Apidologie

, Volume 43, Issue 3, pp 244–268 | Cite as

New vistas on honey bee vision

Original article

Abstract

The honey bee is a traditional animal model for the study of visual perception, learning, and memory. Extensive behavioral studies have shown that honey bees perceive, learn, and memorize colors, shapes, and patterns when these visual cues are paired with sucrose reward. Bee color vision is trichromatic, based on three photoreceptor types (S, M, L), which peak in the UV, blue, and green region of the spectrum. Perceptual color spaces have been proposed to account for bee color vision, and the anatomy of the visual neuropils in the bee brain was described to a large extent. In the last decade, conceptual and technical advances improved significantly our comprehension of visual processing in bees. At the behavioral level, unexpected cognitive visual capacities were discovered such as categorical and conceptual categorization. At the neurobiological level, molecular analyses of the compound eye revealed an intricate heterogeneity in the distribution of photoreceptors in the retina. Spatial segregation and integration of visual information in the bee brain has been analyzed at functional levels so far unexploited. These recent discoveries associated with the perspective of accessing the bee brain of harnessed bees while they perceive and learn visual cues open new avenues toward a comprehension of the neural substrates of visual perception and learning in bees. Understanding how the miniature brain of bees achieves sophisticated visual performances is a fundamental goal for the comparative study of vision and cognition.

Keywords

vision visual processing visual cognition honey bee Apis mellifera insect invertebrate 

Notes

Acknowledgments

We thank two anonymous reviewers and A. Dyer (Melbourne, Australia) for productive collaboration in the field of this review. We also thank the French Research Council (CNRS), the University Paul Sabatier (Project APIGENE), and the National Research Agency (ANR: Project Apicolor) for generous support. A. Avarguès-Weber was supported by the French ministry of Research and T. Mota by a doctoral scholarship from the CAPES Foundation and the Brazilian government. M. Giurfa thanks the Program Raíces of the Argentinean Research Ministry for a Milstein Grant.

References

  1. Abel, J.R., Menzel, R. (2001) Structure and response patterns of olfactory interneurons in the honey bee, Apis mellifera. J. Comp. Neurol. 437, 363–383PubMedCrossRefGoogle Scholar
  2. Anderson, A.M. (1972) The ability of honey bees to generalize visual stimuli. In: Wehner, R. (ed.) Information Processing in the Visual Systems of Arthropods. Springer, Berlin.Google Scholar
  3. Anderson, A.M. (1977) Parameters determining the attractiveness of stripe patterns in the honey bee. Anim. Behav. 25, 80–87CrossRefGoogle Scholar
  4. Autrum, H.J., Zwehl, V. (1964) Die spektrale Empfindlichkeit einzelner Sehzellen des Bienenauges. Z. vergl. Physiol. 48, 357–384CrossRefGoogle Scholar
  5. Avarguès-Weber, A., Deisig, N., Giurfa, M. (2011a) Visual cognition in social insects. Annu. Rev. Entomol. 56, 423–443CrossRefGoogle Scholar
  6. Avarguès-Weber, A., Dyer, A.G., Giurfa, M. (2011b) Conceptualization of above and below relationships by an insect. Proc. R. Soc. B 278, 898–905CrossRefGoogle Scholar
  7. Avarguès-Weber, A., Portelli, G., Benard, J., Dyer, A.G., Giurfa, M. (2010) Configural processing enables discrimination and categorization of face-like stimuli in honey bees. J. Exp. Biol. 213, 593–601PubMedCrossRefGoogle Scholar
  8. Backhaus, W. (1991) Color opponent coding in the visual system of the honey bee. Vision Res. 31, 1381–1397PubMedCrossRefGoogle Scholar
  9. Benard, J., Stach, S., Giurfa, M. (2006) Categorization of visual stimuli in the honey bee Apis mellifera. Anim. Cogn. 9, 257–70PubMedCrossRefGoogle Scholar
  10. Bicker, G., Schäfer, S., Rehder, V. (1987) Chemical neuroanatomy of the honey bee brain. In: Menzel, R., Mercer, A. (eds.) Neurobiology and Behavior of Honey Bees, pp. 202–224. Springer, BerlinCrossRefGoogle Scholar
  11. Bitterman, M.E. (1983) Classical conditioning of proboscis extension in honey bees (Apis mellifera). J. Comp. Psychol. 97, 107–119PubMedCrossRefGoogle Scholar
  12. Campan, R., Lehrer, M. (2002) Discrimination of closed shapes by two species of bee, Apis mellifera and Megachile rotundata. J. Exp. Biol. 205, 559–572PubMedGoogle Scholar
  13. Chittka, L. (1992) The colour hexagon: a chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J. Comp. Physiol. A 170, 533–543Google Scholar
  14. Chittka, L., Geiger, K. (1995) Can honey bees count landmarks? Anim. Behav. 49, 159–164CrossRefGoogle Scholar
  15. Chittka, L., Niven, J. (2009) Are bigger brains better? Curr. Biol. 19, R995–R1008PubMedCrossRefGoogle Scholar
  16. Chittka, L., Thomson, J.D., Waser, N.M. (1999) Flower constancy, insect psychology, and plant evolution. Naturwissenschaften 86, 361–377CrossRefGoogle Scholar
  17. Christensen, T.A., Pawlowski, V.M., Lei, H., Hildebrand, J.G. (2000) Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat. Neurosci. 3, 927–931PubMedCrossRefGoogle Scholar
  18. Collett, T.S. (1996) Insect navigation en route to the goal: multiple strategies for the use of landmarks. J. Exp. Biol. 199, 227–235PubMedCrossRefGoogle Scholar
  19. Collett, T.S., Zeil, J. (1998) Places and landmarks: an arthropod perspective. In: Healy, S. (ed.) Spatial Representation in Animals. Oxford University Press, Oxford.Google Scholar
  20. Collett, T.S., Collett, M. (2002) Memory use in insect visual navigation. Nat. Rev. Neurosci. 3, 542–552PubMedCrossRefGoogle Scholar
  21. Collett, T.S., Graham, P., Durier, V. (2003) Route learning by insects. Curr. Opin. Neurobiol. 13, 718–725PubMedCrossRefGoogle Scholar
  22. Dacke, M., Srinivasan, M.V. (2008) Evidence for counting in insects. Anim. Cogn. 11, 683–689PubMedCrossRefGoogle Scholar
  23. Dafni, A., Lehrer, M., Keyan, P.G. (1997) Spatial flower parameters and insect spatial vision. Biol. Rev. 72, 239–282CrossRefGoogle Scholar
  24. Daly, K.C., Wright, G.A., Smith, B.H. (2004) Molecular features of odorants systematically influence slow temporal responses across clusters of coordinated antennal lobe units in the moth Manduca sexta. J. Neurophysiol. 92, 236–254PubMedCrossRefGoogle Scholar
  25. Daumer, K. (1956) Reizmetrische Untersuchungen des Farbensehens der Bienen. J. Comp. Physiol. 38, 413–478Google Scholar
  26. de Brito Sanchez, M.G., Chen, C., Li, J., Liu, F., Gauthier, M. (2008) Behavioral studies on tarsal gustation in honey bees: sucrose responsiveness and sucrose-mediated olfactory conditioning. J. Comp. Physiol. A 194, 861–869CrossRefGoogle Scholar
  27. Denker, M., Finke, R., Schaupp, F., Grün, S., Menzel, R. (2010) Neural correlates of odor learning in the honey bee antennal lobe. Eur. J. Neurosci. 31, 119–133PubMedCrossRefGoogle Scholar
  28. DeVoe, R.D., Kaiser, W., Ohm, J., Stone, L.S. (1982) Horizontal movement detectors of honey bees: directionally-selective visual neurons in the lobula and brain. J. Comp. Physiol. 147, 155–170CrossRefGoogle Scholar
  29. Doumas, L.A.A., Hummel, J.E., Sandhofer, C.M. (2008) A theory of the discovery and predication of relational concepts. Psychol. Rev. 115, 1–43PubMedCrossRefGoogle Scholar
  30. Dyer, A.G., Paulk, A.C., Reser, D.H. (2011) Colour processing in complex environments: insights from the visual system of bees. Proc. Biol. Sci. 278, 952–959PubMedCrossRefGoogle Scholar
  31. Ehmer, B., Gronenberg, W. (2002) Segregation of visual input to the mushroom bodies in the honey bee (Apis mellifera). J. Comp. Neurol. 451, 362–373PubMedCrossRefGoogle Scholar
  32. Ernst, R., Heisenberg, M. (1999) The memory template in Drosophila pattern vision at the flight simulator. Vision Res. 39, 3920–3933PubMedCrossRefGoogle Scholar
  33. Faber, T., Joerges, J., Menzel, R. (1999) Associative learning modifies neural representations of odours in the insect brain. Nat. Neurosci. 2, 74–78PubMedCrossRefGoogle Scholar
  34. Farooqui, T., Robinson, K., Vaessin, H., Smith, B.H. (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honey bee. J. Neurosci. 23, 5370–5380PubMedGoogle Scholar
  35. Farooqui, T., Vaessin, H., Smith, B.H. (2004) Octopamine receptors in the honey bee (Apis mellifera) brain and their disruption by RNA-mediated interference. J. Insect Physiol. 50, 701–713PubMedCrossRefGoogle Scholar
  36. Fernandez, P.C., Locatelli, F.F., Person-Rennell, N., Deleo, G., Smith, B.H. (2009) Associative conditioning tunes transient dynamics of early olfactory processing. J. Neurosci. 29, 10191–10202PubMedCrossRefGoogle Scholar
  37. Gallistel, C.R. (1993) A conceptual framework for the study of numerical estimation and arithmetic reasoning in animals. In: Boysen, S.T., Capaldi, E.J. (eds.) The Development of Numerical Competence: Animal and Human Models, pp. 211–223. Lawrence Erlbaum Associates, HillsdaleGoogle Scholar
  38. Gerber, B., Smith, B. (1998) Visual modulation of olfactory learning in honeybee. J. Exp. Biol. 201, 2213–2217PubMedGoogle Scholar
  39. Ghirlanda, S., Enquist, M. (2003) A century of generalization. Anim. Behav. 66, 15–36CrossRefGoogle Scholar
  40. Giger, A., Srinivasan, M.V. (1997) Honey bee vision: analysis of orientation and colour in the lateral, dorsal and ventral fields of view. J. Exp. Biol. 200, 1271–1280PubMedGoogle Scholar
  41. Giurfa, M. (2007) Behavioral and neural analysis of associative learning in the honey bee: a taste from the magic well. J. Comp. Physiol. A 193, 801–24CrossRefGoogle Scholar
  42. Giurfa, M., Menzel, R. (1997) Insect visual perception: complex ability of simple nervous systems. Curr. Opin. Neurobiol. 7, 505–513PubMedCrossRefGoogle Scholar
  43. Giurfa, M., Vorobyev, M. (1997) The detection and recognition of color stimuli by honey bees: performance and mechanisms. Israel J. Plant Sci. 45, 129–140Google Scholar
  44. Giurfa, M., Backhaus, W., Menzel, R. (1995) Color and angular orientation in the discrimination of bilateral symmetric patterns in the honey bee. Naturwissenschaften 82, 198–201CrossRefGoogle Scholar
  45. Giurfa, M., Eichmann, B., Menzel, R. (1996a) Symmetry perception in an insect. Nature 382, 458–461PubMedCrossRefGoogle Scholar
  46. Giurfa, M., Zaccardi, G., Vorobyev, M. (1999) How do bees detect coloured targets using different regions of their compound eyes. J. Comp. Physiol. A 185, 591–600CrossRefGoogle Scholar
  47. Giurfa, M., Vorobyev, M., Kevan, P., Menzel, R. (1996b) Detection of coloured stimuli by honey bees: minimum visual angles and receptor specific contrasts. J. Comp. Physiol. A 178, 699–709CrossRefGoogle Scholar
  48. Giurfa, M., Vorobyev, M., Brandt, R., Posner, B., Menzel, R. (1997) Discrimination of coloured stimuli by honey bees: alternative use of achromatic and chromatic signals. J. Comp. Physiol. A 180, 235–243CrossRefGoogle Scholar
  49. Giurfa, M., Zhang, S., Jenett, A., Menzel, R., Srinivasan, M.V. (2001) The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410, 930–933PubMedCrossRefGoogle Scholar
  50. Giurfa, M., Fabre, E., Flaven-Pouchon, J., Groll, H., Oberwallner, B., et al. (2009) Olfactory conditioning of the sting extension reflex in honey bees: memory dependence on trial number interstimulus interval intertrial interval and protein synthesis. Learn. Mem. 16, 761–765PubMedCrossRefGoogle Scholar
  51. Goetz, K.G., Hengstenberg, B., Biesinger, R. (1979) Optomotor control of wing beat and body posture in Drosophila. Biol. Cybern. 35, 101–112CrossRefGoogle Scholar
  52. Grant, V. (1950) The flower constancy of bees. Botanic Rev. 16, 379–398CrossRefGoogle Scholar
  53. Gribakin, F.G. (1975) Functional morphology of the compound eye of the bee. In: Horridge, G.A. (ed.) The Compound Eye and Vision of Insects, pp. 154–176. Clarendon, OxfordGoogle Scholar
  54. Griffin, D.R. (1992) Animal Minds: Beyond Cognition to Consciousness. University Chicago Press, ChicagoGoogle Scholar
  55. Gronenberg, W. (1986) Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain. J. Insect Physiol. 32, 695–704CrossRefGoogle Scholar
  56. Gross, H.J., Pahl, M., Si, A., Zhu, H., Tautz, J., et al. (2009) Number-based visual generalisation in the honey bee. PLoS ONE 4, e4263PubMedCrossRefGoogle Scholar
  57. Halford, G.S., Wilson, W.H., Phillips, S. (2010) Relational knowledge: the foundation of higher cognition. Trends. Cogn. Sci. 14, 497–505PubMedCrossRefGoogle Scholar
  58. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honey bees. Nature 366, 59–63CrossRefGoogle Scholar
  59. Hammer, M., Menzel, R. (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honey bees. Learn. Mem. 5, 146–156PubMedGoogle Scholar
  60. Hempel de Ibarra, N., Giurfa, M. (2003) Discrimination of closed shapes by honey bees requires only contrast to the long wavelength receptor type. Anim. Behav. 66, 903–910CrossRefGoogle Scholar
  61. Hempel de Ibarra, N., Vorobyev, M., Brandt, R., Giurfa, M. (2000) Detection of bright and dim colours by honey bees. J. Exp. Biol. 203, 3289–3298PubMedGoogle Scholar
  62. Hempel de Ibarra, N., Giurfa, M., Vorobyev, M.V. (2002) Discrimination of coloured patterns by honey bees through chromatic and achromatic cues. J. Comp. Physiol. A 188, 503–512CrossRefGoogle Scholar
  63. Herrnstein, R.J. (1990) Levels of stimulus control: a functional approach. Cognition 37, 133–166PubMedCrossRefGoogle Scholar
  64. Hertel, H. (1980) Chromatic properties of identified interneurons in the optic lobes of the bee. J. Comp. Physiol. 137, 215–231CrossRefGoogle Scholar
  65. Hertel, H., Maronde, U. (1987) The physiology and morphology of centrally projecting visual interneurons in the honey bee brain. J. Exp. Biol. 133, 301–315Google Scholar
  66. Hertel, H., Schäfer, S., Maronde, U. (1987) The physiology and morphology of visual commissures in the honey bee brain. J. Exp. Biol. 133, 283–300Google Scholar
  67. Hertz, M. (1929) Die Organisation des optischen Feldes bei der Biene. I. Z. vergl. Physiol. 8, 693–748CrossRefGoogle Scholar
  68. Hertz, M. (1933) Über figurale Intensität und Qualität in der optische Wahrnehmung der Biene. Biol. Zbl. 53, 10–40Google Scholar
  69. Hertz, M. (1935) Die Untersuchungen über den Formensinn der Honigbiene. Naturwissenschaften 23, 618–624CrossRefGoogle Scholar
  70. Homberg, U. (1985) Interneurons of the central complex of the bee brain (Apis mellifica L.). J. Insect Physiol 31, 251–264CrossRefGoogle Scholar
  71. Honey Bee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honey bee Apis mellifera. Nature 443, 931–949CrossRefGoogle Scholar
  72. Hori, S., Takeuchi, H., Arikawa, K., Kinoshita, M., Ichikawa, N., et al. (2006) Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honey bee Apis mellifera L. J. Comp. Physiol. A 192, 691–700CrossRefGoogle Scholar
  73. Hori, S., Takeuchi, H., Kubo, T. (2007) Associative learning and discrimination of motion cues in the harnessed honey bee Apis mellifera L. J. Comp. Physiol. A 193, 825–833CrossRefGoogle Scholar
  74. Horridge, A. (1997) Pattern discrimination by the honey bee: disruption as a cue. J. Comp. Physiol. A 181, 267–277CrossRefGoogle Scholar
  75. Horridge, A. (2009) Generalization in visual recognition by the honey bee (Apis mellifera): a review and explanation. J. Insect Physiol. 55, 499–511PubMedCrossRefGoogle Scholar
  76. Horridge, G.A., Zhang, S.W. (1995) Pattern vision in honey bees (Apis mellifera): flower-like patterns with no predominant orientation. J. Insect Physiol. 41, 681–688CrossRefGoogle Scholar
  77. Horridge, G.A. (1996) The honey bee (Apis mellifera) detects bilateral symmetry and discriminates its axis. J. Insect Physiol. 42, 755–764CrossRefGoogle Scholar
  78. Joerges, J., Küttner, A., Galizia, C.G., Menzel, R. (1997) Representation of odours and odour mixtures visualized in the honey bee brain. Nature 387, 285–288CrossRefGoogle Scholar
  79. Kien, J., Menzel, R. (1977a) Chromatic properties of interneurons in the optic lobes of the bee. I. Broad band neurons. J. Comp. Physiol. A 113, 17–34Google Scholar
  80. Kien, J., Menzel, R. (1977b) Chromatic properties of interneurons in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J. Comp. Physiol. A 113, 35–53CrossRefGoogle Scholar
  81. Kirschner, S., Kleineidam, C.J., Zube, C., Rybak, J., Grünewald, B., et al. (2006) Dual olfactory pathway in the honey bee, Apis mellifera. J. Comp. Neurol. 499, 933–952PubMedCrossRefGoogle Scholar
  82. Kühn, A. (1927) Über den Farbensinn der Bienen. Z. vergl. Physiol. 5, 762–800CrossRefGoogle Scholar
  83. Kühn, A., Pohl, R. (1921) Dressurfähigkeit der Bienen auf Spektrallinien. Naturwissenschaften 9, 738–740CrossRefGoogle Scholar
  84. Kuwabara, M. (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J. Faculty Sci., Hokkaido Univ., Series VI. Zoology 13, 458–464Google Scholar
  85. Labhart, T., Meyer, E.P. (2002) Neural mechanisms in insect navigation: polarization compass and odometer. Curr. Opin. Neurobiol. 12, 707–714PubMedCrossRefGoogle Scholar
  86. Lamberts, K., Shanks, D. (1997) Knowledge, Concepts, and Categories. Psychology, CambridgeGoogle Scholar
  87. Lehrer, M. (1994) Spatial vision in the honey bee: the use of different cues in different tasks. Vision Res. 34, 2363–2385PubMedCrossRefGoogle Scholar
  88. Lehrer, M. (1998) Looking all around: honey bees use different cues in different eye regions. J. Exp. Biol. 201, 3275–3292PubMedGoogle Scholar
  89. Lehrer, M. (1999) Dorsoventral asymmetry of colour discrimination in bees. J. Comp. Physiol. A 184, 195–206CrossRefGoogle Scholar
  90. Lozano, V.C., Armengaud, C., Gauthier, M. (2001) Memory impairment induced by cholinergic antagonists injected into mushroom bodies of the honey bee. J. Comp. Physiol. A 187, 249–254PubMedCrossRefGoogle Scholar
  91. Luu, T., Cheung, A., Ball, D., Srinivasan, M.V. (2011) Honey bee flight: a novel ‘streamlining’ response. J. Exp. Biol. 214, 2215–2225PubMedCrossRefGoogle Scholar
  92. Mareschal, D., Quinn, P.C., Lea, S.E.G. (2010) The Making of Human Concepts. Oxford University Press, OxfordGoogle Scholar
  93. Mauelshagen, J. (1993) Neural correlates of olfactory learning paradigms in an identified neuron in the honey bee brain. J. Neurophysiol. 69, 609–625PubMedGoogle Scholar
  94. Menzel, R. (1974) Spectral sensitivity of monopolar cells in the bee lamina. J. Comp. Physiol. A 93, 337–346CrossRefGoogle Scholar
  95. Menzel, R. (1979) Spectral sensitivity and colour vision in invertebrates. In: Autrum, H. (ed.) Invertebrate Photoreceptors—Handbook of Sensory Physiology, pp. 503–580. Springer, BerlinGoogle Scholar
  96. Menzel, R. (1999) Memory dynamics in the honey bee. J. Comp. Physiol. A 185, 323–340CrossRefGoogle Scholar
  97. Menzel, R., Snyder, A.W. (1974) Polarized light detection in the bee, Apis mellifera. J. Comp. Physiol. 88, 247–270CrossRefGoogle Scholar
  98. Menzel, R., Blakers, M. (1976) Colour receptors in the bee eye—morphology and spectral sensitivity. J. Comp. Physiol. 108, 11–33CrossRefGoogle Scholar
  99. Menzel, R., Lieke, E. (1983) Antagonistic color effects in spatial vision of honey bees. J. Comp. Physiol. 151, 441–448CrossRefGoogle Scholar
  100. Menzel, R., Backhaus, W. (1991) Color vision in insects. In: Gouras, P. (ed.) Vision and Visual Dysfunction the Perception of Color, pp. 262–288. Macmillan, LondonGoogle Scholar
  101. Menzel, R., Ventura, D.F., Hertel, H., de Souza, J.M., Greggers, U. (1986) Spectral sensitivity of photoreceptors in insect compound eyes: comparison of species and methods. J. Comp. Physiol. A 158, 165–177CrossRefGoogle Scholar
  102. Menzel, R., Greggers, U., Smith, A., Berger, S., Brandt, R., et al. (2005) Honey bees navigate according to a map-like spatial memory. Proc. Natl. Acad. Sci. USA 102, 3040–3045PubMedCrossRefGoogle Scholar
  103. Meyer, E. (1984) Retrograde labelling of photoreceptors in different regions of the compound eyes of bees and ants. J. Neurocyt. 13, 825–36CrossRefGoogle Scholar
  104. Milde, J.J. (1988) Visual responses of interneurones in the posterior median protocerebrum and the central complex of the honey bee Apis mellifera. J. Insect Physiol. 34, 427–436CrossRefGoogle Scholar
  105. Mobbs, P.G. (1984) Neural networks in the mushroom bodies of the honey bee. J. Insect Physiol. 30, 43–58CrossRefGoogle Scholar
  106. Mota, T., Giurfa, M., Sandoz, J.C. (2011a) Color modulates olfactory learning in honey bees by an occasion-setting mechanism. Learn. Mem. 18, 144–155CrossRefGoogle Scholar
  107. Mota, T., Roussel, E., Sandoz, J.C., Giurfa, M. (2011b) Visual conditioning of the sting extension reflex in harnessed honey bees. J. Exp. Biol. 214, 3577–3587CrossRefGoogle Scholar
  108. Mota, T., Yamagata, N., Giurfa, M., Gronenberg, W., Sandoz, J.-C. (2011c) Neural organization and visual processing in the anterior optic tubercle of the honey bee brain. J. Neurosci. 31, 11443–11456PubMedCrossRefGoogle Scholar
  109. Müller, U. (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honey bee, Apis mellifera. Neuron 27, 159–168CrossRefGoogle Scholar
  110. Murphy, G.L. (2002) The Big Book of Concepts. MIT, CambridgeGoogle Scholar
  111. Murphy, G.L. (2010) What are categories and concepts? In: Mareschal, D., Quinn, P.C., Lea, S.E.G. (eds.) The Making of Human Concepts. Oxford University Press, OxfordGoogle Scholar
  112. Niggebrugge, C., Leboulle, G., Menzel, R., Komischke, B., de Ibarra, N.H. (2009) Fast learning but coarse discrimination of colours in restrained honey bees. J. Exp. Biol. 212, 1344–1350PubMedCrossRefGoogle Scholar
  113. Paulk, A.C., Gronenberg, W. (2008) Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Struct. Dev. 37, 443–458PubMedCrossRefGoogle Scholar
  114. Paulk, A.C., Phillips-Portillo, J., Dacks, A., Fellous, J.-M., Gronenberg, W. (2008) The processing of color, motion, and stimulus timing are anatomically segregated in the bumblebee brain. J. Neurosci. 28, 6319–6332PubMedCrossRefGoogle Scholar
  115. Paulk, A.C., Dacks, A.M., Gronenberg, W. (2009a) Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens). J. Comp. Neurol. 513, 441–456PubMedCrossRefGoogle Scholar
  116. Paulk, A.C., Dacks, A.M., Phillips-Portillo, J., Fellous, J.-M., Gronenberg, W. (2009b) Visual processing in the central bee brain. J. Neurosci. 29, 9987–9999PubMedCrossRefGoogle Scholar
  117. Pearce, J.M. (1987) A model for stimulus generalization in Pavlovian conditioning. Psychol. Rev. 94, 61–73PubMedCrossRefGoogle Scholar
  118. Peitsch, D., Fietz, A., Hertel, H., Souza, J., Ventura, D.F., et al. (1992) The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A 170, 23–40PubMedCrossRefGoogle Scholar
  119. Ribi, W.A. (1975a) The first optic ganglion of the bee. I. Correlation between visual cell types and their terminals in the lamina and medulla. Cell Tissue Res. 165, 103–111PubMedCrossRefGoogle Scholar
  120. Ribi, W.A. (1975b) The neurons of the first optic ganglion of the bee (Apis mellifera). Adv. Anat. Embryol. Cell Biol. 50, 1–43PubMedGoogle Scholar
  121. Ribi, W.A., Scheel, M. (1981) The second and third optic ganglia of the worker bee: Golgi studies of the neuronal elements in the medulla and lobula. Cell Tissue Res. 221, 17–43PubMedCrossRefGoogle Scholar
  122. Riehle, A. (1981) Color opponent neurons of the honey bee in a heterochromatic flicker test. J. Comp. Physiol. A 142, 81–88CrossRefGoogle Scholar
  123. Rind, F.C. (2004) Bioinspired sensors: From insect eyes to robot vision. In: Christensen, T. A. (ed.) Methods in Insect Sensory Neurosciences. CRC, Boca Raton.Google Scholar
  124. Rossel, S., Wehner, R. (1984) How bees analyse the polarization patterns in the sky. Experiments and model. J. Comp. Physiol. A 154, 607–615CrossRefGoogle Scholar
  125. Rossel, S., Wehner, R. (1986) Polarization vision in bees. Nature 323, 128–131CrossRefGoogle Scholar
  126. Roussel, E., Sandoz, J.C., Giurfa, M. (2010) Searching for learning-dependent changes in the antennal lobe: simultaneous recording of neural activity and aversive olfactory learning in honey bees. Front. Behav. Neurosci. 4, 1–12Google Scholar
  127. Rybak, J., Menzel, R. (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J. Comp. Neurol. 334, 444–465PubMedCrossRefGoogle Scholar
  128. Sandoz, J.C., Galizia, C.G., Menzel, R. (2003) Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honey bee antennal lobes. Neurosci. 120, 1137–1148CrossRefGoogle Scholar
  129. Shepard, R.N. (1987) Toward a universal law of generalization for psychological science. Science 237, 1317–1323PubMedCrossRefGoogle Scholar
  130. Skorupski, P., Chittka, L. (2010) Differences in photoreceptor processing speed for chromatic and achromatic vision in the bumblebee, Bombus terrestris. J. Neurosci. 30, 3896–3903PubMedCrossRefGoogle Scholar
  131. Spaethe, J., Briscoe, A.D. (2004) Early duplication and functional diversification of the opsin gene family in insects. Mol. Biol. Evol. 21, 1583–1594PubMedCrossRefGoogle Scholar
  132. Spaethe, J., Briscoe, A.D. (2005) Molecular characterization and expression of the UV opsin in bumblebees: three ommatidial subtypes in the retina and a new photoreceptor organ in the lamina. J. Exp. Biol. 208, 2347–2361PubMedCrossRefGoogle Scholar
  133. Spence, K.W. (1937) The differential response in animals to stimuli varying within a single dimension. Psychol. Rev. 44, 430–444CrossRefGoogle Scholar
  134. Srinivasan, M.V. (1994) Pattern recognition in the honey bee: recent progress. J. Insect Physiol. 40, 183–194CrossRefGoogle Scholar
  135. Srinivasan, M.V. (2006) Honey bee vision: in good shape for shape recognition. Curr. Biol. 16, R58–R60PubMedCrossRefGoogle Scholar
  136. Srinivasan, M.V. (2011) Honey bees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. Physiol. Rev. 91, 413–460PubMedCrossRefGoogle Scholar
  137. Srinivasan, M.V., Lehrer, M. (1984) Temporal acuity of honey bee vision: behavioural studies using moving stimuli. J. Comp. Physiol. A 155, 297–312CrossRefGoogle Scholar
  138. Srinivasan, M.V., Lehrer, M. (1985) Temporal resolution of colour vision in the honey bee. J. Comp. Physiol. A 157, 579–586PubMedCrossRefGoogle Scholar
  139. Srinivasan, M.V., Lehrer, M. (1988) Spatial acuity of honeybee vision, and its spectral properties. J. Comp. Physiol. A 162, 159–72CrossRefGoogle Scholar
  140. Stach, S., Benard, J., Giurfa, M. (2004) Local-feature assembling in visual pattern recognition and generalization in honey bees. Nature 429, 758–61PubMedCrossRefGoogle Scholar
  141. Strausfeld, N.J., Okamura, J.Y. (2007) Visual system of calliphorid flies: organization of optic glomeruli and their lobula complex efferents. J. Comp. Neurol. 500, 166–188PubMedCrossRefGoogle Scholar
  142. Strausfeld, N.J., Sinakevitch, I., Okamura, J.Y. (2007) Organization of local interneurons in optic glomeruli of the dipterous visual system and comparisons with the antennal lobes. Dev. Neurobiol. 67, 1267–1288PubMedCrossRefGoogle Scholar
  143. Takeda, K. (1961) Classical conditioned response in the honey bee. J. Insect Physiol. 6, 168–179CrossRefGoogle Scholar
  144. Thompson, R. K. R. (1995) Natural and relational concepts in animals. In: Roitblat, H., Meyer, J. A. (eds.) Comparative Approaches to Cognitive Science. MIT, Cambridge.Google Scholar
  145. van Hateren, J.H., Srinivasan, M.V., Wait, P.B. (1990) Pattern recognition in bees: orientation discrimination. J. Comp. Physiol. A 167, 649–654CrossRefGoogle Scholar
  146. Velarde, R.A., Sauer, C.D., Walden, K.O., Fahrbach, S.E., Robertson, H.M. (2005) Pteropsin: a vertebrate-like non-visual opsin expressed in the honey bee brain. Insect Biochem. Mol. Biol. 35, 1367–1377PubMedCrossRefGoogle Scholar
  147. Vergoz, V., Roussel, E., Sandoz, J.C., Giurfa, M. (2007) Aversive learning in honey bees revealed by the olfactory conditioning of the sting extension reflex. PLoS ONE 2, e288PubMedCrossRefGoogle Scholar
  148. von Frisch, K. (1914) Der Farbensinn und Formensinn der Bienen. Z. Jhb. Physiol. 37, 1–128Google Scholar
  149. von Frisch, K. (1967) The Dance Language and Orientation of Bees. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  150. Vorobyev, M., Osorio, D. (1998) Receptor noise as a determinant of colour thresholds. Proc. Biol. Sci. 265, 351–358PubMedCrossRefGoogle Scholar
  151. Vorobyev, M., Gumbert, A., Kunze, J., Giurfa, M., Menzel, R. (2001) Colour threshold and receptor noise: behaviour and physiology compared. Vision Res. 41, 639–653PubMedCrossRefGoogle Scholar
  152. Wakakuwa, M., Kurasawa, M., Giurfa, M., Arikawa, K. (2005) Spectral heterogeneity of honey bee ommatidia. Naturwissenschaften 92, 464–467PubMedCrossRefGoogle Scholar
  153. Waterman, T.H. (1981) Polarization sensitivity. In: Autrum, H. (ed.) Handbook of Sensory Physiology VII/6B, pp. 281–469. Springer, BerlinGoogle Scholar
  154. Wehner, R. (1967) Pattern recognition in bees. Nature 215, 1244–1249PubMedCrossRefGoogle Scholar
  155. Wehner, R. (1971) The generalization of directional visual stimuli in the honey bee. Apis mellifera. J. Insect Physiol. 17, 1579–1591CrossRefGoogle Scholar
  156. Wehner, R., Strasser, S. (1985) The POL area of the honey bee’s eye: behavioural evidence. Physiol. Entomol. 10, 337–349CrossRefGoogle Scholar
  157. Werner, A., Menzel, R., Wehrhahn, C. (1988) Color constancy in the honey bee. J. Neurosci. 8, 156–159PubMedGoogle Scholar
  158. White, R.H., Xu, H., Münch, T.A., Bennett, R.R., Grable, E.A. (2003) The retina of Manduca sexta: rhodopsin-expression, the mosaic of green-, blue-, and UV-sensitive photoreceptors and regional specialization. J. Exp. Biol. 206, 3337–3348PubMedCrossRefGoogle Scholar
  159. Wolf, R., Heisenberg, M. (1991) Basic organization of operant behavior as revealed in Drosophila flight orientation. J. Comp. Physiol. A 169, 699–705PubMedCrossRefGoogle Scholar
  160. Yang, E.C., Lin, H.C., Hung, Y.S. (2004) Patterns of chromatic information processing in the lobula of the honey bee. Apis mellifera L. J. Insect Physiol. 50, 913–925CrossRefGoogle Scholar
  161. Zayan, R., Vauclair, J. (1998) Categories as paradigms for comparative cognition. Behav. Process. 42, 87–99CrossRefGoogle Scholar
  162. Zentall, T.R., Galizio, M., Critchfied, T.S. (2002) Categorization, concept learning, and behavior analysis: an introduction. J. Exp. Analys. Behav. 78, 237–248CrossRefGoogle Scholar
  163. Zentall, T.R., Wasserman, E.A., Lazareva, O.F., Thompson, R.K.R., Rattermann, M.J. (2008) Concept learning in animals. Comp. Cogn. Behav. Rev. 3, 13–45Google Scholar
  164. Zhang, S.W., Srinivasan, M.V., Collett, T. (1995) Convergent processing in Honey bee vision: multiple channels for the recognition of shape. Proc. Natl. Acad. Sci. USA 92, 3029–3031PubMedCrossRefGoogle Scholar
  165. Zhang, S., Srinivasan, M.V., Zhu, H., Wong, J. (2004) Grouping of visual objects by honey bees. J. Exp. Biol. 207, 3289–3298PubMedCrossRefGoogle Scholar
  166. Zhang, S., Bock, F., Si, A., Tautz, J., Srinivasan, M.V. (2005) Visual working memory in decision making by honey bees. Proc. Natl. Acad. Sci. USA 102, 5250–5255PubMedCrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag, France 2012

Authors and Affiliations

  • Aurore Avarguès-Weber
    • 1
    • 2
    • 3
  • Theo Mota
    • 1
    • 2
  • Martin Giurfa
    • 1
    • 2
  1. 1.Centre de Recherches sur la Cognition AnimaleUniversité de Toulouse (UPS)Toulouse Cedex 9France
  2. 2.Centre National de la Recherche Scientifique (CNRS); Centre de Recherches sur la Cognition AnimaleToulouse Cedex 9France
  3. 3.School of Biological and Chemical Sciences, Queen MaryUniversity of LondonLondonUK

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