Way-finding in displaced clock-shifted bees proves bees use a cognitive map

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 24, 2014, Pages 8949-8954

  Cheeseman, James F ^a,b   Millar, Craig D ^b,c   Greggers, Uwe ^d   Lehmann, Konstantin ^d   Pawley, Matthew D M ^a,e   Gallistel, Charles R ^f   Warman, Guy R ^a,b   Menzel, Randolf ^d  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c Allan Wilson Centre for Molecular Ecology & Evolution   (New Zealand)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e MASSEY UNIVERSITY   (New Zealand)

^f RUTGERS UNIVERSITY   (United States)

Author keywords

Circadian; Course setting; Navigation; Shortcuts; Terrain map

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEE; CIRCADIAN RHYTHM; COGNITION; CONTROLLED STUDY; FEEDING BEHAVIOR; FLIGHT; GENERAL ANESTHESIA; HIPPOCAMPUS; MEMORY; NONHUMAN; PRIORITY JOURNAL;

CIRCADIAN; COURSE-SETTING; NAVIGATION; SHORTCUTS; TERRAIN MAP;

ANESTHETICS; ANIMALS; BAYES THEOREM; BEES; BRAIN; CIRCADIAN RHYTHM; COGNITION; CUES; FLIGHT, ANIMAL; HOMING BEHAVIOR; ISOFLURANE; MEMORY; ODDS RATIO; ORIENTATION; SPATIAL BEHAVIOR; SUNLIGHT;

EID: 84902590161     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408039111     Document Type: Article

References (39)

1. Cheng K (1986) A purely geometric module in the rat's spatial representation. Cognition 23(2):149-178.
2. Derdikman D, Moser EI (2010) A manifold of spatial maps in the brain. Trends Cogn Sci 14(12):561-569.
3. Jacobs LF (2003) The evolution of the cognitive map. Brain Behav Evol 62(2):128-139.
4. O'Keefe J (1990) A computational theory of the hippocampal cognitive map. Prog Brain Res 83:301-312.
5. O'Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381(6581):425-428. (Pubitemid 26162732)
6. O'Keefe J, Nadel L (1978) The Hippocampus as a Cognitive Map (Oxford Univ Press, Oxford, England).
7. Wills TJ, Cacucci F, Burgess N, O'Keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328(5985):1573-1576.
8. Gallistel CR (1998) Symbolic Processes in the brain: The case of insect navigation. Conceptual and Methodological Foundations. An Invitation to Cognitive Science, eds Scarborough D, Sternberg S, Osherson D (MIT Press, Cambridge, MA), 2nd Ed, Vol 4, pp 1-51.
9. Wolf H (2011) Odometry and insect navigation. J Exp Biol 214(Pt 10):1629-1641.
10. Menzel R, Brembs B, Giurfa M (2007) Cognition in invertebrates. Evolution of Nervous Systems. Evolution of Nervous Systems in Invertebrates, ed Kaas JH (Academic, New York), Vol 2, pp 403-422.
11. Collett M (2012) How navigational guidance systems are combined in a desert ant. Curr Biol 22(10):927-932.
12. Collett M, Collett TS, Bisch S, Wehner R (1998) Local and global vectors in desert ant navigation. Nature 394(July):269-272. (Pubitemid 28335036)
13. Cruse H, Wehner R (2011) No need for a cognitive map: Decentralized memory for insect navigation. PLOS Comput Biol 7(3):e1002009.
14. Collett TS, Graham P (2004) Animal navigation: Path integration, visual landmarks and cognitive maps. Curr Biol 14(12):R475-R477. (Pubitemid 38791581)
15. Wehner R (1997) From Living Eyes to Seeing Machines, eds Srinivasan MV, Venkatesh S (Oxford Univ Press, Oxford, England), pp 158-173.
16. Wehner R, Wehner S (1990) Insect navigation: Use of maps or Ariadne's thread? Ethol Ecol Evol 2(1):27-48.
17. Wehner R, Menzel R (1990) Do insects have cognitive maps? Annu Rev Neurosci 13:403-414. (Pubitemid 20100658)
18. Menzel R, et al. (2011) A common frame of reference for learned and communicated vectors in honeybee navigation. Curr Biol 21(8):645-650.
19. Dyer FC (1991) Bees acquire route-based memories but not cognitive maps in a familiar landscape. Anim Behav 41(2):239-246.
20. Menzel R, et al. (2005) Honey bees navigate according to a map-like spatial memory. Proc Natl Acad Sci USA 102(8):3040-3045. (Pubitemid 40299912)
21. Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R (2005) The flight paths of honeybees recruited by the waggle dance. Nature 435(7039):205-207. (Pubitemid 40685945)
22. Wystrach A, Mangan M, Philippides A, Graham P (2013) Snapshots in ants? New interpretations of paradigmatic experiments. J Exp Biol 216(Pt 10):1766-1770.
23. Frisch KV, Lindauer M (1954) Himmel und Erde in Konkurrenz bei der Orientierung der Bienen. Naturwissenschaften 41(June):245-253. German.
24. Cheeseman JF, et al. (2012) General anesthesia alters time perception by phase shifting the circadian clock. Proc Natl Acad Sci USA 109(18):7061-7066.
25. Laughlin SB, Horridge GA (1971) Angular sensitivity of the retinula cells of dark-adapted worker bee. Z Vgl Physiol 74:329-335.
26. Srinivasan MV, Zhang S (2004) Visual motor computations in insects. Annu Rev Neurosci 27:679-696. (Pubitemid 39050417)
27. Dyer FC (1998) Cognitive Ecology the Evolutionary Ecology of Information Processing and Decision Making, ed Dukas R (Univ of Chicago, Chicago), pp 201-260.
28. Elsner N, Singer W (1989) Dynamics and Plasticity in Neuronal Systems: Proceedings of the 17th Gottingen Neurobiology Conference, eds Elsner N, Singer W (Thieme, Stuttgart).
29. Lindauer M (1963) Kompaßorientierung. Orientierung der Tiere / Animal Orientation Advances in Biology 26:158-181.
30. Menzel R, Fuchs J, Kirbach A, Lehmann K, Greggers U (2011) Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel, eds Galizia G, Eisenhardt D, Giurfa M (Springer Netherlands, Dordrecht), pp 103-116.
31. Menzel R, et al. (2012) Vector integration and novel shortcutting in honeybee navigation. Apidologie 43(5):229-243.
32. Filannino C, Armstrong C, Guilford T, Gagliardo A (2014) Individual strategies and release site features determine the extent of deviation in clock-shifted pigeons at familiar sites. Anim Cogn 17(1):33-43.
33. Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16(2):130-138.
34. Gallistel CR, Matzel LD (2013) The neuroscience of learning: Beyond the Hebbian synapse. Annu Rev Psychol 64:169-200.
35. Taube JS (2007) The head direction signal: Origins and sensory-motor integration. Annu Rev Neurosci 30:181-207.
36. Riley JR, et al. (1996) Tracking bees with harmonic radar. Nature 379:29-30.
37. Duong T (2012) ks: Kernel smoothing. R package version 1.8.8. Available at: http://CRAN.R-project.org/package=ks. Accessed May 15, 2014.
38. R Development Core Team (2012) R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, Vienna, Austria). www.R-project.org. Accessed May 15, 2014.
39. Duong T, Hazelton ML (2003) Plug-in bandwidth matrices for bivariate kernel density estimation. J Nonparametr Stat 15(1):17-30. (Pubitemid 36294449)