Muscarinic regulation of Kenyon cell dendritic arborizations in adult worker honey bees

Arthropod Structure and Development

Volumn 40, Issue 5, 2011, Pages 409-419

  Dobrin, Scott E ^a   Herlihy, J Daniel ^b   Robinson, Gene E ^c   Fahrbach, Susan E ^a,b  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b WAKE FOREST UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Apis mellifera; Dendritic spine; Golgi technique; Mushroom bodies

Indexed keywords

MUSCARINIC RECEPTOR; PILOCARPINE; SCOPOLAMINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC CELL; FORAGING; GOLGI COMPLEX; GROWTH INHIBITION; HONEYBEE; KENYON CELL; NERVE CELL GROWTH; NERVE FIBER GROWTH; NEUROPIL; NONHUMAN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VARROA; VISUAL CORTEX;

ANIMALS; BEES; BEHAVIOR, ANIMAL; CHOLINERGIC ANTAGONISTS; DENDRITES; DENDRITIC SPINES; INSECT PROTEINS; MUSCARINIC AGONISTS; MUSHROOM BODIES; PILOCARPINE; RECEPTORS, CHOLINERGIC; SCOPOLAMINE HYDROBROMIDE; SIGNAL TRANSDUCTION;

APIS MELLIFERA; BASIDIOMYCOTA;

EID: 80052872126     PISSN: 14678039     EISSN: 18735495     Source Type: Journal    
DOI: 10.1016/j.asd.2011.01.003     Document Type: Article

References (59)

1. Bennett E.L., Diamond M.C., Krech P., Rosenzweig M.R. Chemical and anatomical plasticity of the brain. Science 1964, 146:610-619.
2. Bicker G. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microscopy Research and Technique 1999, 45:174-183.
3. Brandon J., Coss R. Rapid dendritic spine shortening during one-trial learning: the honeybee's first orientation flight. Brain Research 1982, 252:51-61.
4. Burrows M. The Neurobiology of an Insect Brain 1996, Oxford University Press, Oxford, UK.
5. Coss R.G., Brandon J.G., Globus A. Changes in morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experience. Brain Research 1980, 192:49-59.
6. Dukas R., Visscher P. Lifetime learning by foraging honey bees. Animal Behaviour 1994, 48:1007-1012.
7. Durst C., Eichmuller S., Menzel R. Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behavioral Neural Biology 1994, 62:259-263.
8. 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.
9. Fahrbach S.E. Structure of the mushroom bodies of the insect brain. Annual Review of Entomology 2006, 51:209-232.
10. Fahrbach S.E., Strande J.L., Robinson G.E. Neurogenesis is absent in the brains of adult honey bees and does not explain behavioral neuroplasticity. Neuroscience Letters 1995, 197:145-148.
11. Farris S.M., Roberts N.S. Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proceedings of the National Academy of Sciences USA 2005, 102:17394-17399.
12. 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.
13. Farris S.M., Robinson G.E., Davis R.L., Fahrbach S.E. Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera. Journal of Comparative Neurology 1999, 414:97-113.
14. Farris S.M., Robinson G.E., Fahrbach S.E. Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the worker honeybee. Journal of Neuroscience 2001, 21:6395-6404.
15. Frambach I., Rössler W., Winkler M., Schürmann F.W. F-actin at identified synapses in the mushroom body neuropil of the insect brain. Journal of Comparative Neurology 2004, 475:303-314.
16. Groh C., Meinertzhagen I.A. Brain plasticity in diptera and hymenoptera. Frontiers in Bioscience 2010, 2:268-288.
17. Groh C., Tautz J., Rössler W. Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proceedings of the National Academy USA 2004, 101:4268-4273.
18. Groh C., Ahrens D., Rössler W. Environment- and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behavior Evolution 2006, 68:1-14.
19. Gronenberg W. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. Journal of Comparative Neurology 2001, 435:474-489.
20. Gronenberg W., Heeren S., Hölldobler B. Age-dependent and task-related morphological changes in the brain and mushroom bodies of the ant Camponotus floridanus. Journal of Experimental Biology 1996, 199:2011-2019.
21. Hourcade B., Muenz T.S., Sandoz J., Rössler W., Devaud J. Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain?. Journal of Neuroscience 2010, 30:6461-6465.
22. Huang Z., Knowles C. Nicotinic and muscarinic cholinergic receptors in honey bee (Apis mellifera) brain. Comparative Biochemistry and Physiology 1990, 97C:275-281.
23. Ismail N., Robinson G.E., Fahrbach S.E. Stimulation of muscarinic receptors mimics experience-dependent plasticity in the honey bee brain. Proceedings of the National Academy USA 2006, 103:207-211.
24. Ismail N., Christine S., Robinson G.E., Fahrbach S.E. Pilocarpine improves recognition of nestmates in young honey bees. Neuroscience Letters 2008, 439:178-181.
25. Jones T.A., Donlan N.A., O'Donnell S. Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiology of Learning and Memory 2009, 92:485-495.
26. Kenyon F.C. The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda. Journal of Comparative Neurology 1896, 6:133-210.
27. Kozorovitskiy Y., Gross C.G., Kopil C., Battaglia L., McBreen M., Stranahan A.M., Gould E. Experience induces structural and biochemical changes in the adult primate brain. Proceedings of the National Academy USA 2005, 102:17478-17482.
28. Kreissl S., Bicker G. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. Journal of Comparative Neurology 1989, 286:71-84.
29. Krofczik S., Khojasteh U., de Ibarra N.H., Menzel R. Adaptation of microglomerular complexes in the honeybee mushroom body lip to manipulations of behavioral maturation and sensory experience. Developmental Neurobiology 2008, 68:1007-1017.
30. Li Y., Strausfeld N. 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.
31. Lorenz M.W., Kellner R., Völkl W., Hoffmann K.H., Woodring J. A comparative study on hypertrehalosaemic hormones in the hymenoptera: sequence determination, physiological actions and biological significance. Journal of Insect Physiology 2001, 47:563-571.
32. Lozano V.C., Armengaud C., Gauthier M. Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. Journal of Comparative Physiology A 2001, 187:249-254.
33. Lutz C.C., Rodriguez-Zas S.L., Fahrbach S.E., Robinson G.E. Effects of foraging experience on gene expression in the honey bee brain 2009, Society for Neuroscience Annual Meeting, San Diego.
34. Maleszka J., Barron A.B., Helliwell P.G., Maleszka R. Effect of age, behaviour and social environment on honey bee brain plasticity. Journal of Comparative Physiology A 2009, 195:733-740.
35. McEwen B.S. Stress and hippocampal plasticity. Annual Review of Neuroscience 1999, 22:105-122.
36. Menzel R., Blakers M. Colour receptors in the bee eye - morphology and spectral sensitivity. Journal of Comparative Physiology A 1976, 108:11-33.
37. Mobbs P.G. The brain of the honeybee Apis mellifera L. The connections and spatial organization of the mushroom bodies. Philosophical Transactions Royal Society of London B 1982, 298:309-354.
38. Molina Y., Harris R.M., O'Donnell S. Brain organization mirrors caste differences, colony founding and nest architecture in paper wasps (Hymenoptera: Vespidae). Proceedings of the Royal Biological Society B 2009, 276:3345-3351.
39. Mujagic S., Sarkander J., Erber B., Erber J. Sucrose acceptance and different forms of associative learning of the honey bee (Apis mellifera L.) in the field and laboratory. Frontiers in Behavioral Neuroscience 2010, 4:46.
40. O'Donnell S., Donlan N.A., Jones T.A. Mushroom body structural change is associated with division of labor in eusocial wasp workers (Polybia aequatorialis, Hymenoptera: Vespidae). Neuroscience Letters 2004, 356:159-162.
41. Peitsch D., Fietz A., Hertel H., deSouza J., Ventura D.F., Menzel R. The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology A 1992, 170:23-40.
42. Riege W.H. Environmental influences on brain and behavior of year-old rats. Developmental Psychobiology 1971, 4:157-167.
43. Schippers M., Dukas R., Smith R., Wang J., Smolen K., McClelland G. Lifetime performance in foraging honeybees: behaviour and physiology. Journal of Experimental Biology 2006, 209:3828-3836.
44. 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.
45. Seid M.A., Wehner R. Delayed axonal pruning in the ant brain: a study of developmental trajectories. Developmental Neurobiology 2009, 69:350-364.
46. Seid M., Harris K., Traniello J. Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. Journal of Comparative Neurology 2005, 488:269-277.
47. Shapira M., Thompson C.K., Soreq H., Robinson G. Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. Journal of Molecular Neuroscience 2001, 17:1-12.
48. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. Journal of Anatomy 1953, 87:387-407.
49. Stieb S.M., Muenz T.S., Wehner R., Rössler W. Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis. Developmental Neurobiology 2010, 70:408-423.
50. Stranahan A.M., Khalil D., Gould E. Running induces widespread structural alterations in the hippocampus and entorhinal cortex. Hippocampus 2007, 17:1017-1022.
51. 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.
52. Velarde R.A., Robinson G.E., Fahrbach S.E. Coordinated responses to developmental hormones in the Kenyon cells of the adult worker honey brain (Apis mellifera L.). Journal of Insect Physiology 2009, 55:59-69.
53. Volkmar F.R., Greenough W.T. Rearing complexity affects branching of dendrites in the visual cortex of the rat. Science 1972, 176:1445-1447.
54. Winston M.L. The biology of the honey bee 1987, Harvard UP, Cambridge, MA.
55. Withers G.S., Fahrbach S.E., Robinson G.E. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 1993, 364:238-240.
56. Withers G.S., Fahrbach S.E., Robinson G.E. Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. Journal of Neurobiology 1995, 26:130-144.
57. Withers G.S., Day N.F., Talbot E.F., Dobson H.E., Wallace C.S. Experience-dependent plasticity in the mushroom bodies of the solitary bee Osmia lignaria (Megachilidae). Developmental Neurobiology 2008, 68:73-82.
58. Yasuyama K., Salvaterra P.M. Localization of choline acetyltransferase-expressing neurons in drosophila nervous system. Microscopy Research Techniques 1999, 45:65-79.
59. Yasuyama K., Meinertzhagen I., Schürmann F. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. Journal of Comparative Neurology 2002, 445:211-226.