Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The concepts of ‘sameness’ and ‘difference’ in an insect

Nature volume 410, pages 930–933 (2001)Cite this article

Abstract

Insects process and learn information flexibly to adapt to their environment. The honeybee Apis mellifera constitutes a traditional model for studying learning and memory at behavioural, cellular and molecular levels1. Earlier studies focused on elementary associative and non-associative forms of learning determined by either olfactory conditioning of the proboscis extension reflex1 or the learning of visual stimuli2 in an operant context. However, research has indicated that bees are capable of cognitive performances that were thought to occur only in some vertebrate species. For example, honeybees can interpolate visual information3, exhibit associative recall4,5, categorize visual information6,7,8 and learn contextual information9. Here we show that honeybees can form ‘sameness’ and ‘difference’ concepts. They learn to solve ‘delayed matching-to-sample’ tasks, in which they are required to respond to a matching stimulus, and ‘delayed non-matching-to-sample’ tasks, in which they are required to respond to a different stimulus; they can also transfer the learned rules to new stimuli of the same or a different sensory modality. Thus, not only can bees learn specific objects and their physical parameters, but they can also master abstract inter-relationships, such as sameness and difference.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

Buy

All prices are NET prices.

Figure 1: Experiments 1 and 2.
Figure 2: Experiment 4.
Figure 3: Experiments 5 and 6, investigating non-matching performance.

References

  1. Menzel, R. & Müller, U. Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19, 379–404 (1996).

    Article  CAS  Google Scholar 

  2. Menzel, R. in Experimental Behavioral Ecology (eds Hölldobler, B. & Lindauer, M.) 55–74 (Gustav Fischer, Stuttgart, 1985).

    Google Scholar 

  3. Collett, T. S. & Baron, J. Learnt sensori-motor mappings in honeybees: interpolation and its possible relevance to navigation. J. Comp. Physiol. A 177, 287–298 (1995).

    Google Scholar 

  4. Srinivasan, M. V., Zhang, S. W. & Zhu, H. Honeybees links sights to smells. Nature 396, 637–638 (1998).

    Article  ADS  CAS  Google Scholar 

  5. Zhang, S. W., Lehrer, M. & Srinivasan, M. V. Honeybee memory: navigation by associative grouping and recall of visual stimuli. Neurobiol. Learn. Mem. 72, 180–201 (1999).

    Article  CAS  Google Scholar 

  6. Hateren, J. H., Srinivasan, M. V. & Wait, P. B. Pattern recognition in bees: orientation discrimination. J. Comp. Physiol. A 167, 649–654 (1990).

    Article  Google Scholar 

  7. Giurfa, M., Eichmann, B. & Menzel, R. Symmetry perception in an insect. Nature 382, 458–461 (1996).

    Article  ADS  CAS  Google Scholar 

  8. Horridge, G. A. & Zhang, S. W. Pattern vision in honeybees (Apis mellifera): flower-like patterns with no predominant orientation. J. Insect Physiol. 41, 681–688 (1994).

    Article  Google Scholar 

  9. Collett, T. S., Fauria, K., Dale, K. & Baron, J. Places and patterns—a study of context learning in honeybees. J. Comp. Physiol. A 181, 343–353 (1997).

    Article  Google Scholar 

  10. Moon, L. E. & Harlow, H. F. Analysis of oddity learning by rhesus monkeys. J. Comp. Physiol. Psychol. 48, 188–194 (1955).

    Article  CAS  Google Scholar 

  11. Strong, P. N. & Hedges, M. Comparative studies in simple oddity learning. 1. Cats, racoons, monkeys and chimpanzees. Psychonom. Sci. 5, 13–14 (1966).

    Article  Google Scholar 

  12. Thomas, R. K. & Boyd, M. G. A comparison of Cebus albifrons and Samiri sciureus on oddity performance. Anim. Learn. Behav. 1, 151–153 (1973).

    Article  Google Scholar 

  13. Herman, L. M. & Gordon, J. A. Auditory delayed matching in the bottlenose dolphin. J. Exp. Anal. Behav. 21, 19–26 (1974).

    Article  CAS  Google Scholar 

  14. Zentall, T. R. & Hogan, D. E. Same/different concept learning in the pigeon: the effect of negative instances and prior adaptation to transfer stimuli. J. Exp. Anal. Behav. 30, 177–186 (1978).

    Article  CAS  Google Scholar 

  15. Holmes, P. W. Transfer of matching performance in pigeons. J. Exp. Anal. Behav. 31, 103–114 (1979).

    Article  CAS  Google Scholar 

  16. Lombardi, C. M., Fachinelli, C. G. & Delius, J. D. Oddity of visual patterns conceptualized by pigeons. Anim. Learn. Behav. 12, 2–6 (1984).

  17. D'Amato, M. R., Salmon, D. P. & Colombo, M. Extent and limits of the matching concept in monkeys (Cebus apella). J. Exp. Psychol. Anim. Behav. Proc. 11, 35–51 (1985).

    Article  CAS  Google Scholar 

  18. Wilson, B., Mackintosh, N. J. & Boakes, R. A. Transfer of relational rules in matching and oddity learning by pigeons and corvids. Quart. J. Exp. Psychol. 37B, 313–332 (1985).

    Article  Google Scholar 

  19. Oden, D. L., Premack, D. & Thompson, R. K. R. Spontaneous transfer of matching by infant chimpanzees. J. Exp. Psychol. Anim. Behav. Proc. 14, 140–145 (1988).

    Article  CAS  Google Scholar 

  20. Wright, A. A., Santiago, H. C., Urcuioli, P. J. & Sands, S. F. in Quantitative Analyses Of Behavior: Discrimination Processes Vol. IV (eds Commons, M. L., Herrnstein, R. J. & Wagner, A. R.) 295–317 (Ballinger, Cambridge MA, 1984).

    Google Scholar 

  21. Davey, G. Ecological Learning Theory (Routledge, London, 1989).

    Google Scholar 

  22. Menzel, R. & Giurfa, M. Cognitive architecture of a mini-brain: the honeybee. Trends Cognit. Sci. 5, 62–71 (2001).

    Article  CAS  Google Scholar 

  23. Hammer, M. The neural basis of associative reward learning in honeybees. Trends Neurosci. 20, 245–252 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Bönisch and C. Wiley for help with experiments 5 and 6. M.G., A.J. and R.M. were supported by the Special Programme SFB 515 of the Deutsche Forschungsgemeinschaft. M.G. was also supported by a grant from the Deutsche Forschungsgemeinschaft. S.W.Z. and M.S. were supported partly by a grant from the Human Frontiers in Science Program and from the US Defence Advanced Research Projects Agency and the Office of Naval Research. The two laboratories contributed equally to the work.

Author information

Authors and Affiliations

  1. Neurobiologie, Institut für Biologie, Freie Universität Berlin, Königin-Luise-Strasse 28/30, Berlin, 14195, Germany

    Martin Giurfa, Arnim Jenett & Randolf Menzel

  2. Ethologie et Cognition Animale, Universite Paul Sabatier, 118 Route de Narbonne, Toulouse, 30162 Cedex 4, France

    Martin Giurfa

  3. Centre for Visual Science, Research School of Biological Sciences, Australian National University, PO Box 475, Canberra, ACT 2601, Australia

    Shaowu Zhang & Mandyam V. Srinivasan

Authors
  1. Martin Giurfa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaowu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arnim Jenett
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Randolf Menzel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mandyam V. Srinivasan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Giurfa.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Giurfa, M., Zhang, S., Jenett, A. et al. The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410, 930–933 (2001). https://doi.org/10.1038/35073582

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35073582

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing