Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera

Journal of Comparative Physiology - A Sensory, Neural, and Behavioral Physiology

Volumn 185, Issue 6, 1999, Pages 565-576

  Grunewald B ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Inhibitory feedback neurons; Insect; Intracellular recording; Olfactory learning; Sensitisation

Indexed keywords

EID: 0343938859     PISSN: 03407594     EISSN: None     Source Type: Journal    
DOI: 10.1007/s003590050417     Document Type: Article

References (59)

1. Bicker G, Schäfer S, Kingan TG (1985) Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity. Brain Res 360: 394-397
2. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psyc 97: 107-119
3. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39
4. Brotz TM, Bochenek B, Aronstein K, Ffrench-Constant RH, Borst A (1997) gamma-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
5. 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
6. Davis RL (1993) Mushroom bodies and Drosophila learning. Neuron 11: 1-14
7. De Belle JS, Heisenberg M (1994) Associative learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263: 692-695
8. Dubnau J, Tully T (1998) Gene discovery in Drosophila. Annu Rev Neurosci 21: 407-444
9. Dykes RW (1997) Mechanisms controlling neuronal plasticity in somatosensory cortex. Can J Physiol Pharmacol 75: 535-545
10. Erber J (1978) Response characteristics and after effects of multimodal neurons in the mushroom body area of the honey bee. Physiol Entomol 3: 77-89
11. Erber J, Homberg U, Gronenberg W (1987) Functional roles of the mushroom bodies in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. John Wiley and Sons, New York, pp 485-511
12. 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
13. Fahrbach SE, Robinson GE (1995) Behavioural development in the honey bee: toward the study of learning under natural conditions. Learn & Mem 2: 199-224
14. Goldberg F, Grünewald B, Rosenboom H, Menzel R (1999) Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera. J Physiol 514: 759-768
15. Goll W (1967) Strukturuntersuchungen am Gehirn von Formica. Z Morphol Oekol Tiere 59: 145-210
16. Gronenberg W (1986) Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain. J Insect Physiol 32: 695-704
17. Gronenberg W (1987) Anatomical and physiological properties of feedback neurons of the mushroom bodies in the bee brain. Exp Biol 46: 115-125
18. Grünewald B (1999) Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. J Comp Neurol 404: 114-126
19. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366: 59-63
20. Hammer M (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci 20: 245-252
21. Hammer M, Braun G, Mauelshagen J (1994) Food-induced arousal and nonassociative learning in honeybees: dependence of sensitisation on the application site and duration of food stimulation. Behav Neural Biol 62: 210-223
22. Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15: 1617-1630
23. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn & Mem 5: 146-156
24. Harrison JB, Chen HH, Sattelle E, Barker PJ, Huskisson NS, Rauh JJ, Sattelle DB (1999) 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
25. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2: 1-30
26. Hesslow G, Ivarsson M (1996) Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Exp Brain Res 110: 36-46
27. Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154: 825-836
28. Homberg U, Erber J (1979) Response characteristics and identification of extrinsic mushroom body neurons of the brain. Z Naturf 34c: 612-615
29. Homberg U, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248: 1-24
30. Kim JJ, Krupa DJ, Thompson RF (1998) Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279: 570-573
31. Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Ser VI Zool 13: 458-464
32. Laurent G, Naraghi M (1994) Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14: 2993-3004
33. Leitch B, Laurent G (1996) GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 372: 478-514
34. Li Y, Strausfeld NJ (1997) Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J Comp Neurol 387: 631-650
35. MacLeod K, Bäcker A, Laurent G (1998) Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395: 693-698
36. Mauelshagen J (1993) Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. J Neurophysiol 69: 609-625
37. Menzel R (1990) Learning, memory, and "cognition" in honey bees. In: Kesner RP, Olton DS (eds) Neurobiology of comparative cognition. Lawrence Erlbaum, Hillsdale, New Jersey, pp 237-292
38. Menzel R, Durst C, Erber J, Eichmüller S, Hammer M, Hildebrandt H, Mauelshagen J, Müller U, Rosenboom H, Rybak J, Schäfer S, Scheidler A (1994) The mushroom bodies in the honeybee: from molecules to behaviour. In: Schildberger K, Elsner N (eds) Fortschritte der Zoologie, vol 39. Neural basis of behavioural adaptations. Fischer, Stuttgart, pp 81-102
39. Menzel R, Erber J, Masuhr T (1974) Learning and memory in the honeybee. In: Barton Browne L (ed) Experimental analysis of insect behaviour. Springer, Berlin Heidelberg New York, pp 195-217
40. Menzel R, Hammer M, Braun G, Mauelshagen J (1991) Neurobiology of learning and memory in honeybees. In: Goodman LJ, Fisher RC (eds) The behaviour and physiology of bees. C.A.B. International, Wallingford, pp 323-353
41. Menzel R, Müller U (1996) Learning and memory in honeybees: from behaviour to neural substrates. Annu Rev Neurosci 19: 379-404
42. Mobbs PG (1982) The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Phil Trans R Soc Lond B 298: 309-354
43. Mobbs PG (1984) Neural networks in the mushroom bodies of the honeybee. J Insect Physiol 30: 43-58
44. Mobbs PG (1985) Brain structure. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology. Pergamon Press, Oxford, pp 299-370
45. Rosenboom H, Goldberg F, Schäfer S, Menzel R (1994) Ionic currents of Kenyon cells possibly involved in olfactory learning in insects. Soc Neurosci Abstr 20: 333.19
46. Rybak J, Menzel R (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 334: 444-465
47. Rybak, J Menzel R (1998) Integrative properties of the Pel neuron, a unique mushroom body output neuron. Learn & Mem 5: 133-145
48. Schäfer S, Rosenboom H, Menzel R (1994) Ionic currents of Kenyon cells from the mushroom body of the honeybee. J Neurosci 14: 4600-4612
49. Schürmann F-W (1973) Über die Struktur der Pilzkörper des Insektengehirns III. Die Anatomie der Nervenfasern in den Corpora pedunculata bei Acheta domesticus L (Orthoptera): Eine Golgi-Studie. Z Zellforsch 145: 247-285
50. Schürmann F-W (1987) The architecture of the mushroom bodies and related neuropils in the insect brain. In: Gupta AP (ed) Arthropod brain. Its evolution, development, structure, and functions. John Wiley and Sons, New York, pp 231-256
51. Schildberger K (1981) Some physiological features of mushroom-body linked fibers in the house cricket brain. Naturwissenschaften 67: 623-624
52. Schildberger K (1983) Local interneurons associated with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res 230: 573-587
53. Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154: 71-79
54. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature (Lond) 390: 70-74
55. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
56. Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Annu Rev Neurosci 17: 519-549
57. Tomasulo RA, Ramirez JJ, Steward O (1993) Synaptic inhibition regulates associative interactions between afferents during the induction of long-term potentiation and depression. Proc Natl Acad Sci USA 90: 11578-11582
58. Vareschi E (1971) Odor discrimination in the honey bee - single cell and behavioural response. Z Vergl Physiol 75: 143-173
59. Weiss MJ (1978) Giant fiber associated with mushroom body neuropiles in an insect brain: a possible one-cell feedback loop. Soc Neurosci Abstr 4: 210