYCOTA; HEXAPODA;

EID: 84860549978     PISSN: 14678039     EISSN: 18735495     Source Type: Journal    
DOI: 10.1016/j.asd.2012.02.005     Document Type: Review

References (263)

1. Altstein M., Nässel D.R. Neuropeptide signaling in insects. Neuropeptide Systems as Targets for Parasite and Pest Control Landes Bioscience and Science, Austin, TX 2010, 155-165. Springer. T.G. Geary, A.G. Maule (Eds.).
2. Baggerman G., Boonen K., Verleyen P., De Loof A., Schoofs L. Peptidomic analysis of the larval Drosophila melanogaster central nervous system by two-dimensional capillary liquid chromatography quadrupole time-of-flight mass spectrometry. Journal of Mass Spectrometry 2005, 40:250-260.
3. Bang S., Hyun S., Hong S.-T., Kang J., Jeong K., Park J.-J., Choe J., Chung J. Dopamine signalling in mushroom bodies regulates temperature-preference behaviour in Drosophila. PLoS Genetics 2011, 7:e1001346.
4. Barth M., Heisenberg M. Vision affects mushroom bodies and central complex in Drosophila melanogaster. Learning and Memory 1997, 4:219-229.
5. Bell R.A., Joachim F.A. Techniques for rearing laboratory colonies of the tobacco hornworm, Manduca sexta, and pink ballworms. Annals of the Entomological Society of America 1978, 69:365-373.
6. Bellés X., Graham L.A., Bendena W.G., Ding Q.I., Edwards J.P., Weaver R.J., Tobe S.S. The molecular evolution of the allatostatin precursor in cockroaches. Peptides 1999, 20:11-22.
7. Berg B.G., Schachtner J., Utz S., Homberg U. Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens. Cell and Tissue Research 2007, 327:385-398.
8. Berghammer A., Bucher G., Maderspacher F., Klingler M. A system to efficiently maintain embryonic lethal mutations in the flour beetle Tribolium castaneum. Development Genes and Evolution 1999, 209:382-389.
9. Bhalerao S., Sen A., Stocker R., Rodrigues V. Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. Journal of Neurobiology 2003, 54:577-592.
10. Blackburn M.B., Wagner R.M., Kochansky J.P., Harrison D.J., Thomas-Laemont P., Raina A.K. The identification of two myoinhibitory peptides, with sequence similiarities to the galanins, isolated from the ventral nerve cord of Manduca sexta. Regulatory Peptides 1995, 57:213-219.
11. Blackburn M.B., Jaffe H., Kochansky J., Raina A.K. Identification of four additional myoinhibitory peptides (MIPs) from the ventral nerve cord of Manduca sexta. Archives of Insect Biochemistry and Physiology 2001, 48:121-128.
12. Boerjan B., Cardoen D., Bogaerts A., Landuyt B., Schoofs L., Verleyen P. Mass spectrometric profiling of (neuro)-peptides in the worker honeybee, Apis mellifera. Neuropharmacology 2010, 58:248-258.
13. Breidbach O., Wegerhoff R. FMRFamide-like immunoreactive neurons in the brain of the beetle, Tenebrio molitor L. (Coleoptera: Tenebrionidae): constancies and variations in development from the embryo to the adult. International Journal of Insect Morphology and Embryology 1994, 23:383-404.
14. Brown M., Klowden M., Crim J., Young L., Shrouder L., Lea A. Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. Journal of Insect Physiology 1994, 40:399-406.
15. Bungart D., Dircksen H., Keller R. Quantitative determination and distribution of the myotropic neuropeptide orcokinin in the nervous system of astacidean crustaceans. Peptides 1994, 15:393-400.
16. Carlsson M.A., Diesner M., Schachtner J., Nässel D.R. Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits. Journal of Comparative Neurology 2010, 518:3359-3380.
17. Cassenaer S., Laurent G. Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 2007, 448:709-713.
18. Cassenaer S., Laurent G. Conditional modulation of spike-timing-dependent plasticity for olfactory learning. Nature Advance Online Publication 2012, 10.1038/nature10776.
19. Chen M.-E., Pietrantonio P.V. The short neuropeptide F-like receptor from the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). Archives of Insect Biochemistry and Physiology 2006, 61:195-208.
20. Christie A.E., Sousa G.L., Rus S., Smith C.M., Towle D.W., Hartline D.K., Dickinson P.S. Identification of A-type allatostatins possessing-YXFGI/Vamide carboxy-termini from the nervous system of the copepod crustacean Calanus finmarchicus. General and Comparative Endocrinology 2008, 155:526-533.
21. Christie A.E., Nolan D.H., Ohno P., Hartline N., Lenz P.H. Identification of chelicerate neuropeptides using bioinformatics of publicly accessible expressed sequence tags. General and Comparative Endocrinology 2010, 170:144-155.
22. Clynen E., Baggerman G., Veelaert D., Cerstiaens A., Van der Horst D., Harthoorn L., Derua R., Waelkens E., De Loof A., Schoofs L. Peptidomics of the pars intercerebralis-corpus cardiacum complex of the migratory locust, Locusta migratoria. European Journal of Biochemistry/FEBS 2001, 268:1929-1939.
23. s signaling in Drosophila mushroom bodies. Science 1996, 274:2104-2107.
24. Crittenden J.R., Skoulakis E.M.C., Han K.-A., Kalderon D., Davis R.L. Tripartite mushroom body architecture revealed by antigenic markers. Learning and Memory 1998, 5:38-51.
25. Davey M., Duve H., Thorpe A., East P. Characterisation of the helicostatin peptide precursor gene from Helicoverpa armigera (Lepidoptera: Noctuidae). Insect Biochemistry and Molecular Biology 1999, 29:1119-1127.
26. Davis N.T., Veenstra J.A., Feyereisen R., Hildebrand J.G. Allatostatin-like-immunoreactive neurons of the tobacco hornworm, Manduca sexta, and isolation and identification of a new neuropeptide related to cockroach allatostatins. Journal of Comparative Neurology 1997, 385:265-284.
27. Davis N.T., Blackburn M.B., Golubeva E.G., Hildebrand J.G. Localization of myoinhibitory peptide immunoreactivity in Manduca sexta and Bombyx mori, with indications that the peptide has a role in molting and ecdysis. Journal of Experimental Biology 2003, 206:1449-1460.
28. Davis R.L. Olfactory learning. Neuron 2004, 44:31-48.
29. Davis R.L. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annual Review of Neuroscience 2005, 28:275-302.
30. de Belle J.S., Heisenberg M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 1994, 263:692-695.
31. de Jong-Brink M., ter Maat A., Tensen C.P. NPY in invertebrates: molecular answers to altered functions during evolution. Peptides 2001, 22:309-315.
32. Dircksen H., Skiebe P., Abel B., Agricola H., Buchner K., Muren J.E., Nässel D.R. Structure, distribution, and biological activity of novel members of the allatostatin family in the crayfish Orconectes limosus. Peptides 1999, 20:695-712.
33. Doeffinger C., Hartenstein V., Stollewerk A. Compartmentalization of the precheliceral neuroectoderm in the spider Cupiennius salei: development of the arcuate body, optic ganglia, and mushroom body. Journal of Comparative Neurology 2010, 518:2612-2632.
34. Donly B.C., Ding Q., Tobe S.S., Bendena W.G. Molecular cloning of the gene for the allatostatin family of neuropeptides from the cockroach Diploptera punctata. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:8807-8811.
35. Dubnau J., Grady L., Kitamoto T., Tully T. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 2001, 411:476-480.
36. Duve H., Johnsen A.H., East P.D., Thorpe A. Comparative aspects of the FMRFamides of blowfl{ligature}ies: isolation of the peptides, genes, and functions. Perspective in Comparative Endocrinology 1994, 91-96. National Research Council of Canada, Ottawa. K.G. Davey, R.E. Peter, S.S. Tobe (Eds.).
37. Duve H., East P., Thorpe A. Regulation of lepidopteran foregut movement by allatostatins and allatotropin from the frontal ganglion. Journal of Comparative Neurology 1999, 413:405-416.
38. Duve H., Audsley N., Weaver R.J., Thorpe A. Triple co-localisation of two types of allatostatin and an allatotropin in the frontal ganglion of the lepidopteran Lacanobia oleracea (Noctuidae): innervation and action on the foregut. Cell and Tissue Research 2000, 300:153-163.
39. Duve H., Johnsen a.H., Sewell J.C., Scott a.G., Orchard I., Rehfeld J.F., Thorpe A. Isolation, structure, and activity of -Phe-Met-Arg-Phe-NH2 neuropeptides (designated calliFMRFamides) from the blowfly Calliphora vomitoria. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:2326-2330.
40. Duve H., Johnsen a.H., Scott a.G., Yu C.G., Yagi K.J., Tobe S.S., Thorpe A. Callatostatins: neuropeptides from the blowfly Calliphora vomitoria with sequence homology to cockroach allatostatins. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:2456-2460.
41. Ehmer B., Gronenberg W. Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). Journal of Comparative Neurology 2002, 451:362-373.
42. Elliott K.L., Hehman G.L., Stay B. Isolation of the gene for the precursor of Phe-Gly-Leu-amide allatostatins in the termite Reticulitermes flavipes. Peptides 2009, 30:855-860.
43. Elliott K.L., Chan K.K., Stay B. Evidence for a Phe-Gly-Leu-amide-like allatostatin in the beetle Tenebrio molitor. Peptides 2010, 31:402-407.
44. Erber J., Masuhr T., Menzel R. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiological Entomology 1980, 5:343-358.
45. Espinoza E., Carrigan M., Thomas S.G., Shaw G., Edison A.S. A statistical view of FMRFamide neuropeptide diversity. Molecular Neurobiology 2000, 21:35-56.
46. Fahrbach S.E., Dobrin S. The how and why of structural plasticity in the honey bee brain. Cognitive Ecology II 2009, 37-48. University of Chicago Press. R. Dukas, J. Ratcliffe (Eds.).
47. Fahrenbach W.H. The brain of the horseshoe crab (Limulus polyphemus) II. Architecture of the corpora pedunculata. Tissue and Cell 1977, 9:157-166.
48. Farris S.M., Sinakevitch I. Development and evolution of the insect mushroom bodies: towards the understanding of conserved developmental mechanisms in a higher brain center. Arthropod Structure and Development 2003, 32:79-101.
49. Farris S.M., Strausfeld N.J. Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation. Journal of Comparative Neurology 2001, 439:331-351.
50. Farris S.M. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Structure and Development 2005, 34:211-234.
51. Farris S.M. Developmental organization of the mushroom bodies of Thermobia domestica (Zygentoma, Lepismatidae): insights into mushroom body evolution from a basal insect. Evolution and Development 2005, 7:150-159.
52. Farris S.M. Structural, functional and developmental convergence of the insect mushroom bodies with higher brain centers of vertebrates. Brain, Behavior and Evolution 2008, 72:1-15.
53. Farris S.M. Tritocerebral tract input to the insect mushroom bodies. Arthropod Structure and Development 2008, 37:492-503.
54. Farris S.M. Evolutionary convergence of higher brain centers spanning the protostome-deuterostome boundary. Brain, Behavior and Evolution 2008, 72:106-122.
55. Farris S.M. Locusts provide clues to insect mushroom body function. Brain, Behavior and Evolution 2011, 77:3-4.
56. Feng G., Reale V., Chatwin H., Kennedy K., Venard R., Ericsson C., Yu K., Evans P.D., Hall L.M. Functional characterization of a neuropeptide F-like receptor from Drosophila melanogaster. European Journal of Neuroscience 2003, 18:227-238.
57. Fiala A., Müller U., Menzel R. Reversible downregulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. Journal of Neuroscience 1999, 19:10125-10134.
58. Fiala A. Olfaction and olfactory learning in Drosophila: recent progress. Current Opinion in Neurobiology 2007, 17:720-726.
59. Flögel J.H.L. Ueber den feineren Bau des Arthropodengehirns. Tageblatt der Versammlung Deutscher Naturforscher und Ärzte 1876, 49:115-120.
60. Fukushima R., Kanzaki R. Modular subdivision of mushroom bodies by Kenyon cells in the silkmoth. Journal of Comparative Neurology 2009, 513:315-330.
61. Fusé M., Zhang J.R., Partridge E., Nachman R.J., Orchard I., Bendena W.G., Tobe S.S. Effects of an allatostatin and a myosuppressin on midgut carbohydrate enzyme activity in the cockroach Diploptera punctata. Peptides 1999, 20:1285-1293.
62. Galizia C.G., Rössler W. Parallel olfactory systems in insects: anatomy and function. Annual Review of Entomology 2010, 55:399-420.
63. Gard A.L., Lenz P.H., Shaw J.R., Christie A.E. Identification of putative peptide paracrines/hormones in the water flea Daphnia pulex (Crustacea; Branchiopoda; Cladocera) using transcriptomics and immunohistochemistry. General and Comparative Endocrinology 2009, 160:271-287.
64. Gronenberg W., Heeren S., Hölldobler B. Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. Journal of Experimental Biology 1996, 199:2011-2019.
65. Gronenberg W. Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain. Journal of Insect Physiology 1986, 32:695-704.
66. Gronenberg W. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. Journal of Comparative Neurology 2001, 435:474-489.
67. Grünewald B. Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera. Journal of Comparative Physiology A 1999, 185:565-576.
68. Guo F., Yi W., Zhou M., Guo A. Go signaling in mushroom bodies regulates sleep in Drosophila. Sleep 2011, 34:273-281.
69. Hammer M., Menzel R. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learning and Memory 1998, 5:146-156.
70. Hammer M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 1993, 366:59-63.
71. Hanström B. Vergleichende Anatomie des Nervensystems der wirbellosen Tiere unter Berücksichtigung seiner Funktion 1928, Springer, Berlin, 368 pp.
72. Hauser F., Neupert S., Williamson M., Predel R., Tanaka Y., Grimmelikhuijzen C.J.P. Genomics and peptidomics of neuropeptides and protein hormones present in the parasitic wasp Nasonia vitripennis. Journal of Proteome Research 2010, 9:5296-5310.
73. Heisenberg M., Borst a, Wagner S., Byers D. Drosophila mushroom body mutants are deficient in olfactory learning. Journal of Neurogenetics 1985, 2:1-30.
74. Heisenberg M. What do the mushroom bodies do for the insect brain? An introduction. Learning and Memory 1998, 5:1-10.
75. Heisenberg M. Mushroom body memoir: from maps to models. Nature Reviews Neuroscience 2003, 4:266-275.
76. Heuer C.M., Loesel R. Immunofluorescence analysis of the internal brain anatomy of Nereis diversicolor (Polychaeta, Annelida ). Cell and Tissue Research 2008, 331:713-724.
77. Heuer C.M., Müller C.H.G., Todt C., Loesel R. Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida. Frontiers in Zoology 2010, 7:1-21.
78. Hewes R.S., Taghert P.H. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Research 2001, 11:1126-1142.
79. Hildebrand J.G., Shepherd G.M. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annual Review of Neuroscience 1997, 20:595-631.
80. Hinke W. Das relative postembryonale Wachstum der Hirnteile von Culex pipiens, Drosophila melanogaster und Drosophila-Mutanten. Zeitschrift für Morphologie und ökologie der Tiere 1961, 50:81-118.
81. Hofer S., Dircksen H., Tollbäck P., Homberg U. Novel insect orcokinins: characterization and neuronal distribution in the brains of selected dicondylian insects. Journal of Comparative Neurology 2005, 490:57-71.
82. Holmgren N. Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Kungliga Svenska Vetenskaps Akademiens Handlingar 1916, 56:1-303.
83. Homberg U., Kingan T.G., Hildebrand J.G. Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell and Tissue Research 1990, 259:401-419.
84. Homberg U., Brandl C., Clynen E., Schoofs L., Veenstra J.A. Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria. Cell and Tissue Research 2004, 318:439-457.
85. Homberg U. Neurotransmitters and neuropeptides in the brain of the locust. Microscopy Research and Technique 2002, 56:189-209.
86. Honegger H., Schürmann F. Cobalt sulphide staining of optic fibres in the brain of the cricket, Gryllus campestris. Cell and Tissue Research 1975, 225:213-225.
87. Hong S.-T., Bang S., Hyun S., Kang J., Jeong K., Paik D., Chung J., Kim J. cAMP signalling in mushroom bodies modulates temperature preference behaviour in Drosophila. Nature 2008, 454:771-775.
88. Huber F. Untersuchen ueber die Funktion des Zentralnervensystems und insbesondere des Gehirnes bei der Fortbewegung und der Lauterzeugung der Grillen. Zeitschrift für Vergleichende Physiologie 1960, 44:60-132.
89. Hummon A.B., Richmond T.A., Verleyen P., Baggerman G., Huybrechts J., Ewing M.a., Vierstraete E., Rodriguez-Zas S.L., Schoofs L., Robinson G.E., Sweedler J.V. From the genome to the proteome: uncovering peptides in the Apis brain. Science 2006, 314:647-649.
90. Huybrechts J., Nusbaum M., Bosch L.V., Baggerman G., De Loof A., Schoofs L. Neuropeptidomic analysis of the brain and thoracic ganglion from the Jonah crab, Cancer borealis. Biochemical and Biophysical Research Communications 2003, 308:535-544.
91. Huybrechts J., De Loof A., Schoofs L. Diapausing Colorado potato beetles are devoid of short neuropeptide FI and II. Biochemical and Biophysical Research Communications 2004, 317:909-916.
92. Huybrechts J., Bonhomme J., Minoli S., Prunier-Leterme N., Dombrovsky A., Abdel-Latief M., Robichon A., Veenstra J.A., Tagu D. Neuropeptide and neurohormone precursors in the pea aphid, Acyrthosiphon pisum. Insect Molecular Biology 2010, 19(Suppl. 2):87-95.
93. Ignell R., Root C.M., Birse R.T., Wang J.W., Nässel D.R., Winther A.M.E. Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:13070-13075.
94. Ito K., Suzuki K., Estes P., Ramaswami M., Yamamoto D., Strausfeld N.J. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melano- gaster Meigen. Learning and Memory 1998, 5:52-77.
95. Janssen I., Schoofs L., Spittaels K., Neven H., Vanden Broeck J., Devreese B., van Beeumen J., Shabanowitz J., Hunt D.F., De Loof A. Isolation of NEB-LFamide, a novel myotopic neuropeptide from the grey fleshfly. Molecular and Cellular Endocrinology 1996, 117:157-165.
96. Johard H.A.D., Muren J.E., Nichols R., Larhammar D.S., Nassel D.R. A putative tachykinin receptor in the cockroach brain: molecular cloning and analysis of expression by means of antisera to portions of the receptor protein. Brain Research 2001, 919:94-105.
97. Johard H.A.D., Enell L.E., Gustafsson E., Trifilieff P., Veenstra J.A., Nässel D.R. Intrinsic neurons of drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. Journal of Comparative Neurology 2008, 507:1479-1496.
98. Johard H.A.D., Yoishii T., Dircksen H., Cusumano P., Rouyer F., Helfrich-Förster C., Nässel D.R. Peptidergic clock neurons in Drosophila: ion transport peptide and short neuropeptide F in subsets of dorsal and ventral lateral neurons. Journal of Comparative Neurology 2009, 519:59-73.
99. Joiner W.J., Crocker A., White B.H., Sehgal A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 2006, 441:757-760.
100. Jortner R.A., Farivar S.S., Laurent G. A simple connectivity scheme for sparse coding in an olfactory system. Journal of Neuroscience 2007, 27:1659-1669.
101. Kataoka H., Toschi A., Li J.P., Carney R.L., Schooley D.A., Kramer S.J. Identification of an allatotropin from adult Manduca sexta. Science 1989, 243:1481-1483.
102. Keenan C.L., Coss R., Koopowitz H. Cytoarchitecture of primitive brains: golgi studies in flatworms. Journal of Comparative Neurology 1981, 195:697-716.
103. Keene A.C., Waddell S. Drosophila olfactory memory: single genes to complex neural circuits. Nature Reviews: Neuroscience 2007, 8:341-354.
104. Kim Y.-J., Bartalska K., Audsley N., Yamanaka N., Yapici N., Lee J.-Y., Kim Y.-C., Markovic M., Isaac E., Tanaka Y., Dickson B.J. MIPs are ancestral ligands for the sex peptide receptor. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:6520-6525.
105. Kingan T.G., Teplow D.B., Phillips J.M., Riehm J.P., Rao K.R., Hildebrand J.G., Homberg U., Kammer A.E., Jardine I., Griffin P.R. A new peptide in the FMRFamide family isolated from the CNS of the hawkmoth, Manduca sexta. Peptides 1990, 11:849-856.
106. Kingan T., Shabanowitz J., Hunt D., Witten J. Characterization of two myotrophic neuropeptides in the FMRFamide family from the segmental ganglia of the moth Manduca sexta: candidate neurohormones and neuromodulators. Journal of Experimental Biology 1996, 199:1095-1104.
107. Klagges B.R.E., Heimbeck G., Godenschwege T.A., Hofbauer A., Pflugfelder G.O., Reifegerste R., Reisch D., Schaupp M., Buchner S., Buchner E. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. Journal of Neuroscience 1996, 16:3154-3165.
108. Koladich P.M., Cusson M., Bendena W.G., Tobe S.S., McNeil J.N. Cardioacceleratory effects of Manduca sexta allatotropin in the true armyworm moth, Pseudaletia unipuncta. Peptides 2002, 23:645-651.
109. Kollmann M., Huetteroth W., Schachtner J. Brain organization in Collembola (springtails). Arthropod Structure and Development 2011, 40:304-316.
110. Kollmann M., Minoli S., Bonhomme J., Homberg U., Schachtner J., Tagu D., Anton S. Revisiting the anatomy of the central nervous system of a hemimetabolous model insect species: the pea aphid Acyrthosiphon pisum. Cell and Tissue Research 2011, 343:343-355.
111. Kolodziejczyk A., Nässel D.R. A novel wide-field neuron with branches in the lamina of the Drosophila visual system expresses myoinhibitory peptide and may be associated with the clock. Cell and Tissue Research 2010, 343:357-369.
112. Kreissl S., Strasser C., Galizia C.G. Allatostatin immunoreactivity in the honeybee brain. Journal of Comparative Neurology 2010, 518:1391-1417.
113. Kutsch W., Breidbach O. Homologous structures in the nervous systems of Arthropoda. Advances in Insect Physiology 24 1994, 1-113. TJ Press Ltd, Padstow, Cornwall. P.D. Evans (Ed.).
114. Lane M.E., Kalderon D. Genetic investigation of cAMP-dependent protein kinase function in Drosophila development. Genes and Development 1993, 7:1229-1243.
115. Lange A.B., Peeff N.M., Orchard I. Isolation, sequence, and bioactivity of FMRFamide-related peptides from the locust ventral nerve cord. Peptides 1994, 15:1089-1094.
116. Lange A.B., Bendena W.G., Tobe S.S. The effect of the thirteen Dip-allatostatins on myogenic and induced contractions of the cockroach (Diploptera punctata) hindgut. Journal of Insect Physiology 1995, 41:581-588.
117. Lee K.Y., Horodyski F.M., Chamberlin M.E. Inhibition of midgut ion transport by allatotropin (Mas-AT) and Manduca FLRFamides in the tobacco hornworm Manduca sexta. Journal of Experimental Biology 1998, 201:3067-3074.
118. Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999, 126:4065-4076.
119. Lee K.-Y., Chamberlin M.E., Horodyski F.M. Biological activity of Manduca sexta allatotropin-like peptides, predicted products of tissue-specific and developmentally regulated alternatively spliced mRNAs. Peptides 2002, 23:1933-1941.
120. Lee K.-S., You K.-H., Choo J.-K., Han Y.-M., Yu K. Drosophila short neuropeptide F regulates food intake and body size. Journal of Biological Chemistry 2004, 279:50781-50789.
121. Lenz C., Williamson M., Grimmelikhuijzen C.J. Molecular cloning and genomic organization of an allatostatin preprohormone from Drosophila melanogaster. Biochemical and Biophysical Research Communications 2000, 273:1126-1131.
122. Li Y., Strausfeld N.J. Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. Journal of Comparative Neurology 1997, 387:631-650.
123. Li Y., Strausfeld N.J. Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. Journal of Comparative Neurology 1999, 409:647-663.
124. Li Y., Hernandez-Martinez S., Noriega F.G. Inhibition of juvenile hormone biosynthesis in mosquitoes: effect of allatostatic head factors, PISCF- and YXFGL-amide-allatostatins. Regulatory Peptides 2004, 118:175-182.
125. Li B., Predel R., Neupert S., Hauser F., Tanaka Y., Cazzamali G., Williamson M., Arakane Y., Verleyen P., Schoofs L., Schachtner J., Grimmelikhuijzen C.J.P., Park Y. Genomics, transcriptomics, and peptidomics of neuropeptides and protein hormones in the red flour beetle Tribolium castaneum. Genome Research 2008, 18:113-122.
126. Liu L., Wolf R., Ernst R., Heisenberg M. Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 1999, 400:753-756.
127. Loesel R., Heuer C.M. The mushroom bodies - prominent brain centres of arthropods and annelids with enigmatic evolutionary origin. Acta Zoologica 2010, 91:29-34.
128. Lorenz M.W., Kellner R., Hoffmann K.H. Identification of two allatostatins from the cricket, Gryllus birnaculatus de Geer (Ensifera, Gryllidae): additional members of a family of neuropeptides inhibiting juvenile hormone biosynthesis. Regulatory Peptides 1995, 57:227-236.
129. Lorenz M.W., Kellner R., Hoffmann K.H. A family of neuropeptides that inhibit juvenile hormone biosynthesis in the cricket, Gryllus bimaculatus. Journal of Biological Chemistry 1995, 270:21103-21108.
130. Lorenz M.W., Kellner R., Hoffmann K.H., Gäde G. Identification of multiple peptides homologous to cockroach and cricket allatostatins in the stick insect Carausius morosus. Insect Biochemistry and Molecular Biology 2000, 30:711-718.
131. Mao Z., Davis R.L. Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Frontiers in Neural Circuits 2009, 3:5.
132. Marder E., Bucher D. Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annual Review of Physiology 2007, 69:291-316.
133. Marder E., Taylor A.L. Multiple models to capture the variability in biological neurons and networks. Nature Neuroscience 2011, 14:133-138.
134. Marder E., Calabrese R.L., Nusbaum M.P., Trimmer B. Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous systems of the rock crab, Cancer borealis, and the spiny lobster, Panulirus interruptus. Journal of Comparative Neurology 1987, 259:150-163.
135. Martin J., Ernst R., Heisenberg M. Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learning and Memory 1998, 5:179-191.
136. Masek P., Scott K. Limited taste discrimination in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:14833-14838.
137. Matsumoto S., Brown M., Crim J., Vigna S., Lea A. Isolation and primary structure of neuropeptides from the mosquito, Aedes aegypti, immunoreactive to FMRFamide antiserum. Insect Biochemistry 1989, 19:277-283.
138. Maule A.G., Shaw C., Halton D.W., Thim L., Johnston C.F., Fairweather I., Buchanan K.D. Neuropeptide F: a novel parasitic flatworm regulatory peptide from Moniezia expansa (Cestoda: Cyclophyllidea). Parasitology 1991, 102:309-316.
139. Mcguire S.E., Le P.T., Davis R.L. The role of Drosophila mushroom body signaling in olfactory memory. Science 2001, 10:1126-1129.
140. McNeil J.N., Tobe S.S. Flights of fancy: possible roles of allatostatin and allatotropin in migration and reproductive success of Pseudaletia unipuncta. Peptides 2001, 22:271-277.
141. Medina L., Abellán A. Development and evolution of the pallium. Seminars in Cell and Developmental Biology 2009, 20:698-711.
142. Menzel R., Giurfa M. Cognitive architecture of a mini-brain: the honeybee. Trends in Cognitive Sciences 2001, 5:62-71.
143. Menzel R., Leboulle G., Eisenhardt D. Small brains, bright minds. Cell 2006, 124:237-239.
144. Menzel R. Searching for the memory trace in a mini-brain, the honeybee. Learning and Memory 2001, 8:53-62.
145. Mertens I., Meeusen T., Huybrechts R., De Loof A., Schoofs L. Characterization of the short neuropeptide F receptor from Drosophila melanogaster. Biochemical and Biophysical Research Communications 2002, 297:1140-1148.
146. Meyering-Vos M. Expression of allatostatins in the mediterranean field cricket, Gryllus bimaculatus de Geer (Ensifera, Gryllidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2003, 136:207-215.
147. Miao Y., Waters E.M., Witten J.L. Developmental and regional-specific expression of FLRFamide peptides in the tobacco hornworm, Manduca sexta, suggests functions at ecdysis. Journal of Neurobiology 1998, 37:469-485.
148. Mizunami M., Weibrecht J.M., Strausfeld N.J. A new role for the insect mushroom bodies: place memory and motor control. Biological Neural Networks in Invertebrate Neuroethology and Robotics 1993, 199-225. Academic Press, Cambridge, MA. R.D. Beer, R. Ritzmann, T. McKenna (Eds.).
149. Mizunami M., Okada R., Li Y., Strausfeld N.J. Mushroom bodies of the cockroach: activity and identities of neurons recorded in freely moving animals. Journal of Comparative Neurology 1998, 402:501-519.
150. Mizunami M., Weibrecht J.M., Strausfeld N.J. Mushroom bodies of the cockroach: their participation in place memory. Journal of Comparative Neurology 1998, 402:520-537.
151. Muren J.E., Lundquist C.T., Nässel D.R. Abundant distribution of locustatachykinin-like peptide in the nervous system and intestine of the cockroach Leucophaea maderae. Philosophical Transactions of the Royal Society B 1995, 348:423-444.
152. Nambu J.R., Murphy-Erdosh C., Andrews P.C., Feistner G.J., Scheller R.H. Isolation and characterization of a Drosophila neuropeptide gene. Neuron 1988, 1:55-61.
153. Nässel D.R., Homberg U. Neuropeptides in interneurons of the insect brain. Cell and Tissue Research 2006, 326:1-24.
154. Nässel D.R., Winther A.M.E. Drosophila neuropeptides in regulation of physiology and behavior. Progress in Neurobiology 2010, 92:42-104.
155. Nässel D.R., Enell L.E., Santos J.G., Wegener C., Johard H.A.D. A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions. BMC Neuroscience 2008, 9:90.
156. Nässel D.R. Insect myotropic peptides: differential distribution of locustatachykinin- and leucokinin-like immunoreactive neurons in the locust brain. Cell and Tissue Research 1993, 274:27-40.
157. Nässel D.R. Tachykinin-related peptides in invertebrates: a review. Peptides 1999, 20:141-158.
158. Nässel D.R. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progress in Neurobiology 2002, 68:1-84.
159. Neder R. Allometrisches Wachstum von Hirnteilen bei drei verschieden grossen Schabenarten. Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 1959, 77:411-464.
160. Nishino H., Iwasaki M., Yasuyama K., Hongo H., Watanabe H., Mizunami M. Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach. Arthropod Structure and Development 2012, 41:3-16.
161. Nusbaum M.P., Blitz D.M., Swensen A.M., Wood D., Marder E. The roles of co-transmission in neural network modulation. Trends in Neurosciences 2001, 24:146-154.
162. Oeh U., Lorenz M.W., Dyker H., Lösel P., Hoffmann K.H. Interaction between Manduca sexta allatotropin and manduca sexta allatostatin in the fall armyworm Spodoptera frugiperda. Insect Biochemistry and Molecular Biology 2000, 30:719-727.
163. Oeh U. Myotropic effect of helicokinins, tachykinin-related peptides and Manduca sexta allatotropin on the gut of Heliothis virescens (Lepidoptera: Noctuidae). Journal of Insect Physiology 2003, 49:323-337.
164. Okada R., Ikeda J. Sensory responses and movement-related activities in extrinsic neurons of the cockroach mushroom bodies. Journal of Comparative Physiology A 1999, 185:115-129.
165. Olsen S.R., Bhandawat V., Wilson R.I. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 2007, 54:89-103.
166. Ons S., Sterkel M., Diambra L., Urlaub H., Rivera-Pomar R. Neuropeptide precursor gene discovery in the Chagas disease vector Rhodnius prolixus. Insect Molecular Biology 2010, 20:29-44.
167. Orchard I., Lange A.B., Bendena W.G. FMRFamide-related peptides: a multifunctional family of structurally related neuropeptides in insects. Advances in Insect Physiology 2001, 28:267-329.
168. Ott S.R., Rogers S.M. Gregarious desert locusts have substantially larger brains with altered proportions compared with the solitarious phase. Proceedings of the Royal Society B 2010, 277:3087-3096.
169. Otto D. Untersuchungen zur zentralnervösen Kontrolle der Lauterzeugung von Grillen. Zeitschrift für Vergleichende Physiologie 1971, 74:227-271.
170. Paemen L., Tips A., Schoofs L., Proost P., Van Damme J., De Loof A. Lom-AG-myotropin: a novel myotropic peptide from the male accessory glands of Locusta migratoria. Peptides 1991, 12:7-10.
171. Paemen L., Schoofs L., Loof A. Localization of Lom-AG-myotropin I-like substances in the male reproductive and nervous tissue of the locust, Locusta migratoria. Cell and Tissue Research 1992, 268:91-97.
172. Park C., Hwang J.S., Kang S.W., Lee B.H. Molecular characterization of a cDNA from the silk moth Bombyx mori encoding Manduca sexta allatotropin peptide. Zoological Science 2002, 19:287-292.
173. Pascual N., Castresana J., Valero M.-L., Andreu D., Bellés X. Orcokinins in insects and other invertebrates. Insect Biochemistry and Molecular Biology 2004, 34:1141-1146.
174. Paulk A.C., Gronenberg W. Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Structure and Development 2008, 37:443-458.
175. Peng Y., Xi W., Zhang W., Zhang K., Guo A. Experience improves feature extraction in Drosophila. The Journal of Neuroscience 2007, 27:5139-5145.
176. Perez-Orive J., Mazor O., Turner G.C., Cassenaer S., Wilson R.I., Laurent G. Oscillations and sparsening of odor representations in the mushroom body. Science 2002, 297:359-365.
177. Petri B., Homberg U., Loesel R., Stengl M. Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. Journal of Experimental Biology 2002, 205:1459-1469.
178. Pitman J.L., McGill J.J., Keegan K.P., Allada R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 2006, 441:753-756.
179. Pratt G.E., Farnsworth D.E., Siegel N.R., Fok K.F., Feyereisen R. Identification of an allatostatin from adult Diploptera punctata. Biochemical and Biophysical Research Communications 1989, 163:1243-1247.
180. Predel R., Neupert S. Social behavior and the evolution of neuropeptide genes: lessons from the honeybee genome. BioEssays 2007, 29:416-421.
181. Predel R., Rapus J., Eckert M. Myoinhibitory neuropeptides in the american cockroach. Peptides 2001, 22:199-208.
182. Predel R., Neupert S., Wicher D., Gundel M., Roth S., Derst C. Unique accumulation of neuropeptides in an insect: FMRFamide-related peptides in the cockroach, Periplaneta americana. European Journal of Neuroscience 2004, 20:1499-1513.
183. Predel R., Neupert S., Roth S., Derst C., Nässel D.R. Tachykinin-related peptide precursors in two cockroach species. FEBS Journal 2005, 272:3365-3375.
184. Predel R., Russell W.K., Russell D.H., Lopez J., Esquivel J., Nachman R.J. Comparative peptidomics of four related hemipteran species: pyrokinins, myosuppressin, corazonin, adipokinetic hormone, sNPF, and periviscerokinins. Peptides 2008, 29:162-167.
185. Predel R., Neupert S., Garczynski S.F., Crim J.W., Brown M.R., Russell W.K., Russell D.H., Nachman R.J. Neuropeptidomics of the mosquito Aedes aegypti. Journal of Proteome Research 2010, 1:2006-2015.
186. Price D., Greenberg M. Structure of a molluscan cardioexcitatory neuropeptide. Science 1977, 197:671.
187. Riehle M.A., Garczynski S.F., Crim J.W., Hill C.a., Brown M.R. Neuropeptides and peptide hormones in Anopheles gambiae. Science 2002, 298:172-175.
188. Roller L., Yamanaka N., Watanabe K., Daubnerová I., Žitňan D., Kataoka H., Tanaka Y. The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochemistry and Molecular Biology 2008, 38:1147-1157.
189. Rudwall A.J., Sliwowska J., Nässel D.R. Allatotropin-like neuropeptide in the cockroach abdominal nervous system: myotropic actions, sexually dimorphic distribution and colocalization with serotonin. Journal of Comparative Neurology 2000, 428:159-173.
190. Schachtner J., Schmidt M., Homberg U. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Structure and Development 2005, 34:257-299.
191. Schildberger K. Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. Journal of Comparative Physiology A 1984, 154:71-79.
192. Schneider L.E., Taghert P.H. Isolation and characterization of a Drosophila gene that encodes multiple neuropeptides related to Phe-Met-Arg-Phe-NH2 (FMRFamide). Proceedings of the National Academy of Sciences of the United States of America 1988, 85:1993-1997.
193. Schoofs L., Clynen E., Cerstiaens a, Baggerman G., Wei Z., Vercammen T., Nachman R., De Loof A., Tanaka S. Newly discovered functions for some myotropic neuropeptides in locusts. Peptides 2001, 22:219-227.
194. Schoofs L., Holman G.M., Hayes T.K., Nachman R.J., De Loof A. Locustatachykinins I and II, two novel insect neuropeptides with homology to peptides of the vertebrate tachykinin family. FEBS Letters 1990, 261:340-397.
195. Schoofs L., Holman G.M., Hayes T.K., Nachman R.J., Kochansky J.P., De Loof A. Locustatachykinins III and IV: two additional insect neuropeptides with homology to peptides of the vertebrate tachykinin family. Regulatory Peptides 1990, 31:199-212.
196. Schoofs L., Holman G.M., Hayes T.K., Nachman R.J., De Loof A. Isolation, identification and synthesis of locustamyoinhibiting peptide (LOM-MIP), a novel biologically active neuropeptide from Locusta migratoria. Regulatory Peptides 1991, 36:111-119.
197. Schoofs L., Veelaert D., Vanden Broeck J., De Loof A. Immunocytochemical distribution of locustamyoinhibiting peptide (Lom-MIP) in the nervous system of Locusta migratoria. Regulatory Peptides 1996, 63:171-179.
198. Schroll C., Riemensperger T., Bucher D., Ehmer J., Völler T., Erbguth K., Gerber B., Hendel T., Nagel G., Buchner E., Fiala A. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Current Biology: CB 2006, 16:1741-1747.
199. Schröter U., Menzel R. A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. Journal of Comparative Neurology 2003, 465:168-178.
200. Schürmann F.W., Erber J. FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifera). A light- and electron microscopical study. Neuroscience 1990, 38:797-807.
201. Schwaerzel M., Monastirioti M., Scholz H., Friggi-Grelin F., Birman S., Heisenberg M. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. The Journal of Neuroscience 2003, 23:10495-10502.
202. Secher T., Lenz C., Cazzamali G., Sørensen G., Williamson M., Hansen G.N., Svane P., Grimmelikhuijzen C.J. Molecular cloning of a functional allatostatin gut/brain receptor and an allatostatin preprohormone from the silkworm Bombyx mori. Journal of Biological Chemistry 2001, 276:47052-47060.
203. Settembrini B.P., Villar M.J. FMRFamide-like immunocytochemistry in the brain and subesophageal ganglion of Triatoma infestans (Insecta: Heteroptera). Coexpression with beta-pigment-dispersing hormone and small cardioactive peptide B. Cell and Tissue Research 2005, 321:299-310.
204. Severini C., Improta G., Falconieri-Erspamer G., Salvadori S., Erspamer V. The tachykinin peptide family. Pharmacological Reviews 2002, 54:285-322.
205. Simões P., Ott S.R., Niven J.E. Associative olfactory learning in the desert locust, Schistocerca gregaria. The Journal of Experimental Biology 2011, 214:2495-2503.
206. Sinakevitch I., Farris S.M., Strausfeld N.J. Taurine-, aspartate-, and glutamate-like immunoreactivity identifies chemically distinct subdivisions of kenyon cells in the cockroach mushroom body. Journal of Comparative Neurology 2001, 439:352-367.
207. Sinakevitch I., Sjöholm M., Hansson B.S., Strausfeld N.J. Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis. Arthropod Structure and Development 2008, 37:260-272.
208. Sinakevitch I., Grau Y., Strausfeld N.J., Birman S. Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila. Neural Development 2010, 5:10.
209. Siviter R.J., Coast G.M., Winther A.M., Nachman R.J., Taylor C.a., Shirras A.D., Coates D., Isaac R.E., Nässel D.R. Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. Journal of Biological Chemistry 2000, 275:23273-23280.
210. Sjöholm M., Sinakevitch I., Ignell R., Strausfeld N.J., Hansson B.S. Organization of Kenyon cells in subdivisions of the mushroom bodies of a lepidopteran insect. The Journal of Comparative Neurology 2005, 491:290-304.
211. Sjöholm M., Sinakevitch I., Strausfeld N.J., Ignell R., Hansson B.S. Functional division of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis revealed by antibodies against aspartate, taurine, FMRF-amide, Mas-allatotropin and DC0. Arthropod Structure and Development 2006, 35:153-168.
212. Skiebe P., Dreger M., Meseke M., Evers J.F., Hucho F. Identification of orcokinins in single neurons in the stomatogastric nervous system of the crayfish, Cherax destructor. Journal of Comparative Neurology 2002, 444:245-259.
213. Sokoloff A. The Genetics of Tribolium and Related Species. Advances in Genetics, Suppl. 1 1966, Academic Press, New York.
214. Spittaels K., Vankeerberghen A., Schoofs L., Proost P., Van Damme J., De Loof A. Isolation and characterization of Locusta migratoria accessory gland myotropin I (Lom-Ag-MT-I) from the brain of the colorado potato beetle, Leptinotarsa decemlineata. Archives of Insect Biochemistry and Physiology 1996, 31:149-155.
215. Spittaels K., Verhaert P., Shaw C., Johnston R.N., Devreese B., Van Beeumen J., De Loof A. Insect neuropeptide F (NPF)-related peptides: isolation from colorado potato beetle (Leptinotarsa decemlineata) brain. Insect Biochemistry and Molecular Biology 1996, 26:375-382.
216. Stangier J., Hilbich C., Burdzik S., Keller R. Orcokinin: a novel myotropic peptide from the nervous system of the crayfish, Orconectes limosus. Peptides 1992, 13:859-864.
217. Stay B., Tobe S.S. The role of allatostatins in juvenile hormone synthesis in insects and crustaceans. Annual Review of Entomology 2007, 52:277-299.
218. Strausfeld N.J., Li Y. Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies. Journal of Comparative Neurology 1999, 409:626-646.
219. Strausfeld N.J., Buschbeck E.K., Gomez R.S. The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach 1995, 349-381. Birkhäuser, Basel. O. Breidbach, W. Kutsch (Eds.).
220. Strausfeld N.J., Homberg U., Kloppenberg P. Parallel organization in honey bee mushroom bodies by peptidergic kenyon cells. Journal of Comparative Neurology 2000, 424:179-195.
221. Strausfeld N.J., Strausfeld C.M., Stowe S., Rowell D., Loesel R. The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli. Arthropod Structure and Development 2006, 35(3):169-196.
222. Strausfeld N.J., Sinakevitch I., Brown S.M., Farris S.M. Ground plan of the insect mushroom body: functional and evolutionary implications. Journal of Comparative Neurology 2009, 513:265-291.
223. Strausfeld N.J. Crustacean - insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain, Behavior and Evolution 1998, 52:186-206.
224. Strausfeld N.J. Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. Journal of Comparative Neurology 2002, 450:4-33.
225. Svidersky V.L., Plotnikova S.I. On structural-functional organization of dragonfly mushroom bodies and some general considerations about purpose of these formations. Journal of Evolutionary Biochemistry and Physiology 2004, 40:608-624.
226. Taghert H., Schneider L.E. Interspecific comparison of a Drosophila gene encoding FMRFamide-related neuropeptides. Journal of Neuroscience 1990, 10:1929-1942.
227. Takeuchi H., Yasuda A., Yasuda-Kamatani Y., Sawata M., Matsuo Y., Kato A., Tsujimoto A., Nakajima T., Kubo T. Prepro-tachykinin gene expression in the brain of the honeybee Apis mellifera. Cell and Tissue Research 2004, 316:281-293.
228. Tanaka N.K., Tanimoto H., Ito K. Neuronal assemblies of the Drosophila. Journal of Comparative Neurology 2008, 508:711-755.
229. Tang S., Guo A. Choice behavior of Drosophila facing contradictory visual cues. Science 2001, 294:1543-1547.
230. Tomer R., Denes A.S., Tessmar-Raible K., Arendt D. Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 2010, 142:800-809.
231. Truesdell P.F., Koladich P.M., Kataoka H., Kojima K., Suzuki A., McNeil J., Mizoguchi A., Tobe S.S., Bendena W.G. Molecular characterization of a cDNA from the true armyworm Pseudaletia unipuncta encoding Manduca sexta allatotropin peptide. Insect Biochemistry and Molecular Biology 2000, 30:691-702.
232. Turner R.S. Observations on the central nervous system of Leptoplana acticola. Journal of Comparative Neurology 1946, 85:53-65.
233. Unoki S., Matsumoto Y., Mizunami M. Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. European Journal of Neuroscience 2005, 22:1409-1416.
234. Utz S., Schachtner J. Development of A-type allatostatin immunoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta. Cell and Tissue Research 2005, 320:149-162.
235. Utz S., Huetteroth W., Wegener C., Predel R., Schachtner J. Direct peptide profiling of lateral cell groups of the antennal lobes of Manduca sexta reveals specific composition and changes in neuropeptide expression during development. Developmental Neurobiology 2007, 67:764-777.
236. Van Loy T., Vandersmissen H.P., Poels J., Van Hiel M.B., Verlinden H., Vanden Broeck J. Tachykinin-related peptides and their receptors in invertebrates: a current view. Peptides 2010, 31:520-524.
237. Vanden Broeck J. Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 2001, 22:241-254.
238. Veelaert D., Schoofs L., Tobe S.S., Yu C.G., Vullings H.G.B., Couillaud F., Loof A.D. Immunological evidence for an allatostatin-like neuropeptide in the central nervous system of Schistocerca gregaria, Locusta migratoria and Neobellieria bullata. Cell and Tissue Research 1995, 279:601-611.
239. Veenstra J.A., Costes L. Isolation and identification of a peptide and its cDNA from the mosquito Aedes aegypti related to Manduca sexta allatotropin. Peptides 1999, 20:1145-1151.
240. Veenstra J.A., Hagedorn H.H. Sensitive enzyme immunoassay for Manduca allatotropin and the existence of an allatotropin-immunoreactive peptide in Periplaneta americana. Archives of Insect Biochemistry and Physiology 1993, 23:99-109.
241. Veenstra J.A., Lambrou G. Isolation of a novel RFamide peptide from the midgut of the American cockroach, Periplaneta americana. Biochemical and Biophysical Research Communications 1995, 213:519-524.
242. Veenstra J.A., Lehman H.K., Davis N.T. Short communication: Allatotropin is a cardioaccelatory peptide in Manduca sexta. Journal of Experimental Biology 1994, 188:347-354.
243. Veenstra J.A., Noriega F.G., Graf R., Feyereisen R. Identification of three allatostatins and their cDNA from the mosquito Aedes aegypti. Peptides 1997, 18:937-942.
244. Verleyen P., Huybrechts J., Baggerman G., Lommel A., van, De Loof A., Schoofs L. SIFamide is a highly conserved neuropeptide: a comparative study in different insects. Biochemical and Biophysical Research Communications 2004, 320:334-341.
245. Verleyen P., Huybrechts J., Schoofs L. SIFamide illustrates the rapid evolution in arthropod neuropeptide research. General and Comparative Endocrinology 2009, 162:27-35.
246. Vitzthum H., Homberg U., Agricola H. Distribution of Dip-Allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. Journal of Comparative Neurology 1996, 369:419-437.
247. Waddell S., Armstrong J.D., Kitamoto T., Kaiser K., Quinn W.G. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 2000, 103:805-813.
248. Wadepuhl M. Control of grasshopper singing behavior by the brain responses to electrical stimulation. Zeitschrift für Tierpsychologie 1983, 63:173-200.
249. Walker R.J., Papaioannou S., Holden-Dye L. A review of FMRFamide- and RFamide-like peptides in metazoa. Invertebrate Neuroscience: IN 2009, 9:111-153.
250. Wasielewski O., Skonieczna M., Kodrík D. Role of allatostatin-like factors from the brain of Tenebrio molitor females. Archives of Insect Biochemistry and Physiology 2009, 71:223-235.
251. Weiss M.J. Structural patterns in the corpora pedunculata of orthoptera: a reduced silver analysis. Journal of Comparative Neurology 1981, 203:515-553.
252. Wessnitzer J., Webb B. Multimodal sensory integration in insects - towards insect brain control architectures. Bioinspiration and Biomimetics 2006, 1:63-75.
253. Williamson M., Lenz C., Winther A.M., Nässel D.R., Grimmelikhuijzen C.J., Winther M.E. Molecular cloning, genomic organization, and expression of a B-type (cricket-type) allatostatin preprohormone from Drosophila melanogaster. Biochemical and Biophysical Research Communications 2001, 281:544-550.
254. Winther A.M.E., Acebes A., Ferrús A. Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Molecular and Cellular Neurosciences 2006, 31:399-406.
255. Withers G.S., Fahrbach S.E., Robinson G.E. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 1993, 364:238-240.
256. Woodhead A.P., Stay B., Seidel S.L., Khan M.A., Tobe S.S. Primary structure of four allatostatins: neuropeptide inhibitors of juvenile hormone synthesis. Proceedings of the National Academy of Sciences of the United States of America 1989, 86:5997-6001.
257. Xi W., Peng Y., Guo J., Ye Y., Zhang K., Yu F., Guo A. Mushroom bodies modulate salience-based selective fixation behavior in Drosophila. European Journal of Neuroscience 2008, 27:1441-1451.
258. Yagi K.J., Kwok R., Chan K.K., Setter R.R., Myles T.G., Tobe S.S., Stay B. Phe-Gly-Leu-amide allatostatin in the termite Reticulitermes flavipes: content in brain and corpus allatum and effect on juvenile hormone synthesis. Journal of Insect Physiology 2005, 51:357-365.
259. Yasuda A., Yasuda-Kamatani Y., Nozaki M., Nakajima T. Identification of GYRKPPFNGSIFamide (crustacean-SIFamide) in the crayfish Procambarus clarkii by topological mass spectrometry analysis. General and Comparative Endocrinology 2004, 135:391-400.
260. Yasuda-Kamatani Y., Yasuda A. Identification of orcokinin gene-related peptides in the brain of the crayfish Procambarus clarkii by the combination of MALDI-TOF and on-line capillary HPLC/Q-Tof mass spectrometries and molecular cloning. General and Comparative Endocrinology 2000, 118:161-172.
261. Yew J.Y., Wang Y., Barteneva N., Dikler S., Kutz-Naber K.K., Li L., Kravitz E.A. Analysis of neuropeptide expression and localization in adult Drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry. Journal of Proteome Research 2009, 8:1271-1284.
262. Zhang K., Guo J.Z., Peng Y., Xi W., Guo A. Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila. Science 2007, 316:1901-1904.
263. Zhao X., Coptis V., Farris S.M. Metamorphosis and adult development of the mushroom bodies of the red flour beetle, Tribolium castaneum. Developmental Neurobiology 2008, 68:1487-1502.