The effects of queenlessness on the maturation of the honey bee olfactory system

Behavioural Brain Research

Volumn 91, Issue 1-2, 1998, Pages 115-126

  Morgan, Stewart M ^a   Butz Huryn, Vivian M ^a   Downes, Stephen R ^a   Mercer, Alison R ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Apis mellifera; Development; Learning; Olfaction; Structural plasticity

Indexed keywords

PHEROMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BRAIN DEVELOPMENT; CHEMORECEPTOR; CONDITIONING; CONTROLLED STUDY; HONEYBEE; LEARNING; MATURATION; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; STATE DEPENDENT LEARNING;

AGING; ANIMALS; ASSOCIATION LEARNING; BEES; BRAIN; CONDITIONING, OPERANT; FEEDING BEHAVIOR; LEARNING; OLFACTORY PATHWAYS; REFLEX; SENSE ORGANS; SMELL; SOCIAL BEHAVIOR;

EID: 0032033230     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(97)00118-6     Document Type: Article

References (102)

1. Allan S.A., Slessor K.N., Winston M.L., King G.G.S. The influence of age and task specialization on the production and perception of honey bee pheromones. J Insect Physiol. 33:1987;917-922.
2. Allen M.D. Observations of honeybees attending their queen. Br J Anim Behav. 3:1955;66-69.
3. Allen M.D. The honeybee queen and her attendants. Anim Behav. 8:1960;201-208.
4. Arnold G., Masson C., Budharugsa S. Demonstration of a sexual dimorphism in the olfactory pathways of the drones of Apis mellifica L. (Hymenoptera, Apidae). Experientia. 40:1984;723-725.
5. Arnold G., Masson C., Budharugsa S. Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone (Apis mellifera). Cell Tissue Res. 242:1985;593-605.
6. Bailey C.H., Chen M. Morphological aspects of synaptic plasticity in Aplysia: an anatomical substrate for long-term memory. Ann NY Acad Sci. 627:1991;181-196.
7. Bailey C.H., Kandel E.R. Structural changes accompanying memory storage. Annu Rev Physiol. 55:1993;397-426.
8. Bhagavan S., Benatar S., Cobey S., Smith B.H. Effect of genotype but not of age or caste on olfactory learning performance in the honey bee, Apis mellifera. Anim Behav. 48:1994;1357-1369.
9. Boeckh J., Ernst K.-D. Contribution of single unit analysis in insects to an understanding of olfactory function. J Comp Physiol A. 161:1987;549-565.
10. Boeckh J., Tolbert L.P. Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech. 24:1993;260-280.
11. Brandes C. Estimation of heritability of learning behaviour in honeybees (Apis mellifera capensis). Behav Genet. 1:1988;119-131.
12. Brandon J.G., Coss R.G. Rapid dendritic spine stem shortening during one-trial learning: the honeybee's first orientation flight. Brain Res. 252:1982;51-61.
13. Brockman A., Brückner D. Zur funktionellen Organisation des antennalen und olfaktorischen Systems der Arbeiterin der Honigbiene, Apis mellifera L. Apidologie. 24:1993;219-233.
14. Burrows M., Boeckh J., Esslen J. Physiological and morphological properties of interneurons in the deutocerebrum of male cockroaches which respond to female pheromone. J Comp Physiol A. 145:1982;447-457.
15. Butler C.G. Insect pheromones. Biol Rev. 42:1967;42-87.
16. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell. 78:1994;823-834.
17. Christensen TA, Hildebrand JG. Functions, organization and physiology of the olfactory pathways in the lepidopteran brain. In: Gupta AP, editor. Arthropod Brain: Its Evolution, Development, Structure and Functions. New York: Wiley, 1987:457-84.
18. Christensen T.A., Hildebrand J.G. Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth, Manduca sexta. J Comp Physiol A. 160:1987;553-569.
19. Collins A.M. Effect of age on the response to alarm pheromones by caged honeybees. Ann Entomol Soc Am. 73:1980;307-309.
20. Coss R.G., Brandon J.G., Globus A. Changes in morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experiences. Brain Res. 192:1980;49-59.
21. De Voogd T.J., Nottebohm F. Gonadal hormones induce dendritic growth in the adult avian brain. Science. 214:1981;202-204.
22. Durst C., Eichmüller S., Menzel R. Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav Neural Biol. 62:1994;259-263.
23. Erber J. Neural correlates of learning in the honeybee. Trends Neurosci. 1:1981;270-273.
24. Esslen J., Kaissling K.E. Zahl und Verteilung antennaler Sensillen bei der Honigbiene. Zoomorphologie. 83:1976;227-251.
25. Fahrbach S.E., Robinson G.E. Juvenile hormone, behavioural maturation and brain strucutre in the honey bee. Dev Neurosci. 18:1995;102-114.
26. Fahrbach S.E., Giray T., Robinson G.E. Volume changes in the mushroom bodies of adult honey bee queens. Neurobiol Learn Memory. 63:1995;181-191.
27. Flanagan D., Mercer A.R. An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol. 18:1989;145-159.
28. Flanagan D., Mercer A.R. Morphology and response characteristics of neurons in the deutocerebrum of the brain in the honey bee Apis mellifera. J Comp Physiol A. 164:1989;483-494.
29. Fonta C., Sun X.J., Masson C. Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses. 18:1993;101-119.
30. Free JB. Pheromones of Social Insects. Ithaca (NY): Cornell University Press, 1987:218.
31. Gascuel J., Masson C. Influence of olfactory deprivation on synapse frequency in developing antennal lobe of the honeybee Apis mellifera. Neurosci Res Commun. 1:1987;173-180.
32. Gascuel J, Pham-Delegue M-H, Arnold G, Masson C. Evidence for a sensitive period during the development of the olfactory system in honey bees: anatomical, functional and behavioural data. In: Eder J, Rembold H, editors. Chemistry and Biology of Social Insects. Germany: J. Peperny Verlag, 1987:226-7.
33. Greenough WT, Black JE, Wallace CS. Morphological changes in the nervous system arising from behavioural experience: What is the evidence that they are involved in learning and memory? In: Squire LR, Lindenlaub E, editors. The Biology of Memory, Symposia Medica Hoechst 23. Stuttgart: F.K. Schattauder Verlag, 1990:159-83.
34. Greggers U., Menzel R. Memory dynamics and foraging strategies of honeybees. Behav Ecol Sociobiol. 32:1993;17-29.
35. Gundersen H.J.G., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., Møller A., Nielsen K., Nyengaard J.R., Pakkenberg B., Sorensen F.B., Vesterby A., West M.J. The new stereological tools: dissector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 96:1988;379-881.
36. Hammer M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature. 366:1993;59-63.
37. Hammer M., Menzel R. Learning and memory in the honeybee. J Neurosci. 15:1995;1617-1630.
38. Hammer M., Braun G., Mauelshagen J. Food-induced arousal and nonassociative learning in honeybees: dependence of sensitization on the application site and duration of food stimulation. Behav Neural Biol. 62:1994;210-223.
39. Hansson B.S., Christensen T.A., Hildebrand J.G. Functionally distinct subdivisions of the macroglomerular complex in the antennal lobes of the male sphinx moth Manduca sexta. J Comp Neurol. 312:1991;264-278.
40. Hansson B.S., Ljungberg H., Hallberg E., Löfstedt C. Functional specialization of olfactory glomeruli in a moth. Science. 256:1992;1313-1315.
41. Harraway J. Regression Methods Applied. Dunedin: Otago University Press, 1995.
42. Harris J.W., Woodring J. Elevated brain dopamine levels associated with ovary development in queenless worker honey bees (Apis mellifera L.). Comp Biochem Physiol C. 111:1995;271-279.
43. Heisenberg M., Heusipp M., Wanke C. Structural plasticity in the Drosophila brain. J Neurosci. 15:1995;1951-1960.
44. Homberg U. Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A. 154:1984;825-836.
45. Homberg U., Christensen T.A., Hildebrand J.G. Structure and function of the deutocerebrum in insects. Annu Rev Entomol. 34:1989;477-501.
46. Itoh T., Yokohari F., Tominaga Y. Response to humidity change of deutocerebral interneurons of the honeybee, Apis mellifera L. Naturwissenschaften. 78:1991;320-322.
47. Jenkins W.M., Merzenich M.M., Ochs M.T., Allard T., Guic-Robles E. Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviourally controlled tactile stimulation. J Neurophysiol. 63:1990;82-104.
48. Kandel E.R., Hawkins R.D. The biological basis of learning and individuality. Sci Am. 267:1992;76-86.
49. Kirchhof BS, Mercer AR. Antennal-lobe neurons of the honey bee, Apis mellifera, express a D2-like dopamine receptor in vitro. J Comp Neurol 1997:in press.
50. Kloppenburg P., Hildebrand J.G. Modulatory effects of 5-hydroxytryptamine on interneurons in the antennal lobe of the sphinx moth Manduca sexta. J Exp Biol. 198:1995;603-611.
51. Kokay I.C., Mercer A.R. Ontogeny of dopamine receptors in insect (Apis mellifera) brain. Soc Neurosci Abstr. 21:1995;632.
52. Kokay I.C., Mercer A.R. Characterisation of dopamine receptors in insect (Apis mellifera) brain. Brain Res. 706:1996;47-56.
53. Kral K., Meinertzhagen I.A. Anatomical plasticity of synapses in the lamina of the optic lobe of the fly. Philos Trans R Soc Lond [Biol]. 323:1989;155-183.
54. Kuwabara M. Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene (Apis mellifica). J Fac Sci Hokkaido Univ. 13:1957;458-467.
55. Lancet D. Vertebrate olfactory reception, A. Rev Neurosci. 9:1986;329-355.
56. Lopatina N.G., Chesnokova E.G., Dolotovskaya L.Z., Medvedeva A.V. Conditioning and ontogenesis of honey bee mutants defective in tryptophan metabolism via kynurenine pathway. Ontogenez. 16:1985;616-619.
57. Luna LG. Manual of Histological Staining Methods of the Armed Forces Institute of Pathology. New York: McGraw-Hill, 1968.
58. McEwen B.S., Coirini H., Westlin D., Danielson A., Frankfurt M., Gould E., Schumacher M., Woolley C. Steroid hormones as mediators of neural plasticity. Steroid Biochem Mol Biol. 39:1991;223-232.
59. Macmillan C.S., Mercer A.R. An investigation of the role of dopamine in the antennal lobes of the honeybee Apis mellifera. J Comp Physiol A. 160:1987;359-366.
60. Masson C., Arnold G. Ontogeny, maturation and plasticity of the olfactory system in the workerbee. J Insect Physiol. 30:1984;7-14.
61. Masson C, Arnold G. Organisation and plasticity of the olfactory system of the honeybee, Apis mellifera. In: Menzel R, Mercer A, editors. Neurobiology and Behaviour of Honeybees. Berlin: Springer-Verlag, 1987:280-95.
62. Masson C., Mustaparta H. Chemical information processing in the olfactory system of insects. Physiol Rev. 70:1990;199-245.
63. Masson C., Pham-Delègue M.H., Fonta C., Gascuel J., Arnold G., Nicolas G., Kerszberg M. Recent advances in the concept of adaptation to natural odour signals in the honeybee Apis mellifera L. Apidologie. 24:1993;169-194.
64. Mauelshagen J. Neural correlates of olfactory learning in an identified neuron in the honeybe brain. J Neurophysiol. 69:1992;609-625.
65. Mauelshagen J., Greggers U. Experimental access to associative learning in honeybees. Apidologie. 24:1993;249-266.
66. Menzel R. Associative learning in honey bees. Apidologie. 24:1993;157-168.
67. Menzel R., Erber J. Learning and memory in bees. Sci Am. 239:1978;80-87.
68. Menzel R., Müller U. Learning and memory in honeybees: from behaviour to neural substrates. Annu Rev Neurosci. 19:1996;379-404.
69. Menzel R, Erber J, Masuhr T. Learning and memory in the honeybee. In: Barton Brown L, editor. Experimental Analysis of Insect Behaviour. New York: Springer Verlag, 1974:195-217.
70. Menzel R, Michelsen B, Rüffer P, Sugawa M. Neuropharmacology of learning and memory in honey bees. In: Hertig G, Spatz HC, editors. Modulation of Synaptic Transmission and Plasticity in Nervous Systems. Berlin: Springer Verlag, 1988:333-50.
71. Mercer A.R., Menzel R. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol. 145:1982;363-368.
72. Mercer A.R., Hayashi J.H., Hildebrand J.G. Modulatory effects of 5-hydroxytryptamine on voltage-activated currents in cultured antennal-lobe neurons of the sphinx moth Manduca sexta. J Exp Biol. 198:1995;613-627.
73. Mercer A.R., Kloppenburg P., Hildebrand J.G. Serotonin-induced changes in the excitability of cultured antennal-lobe neurons of the sphinx moth Manduca sexta. J Comp Physiol A. 178:1996;21-31.
74. Mercer A.R., Kirchhof B.S., Hildebrand J.G. Enhancement by serotonin of the growth in vitro of antennal lobe neurons of the sphinx moth Manduca sexta. J Neurobiol. 29:1996;49-64.
75. Merzenich M.M., Kaas J.H., Wall J., Nelson R.J., Sur M., Felleman D. Topographic reoorganization of somatosensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience. 8:1983;33-55.
76. Merzenich M.M., Kaas J.H., Wall J., Sur M., Nelson R.J., Felleman D. Progression of change following median nerve section in the cortical represention of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience. 10:1983;639-665.
77. Mobbs P.G. The brain of the honeybee Apis mellifera. I. The connections and spatial organisation of the mushroom bodies. Phil Trans R Soc Lond B. 298:1982;309-354.
78. Nottebohm F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary bird. Science. 214:1981;1368-1370.
79. Pettis J.S., Winston M.L., Malyon M., Slessor K.N. The use of honeybee queen mandibular gland pheromone in mating nuclei management. Am Bee J. 133:1993;725-727.
80. Pham M.H., Roger B., Pain J. Variation en fonction de l'age des ouvrières d'abeilles (Apis mellifica ligustica S.) du pouvoir d'attraction d'un extrait de phéromones royales. Apidologie. 13:1982;143-155.
81. Pham-Delègue M.-H., Trouiller J., Bakchine E., Roger B., Masson C. Age dependency of worker bee response to queen pheronone in a four-armed olfactometer. Insectes Soc. 38:1991;283-292.
82. Pham-Delègue M.H., Trouiller J., Caillaud M., Roger B., Masson C. Effect of queen pheromone on worker bees of different ages: behavioural and electrophysiological responses. Apidologie. 24:1993;267-281.
83. Ressler K.J., Sullivan S.L., Buck L.B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell. 79:1994;1245-1255.
84. Robinson G.E. Alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally modulated response thresholds. J Comp Physiol A. 160:1987;613-619.
85. Schäfer S., Rehder V. Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol. 280:1989;43-58.
86. Schürmann F.W., Elekes K., Geffard M. Dopamine-like immunoreactivity in the bee brain. Cell Tissue Res. 256:1989;399-410.
87. Seeley T. Queen substance dispersal by messenger workers in honeybee colonies. Behav Ecol Sociobiol. 5:1979;391-415.
88. Seeley TD. Honeybee Ecology. Princeton: Princeton University Press, 1985.
89. Singer M.S., Shepherd G.M., Greer C.A. Olfactory receptors guide axons. Nature. 377:1995;19-20.
90. Smith B.H., The olfactory memory of the honeybee Apis mellifera I. Odorant modulation of short- and intermediate-term memory after single-trial conditioning. J Exp Biol. 161:1991;367-382.
91. Stocker R.F., Singh R.N., Schorderet M., Siddiqi O. Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res. 232:1983;237-248.
92. Stocker R.F., Lienhard M.C., Borst A., Fischbach K.-F. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res. 262:1990;9-34.
93. Sun X.-J., Fonta C., Masson C. Odour quality processing by bee antennal lobe interneurones. Chem Senses. 18:1993;355-377.
94. Taylor D.J., Robinson G.E., Logan B.J., Laverty R., Mercer A.R. Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee. J Comp Physiol A. 170:1992;715-721.
95. Technau G.M. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet. 1:1984;113-126.
96. Vassar R., Chao S.K., Sitcheran R., Nuñez J.M., Vosshall L.B. Topographic organization of sensory projections to the olfactory bulb. Cell. 79:1994;981-991.
97. Winnington A., Napper R.M., Mercer A.R. Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J Comp Neurol. 365:1996;479-490.
98. Winston ML. The Biology of the Honey Bee. Cambridge: Harvard University Press, 1987.
99. Withers G.S., Fahrbach S.E., Robinson G.E. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature. 364:1993;238-240.
100. 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. J Neurobiol. 26:1995;130-144.
101. Woolley C.S., McEwen B.S. Estradiol mediates fluctuation in hippocampal synaptic density during rhe estrous cycle of the adult rat. J Neurosci. 12:1992;2549-2554.
102. Woolley C.S., McEwen B.S. Roles of estradiol and progesterone in regulation of hipppocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol. 336:1993;293-306.