Parallel organization in honey bee mushroom bodies by peptidergic Kenyon cells

Journal of Comparative Neurology

Volumn 424, Issue 1, 2000, Pages 179-195

  Strausfeld, Nicholas J ^a   Homburg, Uwe ^b   Kloppenberg, Peter ^a,c,d  

^a UNIVERSITY OF ARIZONA   (United States)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c Department of Population Medicine and Diagnostic Sciences   (United States)

^d Department of Materials Science and Engineering   (United States)

Author keywords

Apis mellifera; Efferent neurons; Gastrin cholecystokinin; Insect brain; Kenyon cells; Parallel processing; Phe Met Arg Phe NH2 amide; Sensory representation

Indexed keywords

CHOLECYSTOKININ DERIVATIVE; PROTEIN ANTIBODY; TETRAPEPTIDE;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENDRITE; HONEYBEE; IMAGE RECONSTRUCTION; IMMUNOREACTIVITY; NERVE FIBER; NERVE PROJECTION; NEUROANATOMY; NEUROPIL; NONHUMAN; PEPTIDERGIC NERVOUS SYSTEM; PERIKARYON; PERIPLANETA; PRIORITY JOURNAL; SPECIES DIFFERENCE;

ANIMALS; BEES; CENTRAL NERVOUS SYSTEM; NEUROGLIA; NEURONS; NEUROPEPTIDES; SILVER STAINING;

EID: 0034648319     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/1096-9861(20000814)424:1<179::AID-CNE13>3.0.CO;2-K     Document Type: Article

References (70)

1. Bicker G. 1991. Taurine-like immunoreactivity in photoreceptor cells and mushroom bodies: a comparison of the chemical architecture of insect nervous systems. Brain Res 568:201-206.
2. Bicker G, Schäfer S, Kingen TG. 1985. Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity. Brain Res 360:394-397.
3. Bicker G, Schäfer S, Ottersen OP, Storm-Mathisen J. 1988. Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. J Neurosci 8:2108-2122.
4. Bodian D. 1936. A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat Rec 65:89-97.
5. Boer HH, Schot LP, Roubos EW, ter Maat A, Lodder JC, Reichelt D, Swaab F. 1979. ACTH-like immunoreactivity in two electronically coupled giant neurons in the pond snail Lymnaea stagnalis. Cell Tissue Res 202:231-240.
6. Brotz TM, Bochenek B, Aronstein K, ffrench-Constant RH, Borst A. 1997. γ-Aminobutyric acid receptor distribution in the mushroom bodies of a fly (Calliphora erythrocephala): a functional subdivision of Kenyon cells? J Comp Neurol 383:42-48.
7. Crittenden JR, Skoulakis EMC, Han K-A, Kalderon D, Davis RL. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learning Memory 5:38-51.
8. Erber J, Kloppenberg P, Scheidler A. 1991. Neuromodulation in the honeybee: autoradiography, behavior and electrophysiology. In: Goodman LJ, Fisher RC, editors. The behavior and physiology of bees. Wallingford: CAB International. p 273-287.
9. Farris SM, Robinson GE, Davis RL, Fahrbach SE. 1999. Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera. J Comp Neurol 414:97-113.
10. Flögel JHL. 1878. Über die einheitlichen Bau des Gehirns in den verschiedenen Insecten-Ordnungen. Z Wiss Zool 30:556-592.
11. Frontali N, Mancini G. 1970. Studies on the neuronal organization of cockroach corpora pedunculata. J Insect Physiol 16:2293-2301.
12. Goll W. 1967. Strukturuntersuchungen am Gehirn von Formica. Z Morphol Oekol Tiere 59:143-210.
13. Gronenberg W. 1987. Anatomical and physiological properties of feedback neurons of the mushroom bodies in the bee brain. Exp Biol 46:115-125.
14. Gronenberg W. 1999. Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54:85-95.
15. Grünewald B. 1999. Morphology of feedback neurons in the mushroom body of the honey bee, Apis mellifera. J Comp Neurol 404:114-126.
16. Grünewald B. 2000. Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee Apis mellifera. J Comp Physiol A 185:565-576.
17. 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.
18. Hammer M, Menzel R. 1995 Learning and memory in the honeybee. J Neurosci 15:1617-1630.
19. Heisenberg M. 1998. What do the mushroom bodies do for the inset brain? Learning Memory 5:1-10.
20. Homberg U. 1994. Distribution of neurotransmitters in the insect brain. Progr Zool 40:1-88.
21. Homberg U, Erber J. 1979. Response characteristics and identification of extrinsic mushroom body neurons of the bee. Z Naturforsch 34:612-615.
22. Homberg U, Davis NT, Hildebrand JG. 1991. Peptide-immunocytochemistry of neurosecretory cells in the brain and retrocerebral complex of the sphinx moth Manduca sexta. J Comp Neurol 303:35-52.
23. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto, D. 1997. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761-771.
24. Ito K Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ. 1998. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learning Memory 5:52-77.
25. Jawlowski H. 1959. The structure of the corpora pedunculata in Aculeata. Hymenoptera. Folia Biologica 7:61-70.
26. 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.
27. Klemm N. 1983. Monoamine-containing neurons and their projections in the brain (supraoesophageal ganglion) of cockroaches. Cell Tissue Res 229:379-402.
28. Kreissl S, Eichmuller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348:583-595.
29. Landis M, Hansen L, Merchant N, Strausfeld NJ. 1996. Sharing 3D Data Explorer on the World Wide Web. IBM Communiqué 4:9-11.
30. Laurent G, Naraghi M. 1994. Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14:2993-3004.
31. Lee T, Lee A, Luo L. 1999. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-4076.
32. Li YS, Strausfeld NJ. 1997. Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach Periplaneta americana. J Comp Neurol 386:1-20.
33. Li YS, Strausfeld NJ. 1999. Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. J Comp Neurol 409: 647-663.
34. Liu L, Wolf R, Ernst R, Heisenberg M. 1999. Context generalization in Drosophila visual learning requires the mushroom bodies. Nature 400: 753-756.
35. Mancini G, Frontali N. 1970. On the ultrastructural localization of catecholamines in the beta lobes (corpora pedunculata) of Periplaneta americana. Z Zellforsch 103:341-350.
36. Mauelshagen J. 1993. Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J Neurophysiol 69:609-625.
37. Mizunami M, Weibrecht JM, Strausfeld NJ. 1998a. Mushroom bodies of the cockroach: their participation in place memory. J Comp Neurol 402:520-537.
38. Mizunami M, Okada R, Li YS, Strausfeld NJ. 1998b. Mushroom bodies of the cockroach: activity and identities of neurons recorded in freely moving animals. J Comp Neurol 402:501-519.
39. Mizunami M, Iwasaki M, Okada R, Nishikawa M. 1998c. Topography of four classes of Kenyon cells in the mushroom bodies of cockroaches. J Comp Neurol 399:162-175.
40. Mobbs PG. 1982. The brain of the honeybee Apis mellifera I. The connections and spatial organizations of the mushroom bodies. Phil Trans R Soc London B 298:309-354.
41. Nässel DR, Elekes K. 1992. Aminergic neurons in the brains of blowflies and Drosophila: dopamine- and tyrosine hydroxylase immunoreactive neurons and their relationships with putative histaminergic neurons. Cell Tissue Res 267:147-167.
42. Noble JM, Goodman LJ. 1987. Immunohistochemical localization of a gastrin/CCK-like peptide in the brain of the honeybee. In: Menzel R, Mercer A, editors. Neurobiology and behavior of honeybees. Berlin: Springer, p 235-243.
43. O'Donohue TL, Bishop JF, Chronwall BM, Groome J, Watson WH. 1984. Characterization and distribution of FMRFamide immunoreactivity in the rat central nervous system. Peptides 5:563-568.
44. O'Shea M, Colbert R, Williams L, Dunn S. 1998. Nitric oxide compartments in the mushroom bodies of a locust brain. Neuroreport 9:333-336.
45. Pearson L. 1971. The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera: an anatomical study. Phil Trans R Soc London B 259:477-516.
46. Pflugfelder O. 1937. Vergleichende-anatomische, experimentelle, und embryologische Untersuchungen über das Nervensystem und die Sinnesorgane der Rhynchoten. Zool Stuttgart 34:1-102.
47. 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.
48. Rybak J, Menzel R. 1998. Integrative properties of the Pel neuron, a unique mushroom body output neuron. Learning Memory 5:133-145.
49. Sánchez DS. 1940. Contribucion à la connaissance des centres nerveux des insectes: nouveux apports sur la structure du cerveau des abeilles (Apis mettifica). I. Introduction. Tab Lab Rech Biol Univ Madrid 32:123-210.
50. Sánchez DS. 1941. Contribucion à la connaissance des centres nerveux des insectes: nouveux apports sur la structure du cerveau des abeilles (Apis mellifica). II. Deutocérébron. Tab Lab Rech Biol Univ Madrid 33:165-236.
51. Schäfer S, Rehder V. 1989. Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43-58.
52. Schäfer S, Bicker G, Otterson OP, Storm-Mathisen J. 1988. Taurine-like immunoreactivity in the brain of the honeybee. J Comp Neurol 265: 60-70.
53. 125I] α-bungarotoxin binding sites in honeybee brain. Brain Res 534:332-335.
54. Schildberger K. 1984. Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71-79.
55. Schürmann FW. 1970. Über die Struktur der Pilzkörper des Insektenhirns. I. Synapsen in pedunculus. Z Zellforsch Mikrosk Anat 103:365-381.
56. Schürmann FW. 1971. Synaptic contacts of association fibres in the brain of the bee. Brain Res 26:169-176.
57. Schürmann FW. 1972. Über die Struktur der Pilzkörper des Insektenhirns. II. Synaptische Schaltungen im Alpha-Lobus des Heimschens Acheta domesticus L. Z Zellforsch Mikrosk Anat 127:240-257.
58. Schürmann FW. 1973. Über die Struktur der Pilzkörper des Insektenhirns. III. Die Anatomie der Nervenfasern in den Corpora pedunculata bei Acheta domesticus L. (Orthoptera): eine Golgi-studie. Z Zellforsch Mikrosk Anat 145:247-285.
59. Schürmann FW, Erber J. 1990. FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifera). A light- and electron microscopical study. Neuroscience 3:797-807.
60. Schürmann FW, Ottersen OP, Honegger HW. 2000. Glutamate-like immunoreactivity marks compartments of the mushroom bodies in the brain of the cricket. J Comp Neurol 418:227-239.
61. Strausfeld, NJ. 1970. Variations and invariants of cell arrangements in the nervous system of insects. A review of neural arrangements in the visual system and corpora pedunculata. Verh Dtsch Zool Ges 64:97-107.
62. Strausfeld NJ. 1976. Atlas of an insect brain. Heidelberg: Springer.
63. Strausfeld NJ. 1998a. Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertabrates. Brain Behav Evol 52:185-206.
64. Strausfeld NJ. 1998b. Structural evidence for functional subdivisions in insect mushroom bodies. Soc Neurosci Abstr 24:1192.
65. Strausfeld NJ, Li YS. 1999a. Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. J Comp Neurol 409:603-625.
66. Strausfeld NJ, Li YS. 1999b. Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies. J Comp Neurol 409: 626-646
67. Strausfeld NJ, Hansen L, Li Y-S, Gomez RS, Ito K. 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning Memory 5:11-37.
68. Vowles DM. 1955. The structure and connections of the corpora pedunculata in bees and ants. Q J Microsc Sci 96:239-255.
69. Witthöft W. 1967. Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morphol 108:160-184.
70. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K. 1995. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15:45-54.