Neurogenomic signatures of spatiotemporal memories in time-trained forager honey bees

Journal of Experimental Biology

Volumn 214, Issue 6, 2011, Pages 979-987

  Naeger, Nicholas L ^a   Van Nest, Byron N ^b   Johnson, Jennifer N ^b   Boyd, Sam D ^b   Southey, Bruce R ^a   Rodriguez Zas, Sandra L ^a   Moore, Darrell ^b   Robinson, Gene E ^a  

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

^b EAST TENNESSEE STATE UNIVERSITY   (United States)

Author keywords

Appetitive behavior; Circadian; Honey bee; Memory; Microarray

Indexed keywords

TRANSCRIPTION FACTOR CLOCK;

ANIMAL; ANTICIPATION; ARTICLE; BEE; BRAIN; DISCRIMINANT ANALYSIS; DNA MICROARRAY; FEEDING BEHAVIOR; GENE EXPRESSION PROFILING; GENETICS; GENOME; HONEY; MEMORY; METABOLISM; NERVOUS SYSTEM; PHYSIOLOGY; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REWARD; TIME;

ANIMALS; ANTICIPATION, PSYCHOLOGICAL; BEES; BRAIN; CLOCK PROTEINS; DISCRIMINANT ANALYSIS; FEEDING BEHAVIOR; GENE EXPRESSION PROFILING; GENOME; HONEY; MEMORY; NERVOUS SYSTEM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; REWARD; TIME FACTORS;

APIS MELLIFERA; APOIDEA;

EID: 79951961091     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.053421     Document Type: Article

References (62)

1. Alaux, C., Sinha, S., Hasadsri, L., Hunt, G. J., Guzman-Novoa, E., DeGrandi- Hoffman, G., Uribe-Rubio, J. L., Southey, B. R., Rodriguez-Zas, S. and Robinson, G. E. (2009a). Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc. Natl. Acad. Sci. USA 106, 15400-15405.
2. Alaux, C., Le Conte, Y., Adams, H. A., Rodriguez-Zas, S., Grozinger, C. M., Sinha, S. and Robinson, G. E. (2009b). Regulation of brain gene expression in honey bees by brood pheromone. Genes Brain Behav. 8, 309-319.
3. Allada, R. and Chung, B. Y. (2010). Circadian organization of behavior and physiology in Drosophila. Annu. Rev. Physiol. 72, 605-624.
4. Ament, S. A., Corona, M., Pollock, H. S. and Robinson, G. E. (2008). Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. USA 105, 4226-4231. (Pubitemid 351754362)
5. Angeles-Castellanos, M., Mendoza, J. and Escobar, C. (2007). Restricted feeding schedules phase shift daily rhythms of c-Fos and protein Per1 immunoreactivity in corticolimbic regions in rats. Neuroscience 144, 344-355. (Pubitemid 44848385)
6. Barrett, R. M. and Wood, M. A. (2008). Beyond transcription factors: the role of chromatin modifying enzymes in regulating transcription required for memory. Learn. Mem. 15, 460-467. (Pubitemid 352008668)
7. Beling, I. (1929). Uber das Zeitgedachtnis der Bienen. Z. Vgl. Physiol. 9, 259-338.
8. Ben-Shahar, Y., Leung, H. T., Pak, W. L., Sokolowski, M. B. and Robinson, G. E. (2003). cGMP-dependent changes in phototaxis: a possible role for the foraging gene in honey bee division of labor. J. Exp. Biol. 206, 2507-2515.
9. Cash, A. C., Whitfield, C. W., Ismail, N. and Robinson, G. E. (2005). Behavior and the limits of genomic plasticity: power and replicability in microarray analysis of honey bee brains. Genes Brain Behav. 4, 267-271. (Pubitemid 40799774)
10. Doorn, W. G. v. and Meeteren, U. v. (2003). Flower opening and closure: a review. J. Exp. Bot. 54, 1801-1812.
11. Eban-Rothschild, A. D. and Bloch, G. (2008). Differences in the sleep architecture of forager and young honey bees (Apis mellifera). J. Exp. Biol. 211, 2408-2416.
12. Eckel-Mahan, K. and Sassone-Corsi, P. (2009). Metabolism control by the circadian clock and vice versa. Nat. Struct. Mol. Biol. 16, 462-467.
13. Escobar, C., Cailotto, C., Angeles-Castellanos, M., Delgado, R. S. and Bujis, R. M. (2009). Peripheral oscillators: the driving force for food-anticipatory activity. Eur. J. Neurosci. 30, 1665-1675.
14. Gimenes, M., Benedito-Silva, A. A. and Marques, M. D. (1993). Chronobiologic aspects of a coadaptive prodess: the interaction of Ludwigia elegans flowers and their more frequent bee visitors. Chronobiol. Int. 10, 20-30.
15. Green, D. J. and Gillette, R. (1982). Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res. 245, 198-200. (Pubitemid 12099332)
16. Harbison, S. T., Mackay, T. F. and Anholt, R. R. (2009). Understanding the neurogenetics of sleep: progress from Drosophila. Trends Genet. 25, 262-269.
17. Hendricks, J. C., Finn, S. M., Panckeri, K. A., Chavkin, J., Williams, J. A., Sehgal, A. and Pack, A. I. (2000). Rest in Drosophila is a sleep-like state. Neuron 26, 295-298.
18. Honeybee Genome Sequencing Consortium (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949.
19. Huang, D. W., Sherman, B. T. and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57.
20. Hung, H. C., Kay, S. A. and Weber, F. (2009). HSP90, a capacitor of behavioral variation. J. Biol. Rhythms 24, 183-192.
21. Kaiser, W. (1988). Busy bees need rest, too: behavioural and electromyographical sleep signs in honeybees. J. Comp. Physiol. A. 163, 565-584.
22. Kaiser, W. and Steiner-Kaiser, J. (1983). Neuronal correlates of sleep, wakefulness, and arousal in a diurnal insect. Nature 301, 707-709. (Pubitemid 13164064)
23. Katzenberg, D., Young, T., Finn, L., Lin, L., King, D. P., Takahashi, J. S. and Mignot, E. (1998). A CLOCK polymorphism associated with human diurnal preference. Sleep 21, 569-576. (Pubitemid 28440699)
24. Kleber, E. (1935). Hat das zeitgedachtnis der bienen biologische bedeutung? Z. Vgl. Physiol 22, 221-262.
25. Klein, B. A., Olzsowy, K. M., Klein, A., Saunders, K. M. and Seeley, T. D. (2008). Caste-dependent sleep of worker honey bees. J. Exp. Biol. 211, 3028-3040.
26. Kononenko, N. I. and Berezetskaya, N. M. (2010). Modeling the spontaneous activity in suprachiasmatic nucleus neurons: role of cation single channels. J. Theor. Biol. 265, 115-125.
27. Körner, I. (1939). Zeitgedächtnis und alarmierung bei den Bienen. Z. Vgl. Physiol. 27, 445-459.
28. Kraus, F. B., Gerecke, E. and Moritz, R. F. A. (in press). Shift work has a genetic basis in honeybee pollen foragers. Behav. Genet. (DOI: 10.1007/s10519-010-9382- 9).
29. Linnaeus, C. (1751). Philosophia Botanica. New York, NY: Oxford University Press.
30. Mackiewicz, M., Naidoo, N., Zimmerman, J. E. and Pack, A. I. (2008). Molecular mechanisms of sleep and wakefullness. Ann. N. Y. Acad. Sci. 1129, 335-349.
31. Matile, P. (2006). Circadian rhythmicity of nectar secretion in Hoya carnosa. Bot. Helv. 116, 1-7. (Pubitemid 44431191)
32. Meredith, A. L., Wiler, S. W., Miller, B. H., Takahashi, J. S., Fodor, A. A., Ruby, N. F. and Aldrich, R. W. (2006). BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat. Neurosci. 9, 1041-1049. (Pubitemid 44264917)
33. Miche, S. and Colwell, C. S. (2001). Cellular communication and coupling within the suprachiasmatic nucleus. Chronobiol. Int. 18, 579-600. (Pubitemid 32929206)
34. Mistlberger, R. E. (2009). Food-anticipatory circadian rhythms: concepts and methods. Eur. J. Neurosci. 30, 1718-1729.
35. Moore, D. and Doherty, P. (2009). Acquisition of a time-memory in forager honey bees. J. Comp. Physiol. A 195, 741-751.
36. Moore, D. and Rankin, M. A. (1983). Diurnal changes in the accuracy of the honeybee foraging rhythm. Biol. Bull. 164, 471-482.
37. Moore, D., Siegfried, D., Wilson, R. and Rankin, M. A. (1989). The influence of time of day on the foraging behavior of the honeybee, Apis mellifera. J. Biol. Rhythms 4, 305-325.
38. Oishi, K., Shiota, M., Sakamoto, K., Kasamatsu, M. and Ishida, N. (2004). Feeding is not a more potent Zeitgeber than the light-dark cycle in Drosophila. NeuroReport 15, 739-743. (Pubitemid 38457173)
39. R Development Core Team (2006). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
40. Ramsey, K. M., Yoshino, J., Brace, C. S., Abrassart, D., Kobayashi, Y., Marcheva, B., Hong, H. K., Chong, J. L., Buhr, E. D., Lee, C. et al. (2009). Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324, 651-654.
41. Renner, M. (1957). Neue versuche uber den zeitsinn der honigbiene. Z. Vgl. Physiol. 40, 85-118.
42. Robinson, G. E., Grozinger, C. M. and Whitfield, C. W. (2005). Sociogenomics: social life in molecular terms. Nat. Rev. Genet. 6, 257-270. (Pubitemid 40469046)
43. Robinson, G. E., Fernald, R. D. and Clayton, D. F. (2008). Genes and social behavior. Science 322, 896-900.
44. Ruben, E. B., Shemesh, Y., Cohen, M., Elgavish, S., Robertson, H. M. and Bloch, G. (2006). Molecular and phylogenetic analyses reveal mammalian-like clockwork in the honey bee (Apis mellifera) and shed new light on the molecular evolution of the circadian clock. Genome Res. 16, 1352-1365. (Pubitemid 44664678)
45. Schulz, D. J. and Robinson, G. E. (1999). Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and agerelated changes in the mushroom bodies. J. Comp. Physiol. A 185, 481-488. (Pubitemid 29298275)
46. Sen Sarma, M., Rodriguez-Zas, S. L., Gernat, T., Nguyen, T., Newman, T. and Robinson, G. E. (2010). Distance-responsive genes found in dancing honey bees. Genes Brain Behav. 9, 825-830.
47. Shaw, P. J., Cirelli, C., Greenspan, R. J. and Tononi, G. (2000). Correlates of sleep and waking in Drosophila melanogaster. Science 287, 1834-1837. (Pubitemid 30143970)
48. Shen, H., Watanabe, M., Tomasiewicz, H., Rutishauser, U., Magnuson, T. and Glass, J. D. (1997). Role of neural cell adhesion molecule and polysialic acid in mouse circadian clock function. J. Neurosci. 17, 5221-5229. (Pubitemid 27263835)
49. Ueda, H. R., Matsumoto, A., Kawamura, M., Iino, M., Tanimura, T. and Hashimoto, S. (2002). Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J. Biol. Chem. 277, 14048-14052. (Pubitemid 34968014)
50. Venables, W. N. and Ripley, B. D. (2002). Modern Applied Statistics Using S, 4th edition. New York, NY: Springer.
51. Vollmers, C., Gill, S., DiTacchio, L., Pulivarthy, S. R., Le, H. D. and Panda, S. (2009). Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression. Proc. Natl. Acad. Sci. USA 106, 21453-21458.
52. von Frisch, K. (1967). The Dance Language and Orientation of Bees. Cambridge, MA: Harvard University Press.
53. Wahl, O. (1932). Neue untersuchungen uber das zeitgedachtnis der bienen. Z. Vgl Physiol. 16, 529-589.
54. Wang, Y., Mutti, N. S., Ihle, K. E., Siegel, A., Dolezal, A. G., Kaftanoglu, O. and Amdam, G. V. (2010). Down-regulation of honey bee IRS gene biases behavior towards food rich in protein. PLoS Genet. 6, e1000896.
55. Wang, Y. C. and Huang, R. C. (2006). Effects of sodium pump activity on spontaneous firing in neurons of the rat suprachiasmatic nucleus. J. Neurophysiol. 96, 109-118.
56. Williams, J. B., Roberts, S. P. and Elekonich, M. M. (2008). Age and natural metabolically intensive behavior affect oxidative stress and antioxidant mechanisms. Exp. Gerentol. 43, 538-549.
57. Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge, MA: Harvard University Press.
58. Webb, I. C., Baltazar, R. M., Lehman, M. N. and Coolen, L. M. (2009). Bidirectional interactions between the circadian and reward systems: is restricted food access a unique zeitgeber? Eur. J. Neurosci. 30, 1739-1748.
59. Welzl, H. and Stork, O. (2003). Cell adhesion molecules: key players in memory consolidation? News Physiol. Sci. 18, 147-150. (Pubitemid 37026103)
60. Whitfield, C. W., Cziko, A. M. and Robinson, G. E. (2003). Gene expression profiles in the brain predict behavior in individual honey bees. Science 302, 296-299. (Pubitemid 37248762)
61. Xu, K., Zheng, X. and Seghal, A. (2008). Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell Metab. 8, 289-300.
62. Zheng, X. and Sehgal, A. (2010). AKT and TOR signaling set the pace of the circadian pacemaker. Curr. Biol. 20, 1203-1208.