Honeybees consolidate navigation memory during Sleep

Journal of Experimental Biology

Volumn 215, Issue 22, 2012, Pages 3981-3988

  Beyaert, Lisa ^a   Greggers, Uwe ^a   Menzel, Randolf ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Honeybee; Memory consolidation; Navigation; Sleep; Sleep deprivation

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; DARKNESS; FEEDING BEHAVIOR; FLYING; MEMORY; PATHOPHYSIOLOGY; PHYSIOLOGY; RADIOFREQUENCY IDENTIFICATION; REST; SLEEP; SLEEP DEPRIVATION; TELECOMMUNICATION; TIME;

ANIMALS; BEES; DARKNESS; FEEDING BEHAVIOR; FLIGHT, ANIMAL; HOMING BEHAVIOR; MEMORY; RADAR; RADIO FREQUENCY IDENTIFICATION DEVICE; REST; SLEEP; SLEEP DEPRIVATION; TIME FACTORS;

ANIMALIA; APIS MELLIFERA; APOIDEA;

EID: 84868255264     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.075499     Document Type: Article

References (41)

1. Born, J. (2010). Slow-wave sleep and the consolidation of long-term memory. World J. Biol. Psychiatry 11 Suppl. 1, 16-21.
2. Born, J., Rasch, B. and Gais, S. (2006). Sleep to remember. Neuroscientist 12, 410-424. (Pubitemid 44316320)
3. Brawn, T. P., Fenn, K. M., Nusbaum, H. C. and Margoliash, D. (2008). Consolidation of sensorimotor learning during sleep. Learn. Mem. 15, 815-819.
4. Bushey, D., Tononi, G. and Cirelli, C. (2011). Sleep and synaptic homeostasis: structural evidence in Drosophila. Science 332, 1576-1581.
5. Capellini, I., McNamara, P., Preston, B. T., Nunn, C. L. and Barton, R. A. (2009). Does sleep play a role in memory consolidation? A comparative test. PLoS ONE 4, e4609.
6. Crocker, A., Shahidullah, M., Levitan, I. B. and Sehgal, A. (2010). Identification of a neural circuit that underlies the effects of octopamine on sleep: wake behavior. Neuron 65, 670-681.
7. Davis, R. L. (2011). Traces of Drosophila memory. Neuron 70, 8-19.
8. Diekelmann, S. and Born, J. (2010). The memory function of sleep. Nat. Rev. Neurosci. 11, 114-126.
9. Eban-Rothschild, A. D. and Bloch, G. (2008). Differences in the sleep architecture of forager and young honeybees (Apis mellifera). J. Exp. Biol. 211, 2408-2416.
10. Eisenhardt, D. and Menzel, R. (2007). Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiol. Learn. Mem. 87, 167-173. (Pubitemid 46038959)
11. Foltenyi, K., Greenspan, R. J. and Newport, J. W. (2007). Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 10, 1160-1167. (Pubitemid 47339955)
12. Greenspan, R. J., Tononi, G., Cirelli, C. and Shaw, P. J. (2001). Sleep and the fruit fly. Trends Neurosci. 24, 142-145. (Pubitemid 32166818)
13. Guo, F., Yi, W., Zhou, M. and Guo, A. (2011). Go signaling in mushroom bodies regulates sleep in Drosophila. Sleep 34, 273-281.
14. Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266-275. (Pubitemid 37271372)
15. 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 25, 129-138. (Pubitemid 30316516)
16. Hussaini, S. A., Bogusch, L., Landgraf, T. and Menzel, R. (2009). Sleep deprivation affects extinction but not acquisition memory in honeybees. Learn. Mem. 16, 698-705.
17. Jackson, C., McCabe, B. J., Nicol, A. U., Grout, A. S., Brown, M. W. and Horn, G. (2008). Dynamics of a memory trace: effects of sleep on consolidation. Curr. Biol. 18, 393-400.
18. Joiner, W. J., Crocker, A., White, B. H. and Sehgal, A. (2006). Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757-760. (Pubitemid 43865222)
19. Kaiser, W. (1988). Busy bees need rest, too - behavioural and electromyographical sleep signs in honeybees. J. Comp. Physiol. A 163, 565-584.
20. Kaiser, W. (2002). Honey bee sleep is different from chill coma - behavioural and electrophysiological recordings in forager honey bees. J. Sleep Res. 11, 115-117.
21. Kaiser, W. and Jander, J. P. (1988). Electromyographic indicators of sleep and wakefulness in honey bees. Sleep 8, 249-251.
22. Kaiser, W. and Steiner-Kaiser, J. (1988). Behavioral and physiological changes occurring during sleep in the honey bee. Sleep 8, 157-159.
23. Klein, B. A. and Seeley, T. D. (2011). Work or sleep? Honeybee foragers opportunistically nap during the day when forage is not available. Anim. Behav. 82, 77-83.
24. Klein, B. A., Klein, A., Wray, M. K., Mueller, U. G. and Seeley, T. D. (2010). Sleep deprivation impairs precision of waggle dance signaling in honey bees. Proc. Natl. Acad. Sci. USA 107, 22705-22709.
25. Marshall, L. and Born, J. (2007). The contribution of sleep to hippocampusdependent memory consolidation. Trends Cogn. Sci. 11, 442-450. (Pubitemid 47588990)
26. Mednick, S., Nakayama, K. and Stickgold, R. (2003). Sleep-dependent learning: a nap is as good as a night. Nat. Neurosci. 6, 697-698. (Pubitemid 36792882)
27. Menzel, R. and Müller, U. (1996). Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19, 379-404. (Pubitemid 26080833)
28. Menzel, R., Brandt, R., Gumbert, A., Komischke, B. and Kunze, J. (2000). Two spatial memories for honeybee navigation. Proc. Biol. Sci. 267, 961-968. (Pubitemid 30326393)
29. Menzel, R., Greggers, U., Smith, A., Berger, S., Brandt, R., Brunke, S., Bundrock, G., Hülse, S., Plümpe, T., Schaupp, F. et al. (2005). Honey bees navigate according to a map-like spatial memory. Proc. Natl. Acad. Sci. USA 102, 3040-3045. (Pubitemid 40299912)
30. Menzel, R., Kirbach, A., Haass, W.-D., Fischer, B., Fuchs, J., Koblofsky, M., Lehmann, K., Reiter, L., Meyer, H., Nguyen, H. et al. (2011). A common frame of reference for learned and communicated vectors in honeybee navigation. Curr. Biol. 21, 645-650.
31. Riley, J. R., Greggers, U., Smith, A. D., Reynolds, D. R. and Menzel, R. (2005). The flight paths of honeybees recruited by the waggle dance. Nature 435, 205-207. (Pubitemid 40685945)
32. Sauer, S., Kinkelin, M., Herrmann, E. and Kaiser, W. (2003). The dynamics of sleeplike behaviour in honey bees. J. Comp. Physiol. A 189, 599-607. (Pubitemid 37105901)
33. Sehgal, A. and Mignot, E. (2011). Genetics of sleep and sleep disorders. Cell 146, 194-207.
34. Seugnet, L., Suzuki, Y., Merlin, G., Gottschalk, L., Duntley, S. P. and Shaw, P. J. (2011). Notch signaling modulates sleep homeostasis and learning after sleep deprivation in Drosophila. Curr. Biol. 21, 835-840.
35. 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)
36. Siegel, J. M. (2005). Clues to the functions of mammalian sleep. Nature 437, 1264-1271. (Pubitemid 41568666)
37. Stephenson, R. and Lewis, V. (2011). Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus). J. Exp. Biol. 214, 747-756.
38. Stollhoff, N., Menzel, R. and Eisenhardt, D. (2005). Spontaneous recovery from extinction depends on the reconsolidation of the acquisition memory in an appetitive learning paradigm in the honeybee (Apis mellifera). J. Neurosci. 25, 4485-4492. (Pubitemid 40629138)
39. von Frisch, K. (1967). The Dance Language and Orientation of Bees. Cambridge, MA: Harvard University Press.
40. Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A. and Stickgold, R. (2002). Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205-211. (Pubitemid 34804334)
41. Wu, M. N. and Raizen, D. M. (2011). Notch signaling: a role in sleep and stress. Curr. Biol. 21, R397-R398.