Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees

Journal of Neurobiology

Volumn 54, Issue 2, 2003, Pages 406-416

  Schulz, David J ^a   Elekonich, Michelle M ^a   Robinson, Gene E ^a  

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

Author keywords

Antennal lobes; Foraging behavior; Octopamine; Serotonin

Indexed keywords

BIOGENIC AMINE; DOPAMINE; OCTOPAMINE; SEROTONIN;

ANIMAL BEHAVIOR; ANTENNA; ARTICLE; CORRELATION ANALYSIS; FLIGHT; FORAGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HONEYBEE; NONHUMAN; PRIORITY JOURNAL;

5-HYDROXYTRYPTOPHAN; ANALYSIS OF VARIANCE; ANIMALS; BEES; BEHAVIOR, ANIMAL; BIOGENIC AMINES; BRAIN; BRAIN CHEMISTRY; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FLIGHT, ANIMAL; MOTOR ACTIVITY; OCTOPAMINE; ORIENTATION; SENSE ORGANS; SEROTONIN; SOCIAL BEHAVIOR;

EID: 0037413908     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10138     Document Type: Article

References (54)

1. Adamo SA, Linn CE, Hoy RR. 1995. The role of neurohormonal octopamine during 'fight or flight' behaviour in the field cricket Gryllus bimaculatus. J Exp Biol 198: 1691-1700.
2. Barron AB, Schulz DJ, Robinson GE. 2002. Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera). J Comp Physiol, to appear.
3. Ben-Shahar Y, Robichon A, Sokolowski MB, Robinson GE. 2002. Influence of Gene Action Across Different Time Scales on Behavior. Science 296:741-744.
4. Beshers SN, Robinson GE, Mittenthal JE. 1999. Response thresholds and division of labor in insect colonies. In: Detrain C, Denoubourg JL, Pasteels JM, editors. Information processing in social insects. Basel, Switzerland: Birkhäuser, pp 115-139.
5. Bloch G, Robinson GE. 2001. Reversal of honeybee behavioural rhythms. Nature 410:1048.
6. Brain PF, Haug M. 1992. Hormonal and neurochemical correlates of various forms of animal "aggression." Psychoneuroendocrinol 17:537-551.
7. Capaldi EA, Smith AO, Osborne JL, Fahrbach SE, Farris SM, Reynolds DR, Edwards AS, Martin A, Robinson GE, Poppy GM, Riley JR. 2000. Ontogeny of orientation flights in the honeybee revealed by harmonic radar. Nature 403:537-540.
8. Corbet SA. 1991. A fresh look at the arousal syndrome of insects. Adv Invert Physiol 23:81-116.
9. Crews D. 1987. Diversity and evolution of behavioral controlling mechanisms. In: Crews D, editor. Psychobiology of Reproductive Behavior: An Evolutionary Perspective. New Jersey: Prentice-Hall, p 88-118.
10. Durst C, Eichmüller S, Menzel R. 1994. Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav Neural Biol 62:259-263.
11. Elekonich MM, Schulz DJ, Bloch G, Robinson GE. 2001. Juvenile hormone levels in honey bee. Apis mellifera L., foragers: foraging experience and diurnal variation. J Insect Physiol 47:1119-1125.
12. Erber J, Kloppenburg P, Scheidler A. 1993. Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073-1083.
13. Feenstra MG, Vogel M, Botterblom MH, Joosten RN, de Bruin JP. 2001. Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue. Eur J Neurosci 13:1051-1054.
14. Fried I, Wilson CL, Morrow JW, Cameron KA, Behnke ED, Ackerson LC, Maidment NT. 2001. Increased dopamine release in the human amygdala during performance of cognitive tasks. Nat Neurosci 4:201-206.
15. Goosey MW, Candy DJ. 1980. The D-octopamine of the haemolymph of the locust Schistocerca gregaria and its elevation during flight. Insect Biochem 10:393-397.
16. Grünbaum L, Müller U. 1998. Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J Neurosci 18:4384-4392.
17. Hammer M, Menzel R. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honey bees. Learn Mem 5:146-156.
18. Harrison J. 1986. Caste specific changes in honey bee flight capacity. Physiol Zool 59:175-187.
19. Hasselmo ME. 1995. Neuromodulation of cortical function: modeling the physiological basis of behavior. Behav Brain Res 67:1-27.
20. Huang ZY, Robinson GE. 1992. Honeybee colony integration: worker-worker interactions mediate hormonally regulated plasticity in division of labor. Proc Nat Acad Sci USA 89:11726-11729.
21. Huang ZY, Robinson GE. 1996. Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol 39:147-158.
22. Huang ZY, Robinson GE, Borst DW. 1994. Physiological correlates of division of labor among similarly aged honey bees. J Comp Physiol 174:731-739.
23. Huang ZY, Robinson GE, Tobe SS, Yagi KJ, Strambi C, Strambi A, Stay B. 1991. Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis. J Insect Physiol 37:733-741.
24. Kravitz EA. 2000. Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J Comp Physiol A 186:221-238.
25. Kucharski R, Maleszka R, Hayward DC, Ball EE. 1998. A royal jelly protein is expressed in a subset of Kenyon cells in the mushroom bodies of the honey bee brain. Naturwissenschaften 85:343-346.
26. Leibowitz SF, Alexander JT. 1998. Hypothalamic serotonin in control of eating behavior, meal size, and body weight. Biol Psychiatry 44:851-864.
27. Lent CM. 1985. Serotonergic modulation of the feeding behavior of the medicinal leech. Brain Res Bull 14:643-655.
28. Lent CM, Dickinson MH. 1984. Serotonin integrates the feeding behavior of the medicinal leech. J Comp Physiol A 154:457-471.
29. Long TF, Murdock LL. 1983. Stimulation of blowfly feeding behavior by octopaminergic drugs. Proc Natl Acad Sci USA 80:4159-4163.
30. Mani SK, Allen JMC, Clark JH, Blaustein JD, O'Malley BW. 1994. Convergent pathways for steroid hormone-and neurotransmitter-induced rat sexual behavior. Science 265:1246-1248.
31. Menzel R, Müller U. 1996. Learning and memory in honeybees: from behavior to neural substrates. Ann Rev Neurosci 19:379-404.
32. Mesce K, Crisp KM, Gilchrist LS. 2001. Mixtures of octopamine and serotonin have nonadditive effects on the CNS of the medicinal leech. J Neurophysiol 85:2039-2046.
33. Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE. 1998. Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147-160.
34. Morse R. 1990. The ABC and XYZ of Bee Culture: An Encyclopedia of Beekeeping. Medina, OH: A I Root Co. 528 p.
35. Müller U. 2000. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27:159-168.
36. Oster GF, Wilson EO. 1978. Caste and Ecology in the Social Insects. Princeton, NJ: Princeton University Press. 352 p.
37. Robinson GE. 1987. Modulation of alarm pheromone perception in the honey bee: evidence for division of labor based on hormonally regulated response thresholds. J Comp Physiol 160:613-619.
38. Robinson GE, Heuser LM, LeConte Y, Lenquette F, Hollingworth RM. 1999. Neurochemicals aid bee nestmate recognition. Nature 399:534-535.
39. Robinson GE, Page RE, Strambi C, Strambi A. 1989. Hormonal and genetic control of behavioral integration in honey bee colonies. Science 246:109-112.
40. Schulz DJ, Robinson GE. 1999. Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in antennal lobes and age-related changes in mushroom bodies. J Comp Physiol A 184:481-488.
41. Schulz DJ, Robinson GE. 2001. Octopamine influences division of labor in honey bee colonies. J Comp Physiol A 187:53-61.
42. Schulz DJ, Sullivan JP, Robinson GE. 2002. Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies. Horm Behav, to appear.
43. Seeley TD. 1995. The wisdom of the hive: the social physiology of honey bee colonies. Cambridge, Massachusetts: Harvard University Press. 295 p.
44. Shapira M, Thompson CK, Soreq H, Robinson GE. 2001. Changes in neuronal acetylcholinesterase gene expression and division of labor in honey bee colonies. J Mol Neurosci 17:1-12.
45. Sigg D, Thompson CM, Mercer AR. 1997. Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera. J Neurosci 17:7148-7156.
46. Stevenson PA, Hofmann HA, Schoch K, Schildberger K. 2000. The fight and flight responses of crickets depleted of biogenic amines. J Neurobiol 43:107-120.
47. Taylor DJ, Robinson GE, Logan BJ, Laverty R, Mercer AR. 1992. Changes in brain amine levels associated with the morphological and behavioral development of the worker honeybee. J Comp Physiol A 170:715-721.
48. Toma DP, Bloch G, Moore D, Robinson GE. 2000. Changes in period mRNA levels in the brain and division of labor in honey bee colonies. Proc Nat Acad Sci USA 97:6914-6919.
49. Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE. 1999. Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471-479.
50. Wang Q, Buntin JD. 1999. The roles of stimuli from young, previous breeding experience, and prolactin in regulating parental behavior in ring doves Streptopelia risoria. Horm Behav 35:241-253.
51. Wang Z, Young LJ, De Vries GJ, Insel TR. 1998. Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 119:483-499.
52. Wingfield JC, Jacobs J, Hillgarth N. 1997. Ecological constraints and the evolution of hormone-behavior interrelationships. Ann NY Acad Sci 807:22-41. Winston ML. 1987. The biology of the honey bee. Cambridge, MA: Harvard University Press. 281 p.
53. Withers GS, Fahrach SE, Robinson GE. 1993. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238-240.
54. Withers GS, Fahrbach SE, Robinson GE. 1995. Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J Neurobiol 26: 130-144.