Cultured insect mushroom body neurons express functional receptors for acetylcholine, GABA, glutamate, octopamine, and dopamine

Journal of Neurophysiology

Volumn 81, Issue 1, 1999, Pages 1-14

  Cayre, M ^a   Buckingham, S D ^a   Yagodin, S ^a   Sattelle, D B ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; ALPHA BUNGAROTOXIN; ATROPINE; CALCIUM; CALCIUM CHLORIDE; CHOLINERGIC RECEPTOR; DOPAMINE; DOPAMINE RECEPTOR; FURA 2; GLUTAMATE RECEPTOR; GLUTAMIC ACID; MECAMYLAMINE; MUSCIMOL; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; NICOTINE; OCTOPAMINE; PICROTOXIN; POTASSIUM CHLORIDE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; INSECT; INTERNEURON; ION CURRENT; NERVE CELL CULTURE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL;

EID: 0033028134     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.1.1     Document Type: Article

References (64)

1. BICKER, G. Taurine-like immunoreactivity in photoreceptor cells and mushroom bodies: a comparison of the chemical architecture of insect nervous system. Brain Res. 560: 201-206, 1991.
2. BICKER, G. AND KREISSL, S. Calcium imaging reveals nicotinic acetylcholine receptors on cultured mushroom body neurons. J. Neurophysiol. 71: 808-810, 1994.
3. BICKER, G. AND MENZEL, R. Chemical codes for the control of behaviour in arthropods. Nature 337: 33-39, 1989.
4. BICKER, G., SCHÄFER, S., AND KINGAN, T. G. Mushroom body feedback interneurones in the honeybee show GABA-like immunoreactivity. Brain Res. 360: 394-397, 1985.
5. BICKER, G., SCHÄFER, S., OTTERSEN, O. P., AND STORM-MATHISEN, J. Glutamate-like immunoreactivity in identified neuronal populations in insect nervous systems. J. Neurosci. 8: 2108-2122, 1988.
6. BIEBER, M. AND FULDNER, D. Brain growth during adult stage of a holometabolous insect. Naturwissenschaften 66: 426, 1979.
7. BLENAU, W., ERBER, J., AND BAUMANN, A. Characterization of a dopamine D1 receptor from Apis mellifera: cloning, functional expression, pharmacology, and mRNA localization in the brain. J. Neurochem. 70: 15-23, 1998.
8. BROTZ, T. M., BOCHENEK, B., ARONSTEIN, A., FFRENCH-CONSTANT, R. H., AND BORST, A. Gamma-aminobutyric acid receptor distribution in the mushroom body of a fly (Calliphora erythrocephala): a functional subdivision of Kenyon cells? J. Comp. Neurol. 383: 42-48, 1997.
9. 3[H] serotonin binding sites in the brain of the honeybee (Apis mellifera carnica). Verh. Ges. Pathol. 81: 859-860, 1987.
10. CAYRE, M., BUCKINGHAM, S. D., STRAMBI, A., STRAMBI, C., AND SATTELLE, D. B. Adult insect mushroom body neurons in primary culture: cell morphology and characterization of potassium channels. Cell Tissue Res. 291: 537-547, 1998.
11. CAYRE, M., STRAMBI, C., CHARPIN, P., AUGIER, R., MEYER, M. R., EDWARDS, J. S., AND STRAMBI, A. Neurogenesis in adult insect mushroom bodies. J. Comp. Neurol. 371: 300-310, 1996.
12. CAYRE, M., STRAMBI, C., AND STRAMBI, A. Neurogenesis in an adult insect brain and its hormonal control. Nature 368: 57-59, 1994.
13. DAVID, J. A. AND SATTELLE, D. B. Actions of cholinergic pharmacological agents on the cell body membrane of the fast coxal depressor motoneuron of the cockroach (Periplaneta americana). J. Exp. Biol. 108: 119-136, 1984.
14. DAVIS, R. L. Physiology and biochemistry of Drosophila learning mutants. Physiol. Rev. 76: 299-317, 1996.
15. DE BELLE, J. S. AND HEISENBERG, M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263: 692-695, 1994.
16. DUJARDIN, F. Mémoire sur le système nerveux des insectes. Ann. Sci. Nature Zool. 14: 547-560, 1850.
17. DURST, C., EICHMULLER, S., AND MENZEL, R. Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav. Neural Biol. 62: 259-263, 1994.
18. ERBER, J., KLOPPENBURG, P., AND SCHEIDLER, A. Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49: 1073-1083, 1993.
19. ERBER, J., MASHUR, T. H., AND MENZEL, R. Localisation of short term memory in the brain of the bee, Apis mellifera. Physiol. Entomol. 5: 343-358, 1980.
20. EVANS, P. D. Studies on the mode of action of octopamine, 5-hydroxytryptamine and proctolin on a myogenic rhythm in the locust. J. Exp. Biol. 110: 231-251, 1984.
21. EVANS, P. D. Octopamine. In: Comprehensive Insect Biochemistry, Physiology and Pharmacology, edited by G. A. Kerhut and L. Gilbert. Oxford: Pergamon, 1985, p. 499-530.
22. FAHRBACH, S. E. AND ROBINSON, G. E. Juvenile hormone, behavioral maturation, and brain structure in the honeybee. Dev. Neurosci. 18: 102-114, 1996.
23. FERVEUR, J. F., STÖRTKUHL, K. F., STOCKER, R. F., AND GREENSPAN, R. J. Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267: 902-905, 1995.
24. i and regulates electrical activity in insect neurosecretory cells (DUM neurons) via an acetylcholine receptor with "mixed" nicotinic-muscarinic pharmacology. Neurosci. Lett. 220: 142-146, 1996.
25. 2+ indicators with greatly improved fluorescent properties. J. Biol. Chem. 260: 3440-3450, 1985.
26. HAMILL, O. P., MARTY, A., NEHER, R., SAKMANN, B., AND SIGWORTH, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391: 85-110, 1981.
27. HAN, K.-A., MILLAR, N. S., GROTEWIEL, M. S., AND DAVIS, R. L. DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16: 1127-1135, 1996.
28. HAN, P. L., LEVIN, L. R., REED, R. R., AND DAVIS, R. L. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9: 619-627, 1992.
29. HARRISON, J. B., CHEN, H. H., SATTELLE, E., BARKER, P. J., HUSKISSON, N. S., RAUGH, J. J., BAI, D., AND SATTELLE, D. B. Immunocytochemical mapping of a C-terminus anti-peptide antibody to the GABA receptor subunit RDL, in the nervous system of Drosophila melanogaster. Cell Tissue Res. 284: 269-278, 1996.
30. HEISENBERG, M., BORST, A., WAGNER, S., AND BYERS, D. Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2: 1-30, 1985.
31. HEISENBERG, M., HEUSIPP, M., AND WANKE, C. Structural plasticity in the Drosophila brain. J. Neurosci. 15: 1951-1960, 1995.
32. HOMBERG, U., KINGAN, T. G., AND HILDEBRAND, J. G. Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res. 248: 1-24, 1987.
33. HOWES, E. A., CHEEK, T. R., AND SMITH, P.J.S. Long-term growth in vitro of isolated, fully differentiated neurones from the central nervous system of an adult insect. J. Exp. Biol. 156: 591-605, 1991.
34. HOWSE, P. E. Brain structure and behavior in insects. Annu. Rev. Entomol. 20: 359-379, 1975.
35. KREISSL, S. AND BICKER, G. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J. Comp. Neurol. 286: 71-84, 1989.
36. KREISSL, S., EICHMULLER, S., BICKER, G., RAPUS, J., AND ECKERT, M. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J. Comp. Neurol. 348: 583-595, 1994.
37. LAPIED, B., LE CORRONC, H., AND HUE, B. Sensitive nicotinic and mixed nicotinic-muscarinic receptors on insect neurosecretory cells. Brain Res. 533: 132-136, 1990.
38. LAURENT, G. AND NARAGHI, M. Odoranl-induced oscillations in the mushroom bodies of the locust. J. Neurosci. 14: 2993-3004, 1994.
39. LEITCH, B. AND LAURENT, G. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J. Comp. Neurol. 372: 487-514, 1996.
40. LOCOCO, D. J., THOMPSON, C. S., AND TOBE, S. S. Intercellular communication in an insect endocrine gland. J. Exp. Biol. 121: 407-419, 1986.
41. MENZEL, R. AND MÜLLER, U. Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19: 379-404, 1996.
42. MERCER, A. AND ERBER, J. The effects of amines on evoked potentials recorded in the mushroom bodies of the bee brain. J. Comp. Physiol. 151: 469-476, 1983.
43. MIZUNAMI, M., WEIBRECHT, J. M., AND STRAUSFELD, N. J. A new role for the insect mushroom bodies: place memory and motor control. In: Biological Neural Networks in Invertebrate Neuroethology and Robotics, edited by R. D. Beer, R. E. Ritzman, and T. McKenna. New York: Academic, 1993, p. 199-225.
44. MÜLLER, U. 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, 1997.
45. NÄSSEL, D. R. AND ELEKES, L. Aminergic neurons in the brain of blowflies and Drosophila: dopamine-and tyrosine hydroxylase-immunoreactive neurons and their relationships with putative histaminergic neurones. Cell Tissue Res. 267: 147-167, 1992.
46. NIGHORN, A., HEALY, M. J., AND DAVIS, R. L. The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6: 455-467, 1991.
47. O'DELL, K.M.C., ARMSTRONG, J. D., YANG, M. Y., AND KAISER, K. Functional dissection of Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15: 55-61, 1995.
48. SATTELLE, D. B. GABA receptors of insects. Adv. Insect Physiol 22: 2-113, 1990.
49. SCHÄFER, S. AND BICKER, G. Distribution of GABA-like immunoreactivity in the brain of the honeybee. J. Comp. Neurol. 246: 287-300, 1986.
50. SCHÄFER, S., BICKER, G., OTTERSEN, O. P., AND STORM-MATHISEN, J. Taurine-like immunoreactivity in the brain of the honeybee. J. Comp. Neurol. 268: 60-70, 1988.
51. SCHÄFER, S. AND REHDER, V. Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J. Comp. Neurol. 280: 43-58, 1989.
52. SCHÄFER, S., ROSENBOOM, H., AND MENZEL, R. Ionic currents of Kenyon cells from the mushroom body of the honeybee. J. Neurosci. 14: 4600-4612, 1994.
53. 125I)α-bungarotoxin binding sites in honeybee brain. Brain Res. 534: 332-335, 1990.
54. SCHILBERGER, K. Some physiological features of mushroom body linked fibers in the house cricket brain. Naturwissenschaften 67: 623, 1981.
55. SCHILBERGER, K. Local interneurons associated with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res. 230: 573-586, 1983.
56. SKOULAKIS, E. M., KALDERON, D., AND DAVIS, R. L. Preferential expression in the mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11: 1-14, 1993.
57. STRAMBI, C., CAYRE, M., SATTELLE, D. B., AUGIER, R., CHARPIN, P., AND STRAMBI, A. Immunocytochemical mapping of an RDL-like GABA receptor subunit and of GABA in brain structures related to learning and memory in the cricket. Learning Memory 5: 78-89, 1998.
58. STRAUSFELD, N. J. Atlas of an Insect Brain. Berlin: Springer-Verlag, 1976, p. 123-131.
59. STRAUSFELD, N. J., BUSCHBECK, E. K., AND GOMEZ, R. S. The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. In: The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach, edited by O. Breidbach and W. Kutsch. Basel: Birkhäuser, 1995, p. 349-381.
60. TECHNAU, G. M. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J. Neurogenet. 1: 113-126, 1984.
61. TECHNAU, G. M. AND HEISENBERO, M. Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295: 405-407, 1982.
62. WITHERS, G. S., FARBACH, S. E., AND ROBINSON, G. E. Selective neuroanatomy and division of labour in honeybee. Nature 364: 238-240, 1993.
63. + currents and the cAMP-dependent modulation in cultured Drosophila mushroom body neurons identified by lacZ expression. J. Neurosci. 15: 1025-1034, 1995.
64. YANG, M. Y., ARMSTRONG, J. D., VILINSKY, I., STRAUSFELD, N. J., AND KAISER, K. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15: 45-54, 1995.