Developmental changes in expression patterns of two dopamine receptor genes in mushroom bodies of the honeybee, Apis mellifera

Journal of Comparative Neurology

Volumn 466, Issue 1, 2003, Pages 91-103

  Kurshan, Peri T ^a   Hamilton, Ingrid S ^a   Mustard, Julie A ^a   Mercer, Alison R ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Biogenic amine; Invertebrate; Metamorphosis; Neuromodulation

Indexed keywords

DOPAMINE RECEPTOR; GENE PRODUCT; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; GENE; GENE AMDOP1; GENE AMDOP2; GENE EXPRESSION REGULATION; GLIA CELL; HONEYBEE; METAMORPHOSIS; MUSHROOM; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; BEES; BRAIN; CELL DIFFERENTIATION; DOPAMINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; METAMORPHOSIS, BIOLOGICAL; MUSHROOM BODIES; NEUROGLIA; NEURONS; PUPA; RECEPTORS, DOPAMINE; RNA, MESSENGER;

EID: 0141481905     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10864     Document Type: Article

References (134)

1. Abel R, Rybak J, Menzel R. 2001. Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437:363-383.
2. Bertholf LM. 1925. The moults of the honeybee. J Econ Entomol 18:380-384.
3. Bicker G. 1999. Biogenic amines in the brain of the honeybee: cellular distribution, development, and behavioral functions. Microsc Res Techniq 44:166-178.
4. Blenau W, Erber J, Baumann A. 1998. Characterization of a dopamine D1 receptor from Apis mellifera: cloning, functional expression, pharmacology, and mRNA localization in the brain. J Neurochem 70:15-23.
5. Blenau W, Schmidt M, Faensen D, Schürmann F-W. 1999. Neurons with dopamine-like immunoreactivity target mushroom body Kenyon cell somata in the brain of some hymenopteran insects. Int J Insect Morphol Embryol 28:203-210.
6. Braissant O, Wahli W. 1998. A simplified in situ hybridisation protocol using nonradioactively labelled probes to detect abundant and rare mRNAs on tissue sections. Biochemica 1:10-16.
7. Budnik V, White K. 1988. Catecholamine-containing neurons in Drosophila melanogaster: distribution and development. J Comp Neurol 268: 400-413.
8. 3H-gammaaminobutyric acid uptake in the lamina ganglionaris of Musca and Drosophila. Z Zellforsch Mikrosk Anat 147:415-431.
9. Carlson SD, Saint Marie RL. 1990. Structure and function of insect glia. Annu Rev Entomol 35:597-621.
10. Cayre M, Buckingham SD, Yagodin S, Sattelle DB. 1999. Cultured insect mushroom body neurons express functional receptors for acetylcholine, GABA, glutamate, octopamine, and dopamine. J Neurophysiol 81:1-14.
11. Crittenden JR, Skoulakis EMC, Han K-A, Kalderon D, Davis RL. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Lean Mem 5:38-51.
12. Davis RL. 1993. Mushroom bodies and Drosophila learning. Neuron 11:1-14.
13. Davis RL, Cherry J, Dauwalder B, Han PL, Skoulakis E. 1995. The cyclic AMP system and Drosophila learning. Mol Cell Biochem 149:271-278.
14. De Belle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
15. Dubnau J, Tully T. 1998. Gene discovery in Drosophila: new insights for learning and memory. Annu Rev Neurosci 21:407-444.
16. Dubnau J, Grady L, Kitamoto T, Tully T. 2001. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411:476-480.
17. Dujardin F. 1853. Quelques observations sur les abeilles et particulièrement sur les actes qui, chez ces insectes peuvent être rapports à l'intelligence. Ann Sci Nat Zool 18:231-240.
18. Ebert PR, Rowland JE, Toma DP. 1998. Isolation of seven unique biogenie amine receptor clones from the honeybee by library scanning. Insect Mol Biol 7:151-162.
19. Ehmer B, Gronenberg W. 2002. Segregation of visual input to the mushroom bodies of the honeybee (Apis mellifera). J Comp Neurol 451:362-373.
20. Eichmüllar S. 1994. Vom Sansillum zum Pilzkörper: Immunohistologische und ontogenetische Aspekte zur Anatomie des Olfaktorischen Systems der Honigbiene. PhD dissertation, Free University Berlin.
21. Eisenhardt D, Fiala A, Braun P, Rosenboom H, Kress H, Ebert PR, Menzel R. 2001. Cloning of a catalytic subunit of cAMP-dependent protein kinase from the honeybee (Apis mellifera) and its localization in the brain. Insect Mol Biol 10:173-181.
22. Erber J. 1978. Response characteristics and after effects of multimodal neurons in the mushroom body area of the honeybee. Physiol Entomol 3:77-89.
23. Erber J. 1981. Neural correlates of learning in the honeybee. Trends Neurosci 4:270-273.
24. Erber J, Masuhr T, Menzel R. 1980. Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol Entomol 5:343-358.
25. Ewer J, Frisch B, Rosbash M, Hall JC. 1992. Expression of the period clock gene within different cell types in the brain of Drosophila adults and mosaic analysis of these cells' influence on circadian behavioural rhythms. J Neurosci 12:3321-3349.
26. Fahrbach SE, Robinson GE. 1996. Juvenile hormone, behavioural maturation, and brain structure in the honeybee. Dev Neurosci 18:102-114.
27. Farris SM, Strausfeld NJ. 2001. Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth and maturation. J Comp Neurol 439:331-351.
28. Farris SM, Robinson GE, Davis RL, Fahrbach SE. 1999. Larval and pupal development of the mushroom bodies in the honeybee, Apis mellifera. J Comp Neurol 414:97-113.
29. Farris SM, Robinson GE, Fahrbach SE. 2001. Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21:6395-6404.
30. Feng G, Hannan F, Reale V, Hon YY, Kousky CT, Evans PD, Hall LM. 1996. Cloning and functional characterization of a novel dopamine receptor from Drosophila melanogaster. J Neurosci 16:3925-3933.
31. Fiala A, Muller U, Menzel R. 1999. Reversible downregulation of protein kinase A during olfactory learning using antisense technique impairs long-term memory formation in the honeybee, Apis mellifera. J Neurosci 19:10125-10134.
32. Frisch B, Hardin PE, Hamblen-Coyle MJ, Rosbash MR, Hall JC. 1994. A promoterless period gene mediates behavioural rhythmicity and cyclical per expression in a restricted subset of the Drosophila nervous system. Neuron 12:555-570.
33. Fuchs E, Dustmann JH, Stadler H, Schürmann FW. 1989. Neuroactive compounds in the brain of the honeybee during imaginal life. Comp Biochem Physiol 92C:337-342.
34. Ganeshina O, Schäfer S, Malun D. 2000. Proliferation and programmed cell death of neuronal precursors in the mushroom bodies of the honeybee. J Comp Neurol 417:349-365.
35. Geng C, Sparks TC, Skomp JR, Gajewski RP. 1993. Biogenic amines in the brain of Manduca sexta during larval-pupal metamorphosis. Comp Biochem Physiol 106C:275-284.
36. 1/5 receptors. Recept Chan 2:131-141.
37. Gregory GE. 1980. The Bodian protargol technique. In: Strausfeld NJ, Miller TA, editors. Neuroanatomical techniques: insect nervous system. New York: Springer-Verlag. p 75-95.
38. Gronenberg W. 2001. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol. 435: 474-489.
39. Hähnlein I, Bicker G. 1996. Morphology of neuroglia in the antennal lobes and mushroom bodies of the brain of the honeybee. J Comp Neurol 367:235-245.
40. Hähnlein I, Bicker G. 1997. Glial patterning during postembryonic development of the central neuropiles in the brain of the honeybee. Dev Genes Evol 207:29-41.
41. Hall JC. 1995. Tripping along the trail to the molecular mechanisms of biological clocks. TINS 18:230-240.
42. Hall JC. 1996. Are cycling gene products as internal Zeitgebers no longer the Zeitgeist of chronobiology? Neuron 17:799-802.
43. Han K-A, Millar NS, Grotewiel MS, Davis RL. 1996. DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16:1127-1135.
44. Han P-L, Levin LR, Reed RR, Davis RL. 1992. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9:619-627.
45. Hannan F, Hall LM. 1996. Temporal and spatial expression patterns of two G-protein coupled receptors in Drosophila melanogaster. Invertebr Neurosci 2:71-83.
46. Hardin P, Siwicki KK. 1995. The multiple roles of per in the Drosophila circadian clock. Semin Neurosci 7:15-25.
47. Harris JW, Woodring J. 1992. Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honeybee (Apis mellifera L.) brain. J Insect Physiol 38:29-35.
48. Hearn MG, Ren Y, McBride EW, Reveillaud I, Beinborn M, Kopin AS. 2002. A Drosophila dopamine 2-like receptor: molecular characterization and identification of multiple alternatively spliced variants. Proc Natl Acad Sci USA 99:14554-14559.
49. Heisenberg M. 1980. Mutants of brain structure and function: what is the significance of the mushroom bodies for behavior? Basic Life Sci 16: 373-390.
50. Heisenberg M. 1998. What do the mushroom bodies do for the insect brain? Learn Mem 5:1-10.
51. Heisenberg M, Borst A, Wagner S, Byers D. 1985. Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1-30.
52. Helfrich-Förster C. 1997. Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 380:335-354.
53. Helfrich-Förster C, Homberg U. 1993. Pigment-dispersing hormone-immunoreactive neurons in the nervous system of wild-type Drosophila melanogaster and of several mutants with altered circadian rhythmicity. J Comp Neurol 337:177-190.
54. Hirasawa A, Horie K, Tanaka T, Takagaki K, Murai M, Yano J, Tsujimoto G. 1993. Cloning, functional expression and tissue distribution of human cDNA for the alpha 1C-adrenergic receptor. Biochem Biophys Res Commun 195:912-909.
55. Humphries MA, Mustard JA, Hunter SJ, Mercer AR, Ward V, Ebert PR. 2003. An invertebrate D2 type dopamine receptor exhibits age-based plasticity of expression in mushroom bodies of the honeybee brain. J Neurobiol 55:315-330.
56. Jay SC. 1962. Colour changes in honeybee pupae. Bee World 43:119-122.
57. Kamikouchi A, Takeuchi H, Sawata M, Ohashi K, Natori S, Kubo T. 1998. Preferential expression of the gene for a putative inositol 1,4,5-triphosphate receptor homologue in the mushroom bodies of the brain of the worker honeybee Apis mellifera L. Biochem Biophys Res Commun 242:181-186.
58. 2+/calmodulin-dependent protein kinase II and protein kinase C in the mushroom bodies of the brain of the honeybee Apis mellifera L. J Comp Neurol 417:501-510.
59. Kenyon FC. 1896. The brain of the bee. A preliminary contribution to the morphology of the nervous system of the Arthropoda. J Comp Neurol 6:133-210.
60. Kirchhof BS, Homberg U, Mercer AR. 1999. Development of dopamine-immunoreactive neurons associated with the antennal lobes of the honeybee, Apis mellifera. J Comp Neurol 411:643-653.
61. Klein DC, Moore RY, Reppert SM, editors. 1991. Suprachiasmatic nucleus: the mind's clock. New York: Oxford University Press.
62. Kokay IC, Mercer AR. 1997. Age-related changes in dopamine receptor densities in the brain of the honeybee, Apis mellifera. J Comp Physiol A181:415-423.
63. 3H]spiperone binding sites in honeybee brain. J Comp Neurol 394:29-37.
64. Kokay IC, Ebert PR, Kirchhof BS, Mercer AR. 1999. Distribution of dopamine receptors and dopamine receptor homologs in the brain of the honeybee, Apis mellifera L. Microsc Res Techniq 44:179-189.
65. Kretzschmar D, Pflugfelder GO. 2002. Glia in development, function, and neurodegeneration of the adult insect brain. Brain Res Bull 57:121-131.
66. Krueger RR, Kramer KJ, Hopkins TL, Speirs RD. 1990. N-β -alanyldopamine and N-acetyldopamine occurrence and synthesis in the central nervous system of Manduca sexta (L.). Insect Biochem 20:605-610.
67. Kucharski R, Ball EE, Hayward DC, Maleszka R. 2000. Molecular cloning and expression analysis of a cDNA encoding a glutamate transporter in the honeybee brain. Gene 242:399-405.
68. Lankford KL, DeMello FG, Klein WL. 1987. A transient embryonic dopamine receptor inhibits growth cone motility and neurite outgrowth in a subset of avian retina neurons. Neurosci Lett 75:169-174.
69. Lankford KL, DeMello FG, Klein WL. 1988. D1-type dopamine receptors inhibit growth cone motility in cultured retina neurons: evidence that neurotransmitters act as morphogenic growth regulators in the developing central nervous system. Proc Natl Acad Sci U S A 85:2839-2843.
70. Lauder JM. 1993. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci 16:233-240.
71. Li Y-S, Strausfeld NJ. 1997. Morphology and sensory modality of mushroom body efferent neurons in the brain of the cockroach, Periplaneta americana. J Comp Neurol 387:631-650.
72. Li Y-S, Strausfeld NJ. 1999. Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. J Comp Neurol 409: 647-663.
73. Lipton SA, Kater SB. 1989. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 12:265-270.
74. Lundell MJ, Hirsh J. 1994. Temporal and spatial development of serotonin and dopamine neurons in the Drosophila CNS. Dev Biol 165:385-396.
75. Macmillan CS, Mercer AR. 1987. An investigation of the role of dopamine in the antennal lobes of the honeybee, Apis mellifera. J Comp Physiol A160:359-366.
76. Malun D. 1998. Early development of mushroom bodies in the brain of the honeybee Apis mellifera as revealed by BrdU incorporation and ablation experiments. Learn Mem 5:90-101.
77. Mauelshagen J. 1993. Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J Neurophysiol 69:609-625.
78. McCobb DP, Haydon PG, Kater SB. 1988. Dopamine and serotonin inhibition of neurite elongation of different identified neurons. J Neurosci Res 19:19-26.
79. McGuire SE, Le PT, Davis RL. 2001. The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333.
80. Menzel R. 1999. Memory dynamics in the honeybee. J Comp Physiol 185:323-340.
81. Menzel R. 2001. Searching for the memory trace in a mini-brain, the honeybee. Learn Mem 8:53-62.
82. Menzel R, Müller U. 1996. Learning and memory in honeybees: from behaviour to neural substrates. Annu Rev Neurosci 19:379-404.
83. Mercer AR, Erber J. 1983. The effects of amines on evoked potentials recorded in the mushroom bodies of the bee brain. J Comp Physiol 151:469-476.
84. Mercer AR, Menzel R. 1982. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol A145:363-368.
85. Mercer AR, Mobbs PG, Davenport AP, Evans PD. 1983. Biogenic amines in the brain of the honeybee, Apis mellifera. Cell Tissue Res 234:655-677.
86. Michelette ERdF, Soares AEE. 1993. Characterization of preimaginal developmental stages in Africanized honeybee workers (Apis mellifera). Apidologie 24:431-440.
87. Michelsen DB. 1988. Catecholamines affect storage and retrieval of conditioned odour stimuli in honeybees. Comp Biochem Physiol 91C:479-482.
88. Mobbs PG. 1982. The brain of the honeybee Apis mellifera I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B Biol Sci 298:309-354.
89. Müller U. 1997. Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies of Drosophila melanogaster and the honeybee Apis mellifera. J Neurobiol 33:33-44.
90. Müller U. 1999. Second messenger pathways in the honeybee brain: immunohisto-chemistry of protein kinase A and protein kinase C. Microsc Res Techniq 45:165-173.
91. Müller U. 2000. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27:1-20.
92. Mustard JA, Blenau W, Hamilton IS, Ward VK, Ebert PR, Mercer AR. 2003. Analysis of two D1-like dopamine receptors from the honeybee reveals agonist independent activation. Brain Res Mol Brain Res 113: 67-77.
93. Nässel DR, Laxmyr L. 1983. Quantitative determination of biogenic amines and dopa in the CNS of adult and larval blowflies, Calliphora erythrocephala. Comp Biochem Physiol C75:259-265.
94. Neckameyer WS. 1996. Multiple roles for dopamine in Drosophila development. Dev Biol 176:209-219.
95. Nighorn A, Healy M, Davis RL. 1991. The cAMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in mushroom body neuropil. Neuron 6:455-467.
96. Oland LA, Tolbert LP. 2003. Key interactions between neurons and glial cells during neural development in insects. Annu Rev Entomol 48:89-110.
97. Panov AA. 1957. The structure of the brain in insects in successive stages of postembryonic development. Rev Entomol USSR 36:269-284.
98. Pascuel A, Préat T. 2001. Localization of long-term memory within the Drosophila mushroom body. Science 294:1115-1117.
99. 3H]SCH23390-binding sites in the brain of the honeybee, Apis mellifera L. Brain Res 855:206-216.
100. Reale V, Hannan F, Hall LM, Evans PD. 1997. Agonist-specific coupling of a cloned Drosophila melanogaster D1-like dopamine receptor to multiple second messenger pathways by synthetic agonists. J Neurosci 17: 6545-6553.
101. Reinoso BS, Undie AS, Levitt P. 1996. Dopamine receptors mediate differential morphological effects on cerebral cortical neurons in vitro. J Neurosci Res 43:439-453.
102. Roman G, Davis RL. 2001. Molecular biology and anatomy of Drosophila olfactory associative learning. Bioessays 23:571-581.
103. Rybak J, Menzel R. 1993. Anatomy of the mushroom bodies in the honeybee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 334:444-465.
104. Santos Rodrigues P, Dowling JE. 1990. Dopamine induces neurite retraction in retinal horizontal cells via diacylglycerol and protein kinase C. Proc Natl Adac Sci U S A 87:9693-9697.
105. Schäfer S, Rehder V. 1989. Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43-58.
106. Schmidt U, Beyer C, Oestreicher AB, Reisert I, Schilling K, Pilgrim C. 1996. Activation of dopaminergic D1 receptors promotes morphogenesis of developing striatal neurons. Neuroscience 74:453-460.
107. Schmidt U, Pilgrim C, Beyer C. 1998. Differentiative effects of dopamine on striatal neurons involve stimulation of the cAMP/PKA pathway. Mol Cell Neurosci 11:9-18.
108. Schröter U, Malun D. 2000. Formation of antennal lobe and mushroom body neuropils during metamorphosis in the honeybee, Apis mellifera. J Comp Neurol 422:229-245.
109. Schultz DJ, Robinson GE. 1999. Biogenic amines and division of labor in honeybee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A184:481-488.
110. Schürmann FW, Elekes K, Geffard M. 1989. Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res 256:399-410.
111. Siwicki KK, Eastman C, Petersen G, Rosbash M, Hall JC. 1988. Antibodies to the period gene product of Drosophila reveal diverse tissue distribution and rhythmic changes in the visual system. Neuron 1:141-150.
112. Skoulakis EMC, Kalderon D, Davis RL. 1993. Preferential expression of the catalytic subunit of PKA in the mushroom bodies and its role in learning and memory. Neuron 11:197-208.
113. Spencer GE, Lukowiak K, Syed NI. 1996. Dopamine regulation of neurite outgrowth from identified Lymnaea neurons in culture. Cell Mol Neurobiol 16:577-589.
114. Spencer GE, Klumperman J, Syed NI. 1998. Neurotransmitters and neurodevelopment. Role of dopamine in neurite outgrowth, target selection and specific synapse formation. Perspect Dev Neurobiol 5:451-67.
115. Strausfeld NJ. 2001. Insect brain. In: Roth G, Wulliman MF, editors. Brain, evolution and cognition. New York: Wiley. p 367-400.
116. Strausfeld NJ. 2002. Organization of the honeybee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450:4-33.
117. Strausfeld NJ, Homburg U, Kloppenberg P. 2000. Parallel organization in honeybee mushroom bodies by peptidergic Kenyon cells. J Comp Neurol 424:179-195.
118. Sugamori KS, Demchyshyn LL, McConkey F, Forte MA, Niznik HB. 1995. A primordial dopamine D1-like adenylyl cyclase-linked receptor from Drosophila melanogaster displaying poor affinity for benzazepines. FEBS Lett 362:131-138.
119. Swarzenski BC, Tang L, Oh YJ, O'Malley KL, Todd RD. 1994. Morphogenic potentials of D2, D3, and D4 dopamine receptors revealed in transfected neuronal cell lines. Proc Natl Acad Sci U S A 91:649-653.
120. Swarzenski BC, O'Malley KL, Todd RD. 1996. PTX-sensitive regulation of neurite outgrowth by the dopamine D3 receptor. Neuroreport 7:573-576.
121. Takeuchi H, Kage E, Sawata M, Kamikouchi A, Ohashi K, Ohara M, Fujiyuki T, Kunieda T, Sekimizu K, Natori S, Kubo T. 2001. Identification of a novel gene, Mblk-1, that encodes a putative transcription factor expressed preferentially in the large-type Kenyon cells of the honeybee brain. Insect Mol Biol 10:487-494.
122. Tang S, Guo A. 2001. Choice behavior of Drosophila facing contradictory visual cues. Science 294:1543-1547.
123. Taylor DJ, Robinson GE, Logan BJ, Laverty R, Mercer AR. 1992. Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee. J Comp Physiol A170:715-721.
124. Temple BL, Livingstone MS, Quinn WG. 1984. Mutations in the dopa decarboxylase gene affect learning in Drosophila. Proc Natl Acad Sci U S A 81:3577-3581.
125. Todd RD. 1992. Neural development is regulated by classical neurotransmitters: dopamine D2 receptor stimulation enhances neurite outgrowth. Biol Psychiatry 31:794-807.
126. Toma DP, Bloch G, Moore D, Robinson GE. 2000. Changes in period mRNA levels in the brain and division of labor in honeybee colonies. Proc Nat Acad Sci U S A 97:6914-6919.
127. 1-dopamine receptors activate c-fos expression in the fetal suprachiasmatic nuclei. Proc Nat Acad Sci U S A 89:9201-9204.
128. Weaver DR, Roca AL, Reppert SM. 1995. c-fos And jun-B mRNAs are transiently expressed in fetal rodent suprachiasmatic nucleus following dopaminergic stimulation. Brain Res Dev Brain Res 85:293-297.
129. Winston ML. 1987. The biology of the honeybee. Cambridge, MA: Harvard University Press.
130. Witthöft W. 1967. Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morphol Tiere 61:160-184.
131. Yamamoto KK, Gonzales GA, Biggs WH, Montminy MR. 1988. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature 334:494-498.
132. 1 receptor expression by striatal astrocytes in culture. J Neurosci Res 58:544-552.
133. Zars T, Fischer M, Schulz R, Heisenberg M. 2000. Localization of short-term memory in Drosophila. Science 288:672-675.
134. Zerr DM, Hall JC, Rosbash M, Siwicki KK. 1990. Circadian fluctuations of the period protein immunoreactivity in the CNS and the visual system of Drosophila. J Neurosci 10:2749-2762.