Local-feature assembling in visual pattern recognition and generalization in honeybees

Abstract

Generalization is a cognitive ability that allows similar stimuli along a given dimension to be treated as equivalents1,2,3. Insects exhibit high levels of visual generalization4,5,6. Honeybees trained to recognize complex visual stimuli on the basis of a single feature generalize their choice to novel stimuli sharing that common feature with the trained stimuli7. The demonstration of this kind of performance has been limited to the use of a single visual feature, and the possibility that bees link different features in learning a visual pattern has been denied8,9. Here we show that honeybees trained with a series of complex patterns sharing a common layout comprising four edge orientations remember these orientations simultaneously in their appropriate positions, and generalize their response to novel stimuli that preserve the trained layout. Honeybees also generalize their response to patterns with fewer correct orientations, depending on their match with the trained layout. Stimulation of the achromatic L-photoreceptor input is necessary for this task. The mini-brain of the honeybee can thus extract regularities in its environment and establish correspondences among correlated features. It can thus generate a large set of object descriptions from a finite set of elements.

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Figure 1: Training and test stimuli.
Figure 2: First (a, b), second (c, d) and third (e, f) experiments. S + and S - indicate layouts of the training patterns previously rewarded and non-rewarded, respectively.
Figure 3: Fourth experiment.

References

  1. 1

    Spence, K. The differential response in animals to stimuli varying within a single dimension. Psychol. Rev. 44, 430–444 (1937)

    Article  Google Scholar 

  2. 2

    Shepard, R. N. Toward a universal law of generalization for psychological science. Science 237, 1317–1323 (1987)

    ADS  MathSciNet  CAS  Article  Google Scholar 

  3. 3

    Ghirlanda, S. & Enquist, M. A century of generalization. Anim. Behav. 66, 15–36 (2003)

    Article  Google Scholar 

  4. 4

    Srinivasan, M. V. Pattern recognition in the honeybee: recent progress. J. Insect Physiol. 40, 183–194 (1994)

    Article  Google Scholar 

  5. 5

    Ronacher, B. How do bees learn and recognize visual patterns? Biol. Cybern. 79, 477–485 (1998)

    Article  Google Scholar 

  6. 6

    Giurfa, M. & Menzel, R. Insect visual perception: complex ability of a simple nervous system. Curr. Opin. Neurobiol. 7, 505–513 (1997)

    CAS  Article  Google Scholar 

  7. 7

    Giurfa, M. Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr. Opin. Neurobiol. 13, 726–735 (2003)

    CAS  Article  Google Scholar 

  8. 8

    Horridge, G. A. Vision of the honeybee Apis mellifera for patterns with two pairs of equal orthogonal bars. J. Insect Physiol. A 42, 131–138 (1996)

    CAS  Article  Google Scholar 

  9. 9

    Horridge, G. A. Vision of the honeybee Apis mellifera for patterns with one pair of equal orthogonal bars. J. Insect Physiol. A 43, 741–748 (1997)

    CAS  Article  Google Scholar 

  10. 10

    von Frisch, K. The Dance Language and Orientation of Bees 566 (Belknap Press of Harvard Univ. Press, Cambridge, Massachusetts, 1967)

    Google Scholar 

  11. 11

    Ronacher, B. Pattern recognition in honeybees: multidimensional scaling reveals a city-block metric. Vision Res. 32, 1837–1843 (1992)

    ADS  CAS  Article  Google Scholar 

  12. 12

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

    ADS  CAS  Article  Google Scholar 

  13. 13

    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 (1995)

    CAS  Article  Google Scholar 

  14. 14

    van Hateren, J. H., Srinivasan, M. V. & Wait, P. B. Pattern recognition in bees: orientation discrimination. J. Comp. Physiol. A167, 649–654 (1990)

    Article  Google Scholar 

  15. 15

    Horridge, G. A. Pattern discrimination by the honeybee: disruption as a cue. J. Comp. Physiol. A 181, 267–277 (1997)

    Article  Google Scholar 

  16. 16

    Horridge, G. A. The effect of complexity on the discrimination of oriented bars by the honeybee (Apis mellifera). J. Comp. Physiol. A 189, 703–714 (2003)

    CAS  Article  Google Scholar 

  17. 17

    Maurer, D., Le Grand, R. & Mondloch, C. J. The many faces of configural processing. Trends Cogn. Sci. 6, 255–260 (2002)

    Article  Google Scholar 

  18. 18

    Giurfa, M. et al. Pattern learning by honeybees: conditioning procedure and recognition strategy. Anim. Behav. 57, 315–324 (1999)

    CAS  Article  Google Scholar 

  19. 19

    Srinivasan, M. V. & Lehrer, M. Spatial acuity of honeybee vision and its spectral properties. J. Comp. Physiol. A 162, 159–172 (1988)

    Article  Google Scholar 

  20. 20

    Menzel, R. & Backhaus, W. in Vision and Visual Dysfunction. The Perception of Colour (ed. Gouras, P.) 262–288 (MacMillan, London, 1991)

    Google Scholar 

  21. 21

    Giger, A. D. & Srinivasan, M. V. Pattern recognition in honeybees: chromatic properties of orientation analyses. J. Comp. Physiol. A 178, 763–769 (1996)

    Article  Google Scholar 

  22. 22

    Dill, M., Wolf, R. & Heisenberg, M. Visual pattern recognition in Drosophila involves retinotopic matching. Nature 365, 751–753 (1993)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Osorio, D. Temporal and spectral properties of sustaining cells in the medulla of the locust. J. Comp. Physiol. 161, 441–448 (1987)

    Article  Google Scholar 

  24. 24

    James, A. C. & Osorio, D. Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques. J. Comp. Physiol. A 178, 183–199 (1996)

    CAS  Article  Google Scholar 

  25. 25

    Chen, L., Zhang, S. & Srinivasan, M. V. Global perception in small brains: topological pattern recognition in honeybees. Proc. Natl Acad. Sci. USA 100, 6884–6889 (2003)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Biedermann, I. Recognition-by-components: A theory of human image understanding. Psychol. Rev. 94, 115–147 (1987)

    Article  Google Scholar 

  27. 27

    Werner, C. W. & Rehkämper, G. Discrimination of multidimensional geometrical figures by chickens: categorization and pattern learning. Anim. Cogn. 2, 27–40 (1999)

    Article  Google Scholar 

  28. 28

    Treisman, A. & Gelade, G. A feature-integration theory of attention. Cogn. Psychol. 12, 97–136 (1980)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank J. Delius, M. Fabre-Thorpe, L. Huber, R. Menzel and S. Thorpe for valuable comments and corrections on previous versions of the manuscript, and N. Hempel de Ibarra for help with colour measurements. This work was supported by the German (DFG) and the French (CNRS) Research Councils, the University Paul-Sabatier, the German Academic Exchange Service (DAAD), Naturalia & Biologia (Paris) and the Institut Universitaire de France.

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Correspondence to Martin Giurfa.

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Stach, S., Benard, J. & Giurfa, M. Local-feature assembling in visual pattern recognition and generalization in honeybees. Nature 429, 758–761 (2004). https://doi.org/10.1038/nature02594

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