Abstract
Since the demonstration of color vision in honey bees 100 years ago by Karl von Frisch, appetitive conditioning to color targets has been used as the principal way to access behavioral aspects of bee color vision. Yet, analyses on how conditioning parameters affect color perception remained scarce. Conclusions on bee color vision have often been made without referring them to the experimental context in which they were obtained, and thus presented as absolute facts instead of realizing that subtle variations in conditioning procedures might yield different results. Here, we review evidence showing that color learning and discrimination in bees are not governed by immutable properties of their visual system, but depend on how the insects are trained and thus learn a task. The use of absolute or differential conditioning protocols, the presence of aversive reinforcement in differential conditioning and the degrees of freedom of motor components determine dramatic variations in color discrimination. We, thus, suggest top-down attentional modulation of color vision to explain the changes in color learning and discrimination reviewed here. We discuss the possible neural mechanisms of this modulation and conclude that color vision experiments require a careful consideration of how training parameters shape behavioral responses.
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Andretic R, van Swinderen B, Greenspan RJ (2005) Dopaminergic modulation of arousal in Drosophila. Curr Biol 15(13):1165–1175. doi:10.1016/j.cub.2005.05.025
Avarguès-Weber A, de Brito Sanchez MG, Giurfa M, Dyer AG (2010) Aversive reinforcement improves visual discrimination learning in free-flying honeybees. PLoS One 5(10):e15370
Avarguès-Weber A, Mota T, Giurfa M (2012) New vistas on honey bee vision. Apidologie 43(3):244–268. doi:10.1007/s13592-012-0124-2
Backhaus W (1991) Color opponent coding in the visual system of the honeybee. Vision Res 31:1381–1397
Benard J, Stach S, Giurfa M (2006) Categorization of visual stimuli in the honeybee Apis mellifera. Anim Cognit 9(4):257–270
Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97(2):107–119
Blenau W, Thamm M (2011) Distribution of serotonin (5-HT) and its receptors in the insect brain with focus on the mushroom bodies. Lessons from Drosophila melanogaster and Apis mellifera. Arthr Struct Dev 40(5):381–394. doi:10.1016/j.asd.2011.01.004
Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510
Bukovac Z, Dorin A, Dyer AG (2013) A-bees see: a simulation to assess social bee visual attention during complex search tasks. Adv Artif Life, ECAL, pp 276–283
Burns JG, Dyer AG (2008) Diversity of speed-accuracy strategies benefits social insects. Curr Biol 18(20):R953–R954
Chittka L (1992) The color hexagon: a chromaticity diagram based on photoreceptor excitations as a general representation of colour opponency. J Comp Physiol A 170:533–543
Chittka L, Briscoe A (2001) Why sensory ecology needs to become more evolutionary––insect color vision as a case in point. In: Barth FG, Schmid A (eds) Ecology of sensing. Springer-Verlag, Berlin, pp 19–37
Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics: bees trade off foraging speed for accuracy. Nature 424(6947):388
Conway BR (2009) Color vision, cones, and color-coding in the cortex. Neuroscientist 15(3):274–290
Dacey DM (1996) Circuitry for color coding in the primate retina. Proc Natl Acad Sci USA 93(2):582–588
de Brito Sanchez MG, Chen C, Li J, Liu F, Gauthier M, Giurfa M (2008) Behavioral studies on tarsal gustation in honeybees: sucrose responsiveness and sucrose-mediated olfactory conditioning. J Comp Physiol A 194(10):861–869. doi:10.1007/s00359-008-0357-8
Dobrin SE, Fahrbach SE (2012) Visual associative learning in restrained honey bees with intact antennae. PLoS One 7(6):e37666. doi:10.1371/journal.pone.0037666
Dyer AG (2012) The mysterious cognitive abilities of bees: why models of visual processing need to consider experience and individual differences in animal performance. J Exp Biol 215:387–395. doi:10.1242/jeb.038190
Dyer AG, Chittka L (2004a) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A 190(9):759–763
Dyer AG, Chittka L (2004b) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227
Dyer AG, Neumeyer C (2005) Simultaneous and successive colour discrimination in the honeybee (Apis mellifera). J Comp Physiol A 191(6):547–557
Dyer AG, Spaethe J, Prack S (2008) Comparative psychophysics of bumblebee and honeybee colour discrimination and object detection. J Comp Physiol A 194(7):617–627. doi:10.1007/s00359-008-0335-1
Dyer AG, Paulk AC, Reser DH (2011) Colour processing in complex environments: insights from the visual system of bees. Proc Biol Sci 278:952–959. doi:10.1098/rspb.2010.2412
Ehmer B, Gronenberg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451(4):362–373. doi:10.1002/cne.10355
Forel A (1910) Das Sinnesleben der Insekten: eine Sammlung von experimentellen und kritischen Studien über Insektenpsychologie (1910). Reinhardt, Munich, p 172
Giurfa M (2004) Conditioning procedure and color discrimination in the honeybee Apis mellifera. Die Naturwissenschaften 91(5):228–231
Giurfa M, Sandoz JC (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Mem 19(2):54–66. doi:10.1101/lm.024711.111
Giurfa M, Núñez JA, Chittka L, Menzel R (1995) Colour preferences of flower-naive honeybees. J Comp Physiol A 177:247–259
Giurfa M, Hammer M, Stach S, Stollhoff N, Muller-deisig N, Mizyrycki C (1999) Pattern learning by honeybees: conditioning procedure and recognition strategy. Anim Behav 57(2):315–324
Gouras P (1972) Color opponency from fovea to striate cortex. Invest Ophthalmol 11(6):427–434
Greggers U, Menzel R (1993) Memory dynamics and foraging strategies of honeybees. Behav Ecol Sociobiol 32:17–29
Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York
Helversen Ov (1972) Zur spektralen Unterschiedsempfindlichkeit der Honigbiene. J Comp Physiol 80:439–472
Hori S, Takeuchi H, Arikawa K, Kinoshita M, Ichikawa N, Sasaki M, Kubo T (2006) Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L. J Comp Physiol A 192(7):691–700. doi:10.1007/s00359-005-0091-4
Hori S, Takeuchi H, Kubo T (2007) Associative learning and discrimination of motion cues in the harnessed honeybee Apis mellifera L. J Comp Physiol A 193(8):825–833. doi:10.1007/s00359-007-0234-x
Kien J, Menzel R (1977) Chromatic properties of interneurons in the optic lobes of the bee II. Narrow band and colour opponent neurons. J Comp Physiol A 113:35–53
Kühn A (1927) Über den Farbensinn der Bienen. Z Vergl Physiol 5:762–800. doi:10.1007/bf00302277
Kühn A, Pohl R (1921) Dressurfähigkeit der Bienen auf Spektrallinien. Die Naturwissenschaften 9(37):738–740. doi:10.1007/bf01487183
Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Ser VI Zool 13:458–464
Li W, Howard JD, Parrish TB, Gottfried JA (2008) Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319(5871):1842–1845. doi:10.1126/science.1152837
Lovell JH (1910) The color sense of the honey-bee: can bees distinguish colors? Am Nat 44:673–692
Lubbock J (1883) Ants, bees, and wasps: a record of observations on the habits of the social Hymenoptera. Kegan Paul, Trench, and Co, London, p 448
Matsumoto Y, Menzel R, Sandoz JC, Giurfa M (2012) Revisiting olfactory classical conditioning of the proboscis extension response in honey bees: a step towards standardized procedures. J Neurosci Meths 211(1):159–167
Menzel R (1967) Untersuchungen zum Erlernen von Spektralfarben durch die Honigbiene (Apis mellifica). Z Vergl Physiol 56:22–62
Menzel R (1968) Das Gedaechtnis der Honigbiene fuer Spektralfarben. I.Kurzzeitiges und langzeitiges Behalten. Z Vergl Physiol 60:82–102
Menzel R (1985) Learning in honey bees in an ecological and behavioral context. In: Hölldobler B, Lindauer M (eds) Experimental behavioral ecology and sociobiology. Gustav Fischer Verlag, Stuttgart, pp 55–74
Menzel R, Backhaus W (1989) Color vision in honey bees: phenomena and physiological mechanisms. In: Stavenga D, Hardie R (eds) Facets of vision. Springer, Berlin, pp 281–297
Menzel R, Backhaus W (1991) Colour vision in insects. In: Gouras P (ed) Vision and visual dysfunction. The perception of colour. MacMillan Press, London, pp 262–288
Menzel R, Giurfa M (2006) Dimensions of cognition in an insect, the honeybee. Behav Cognit Neurosci Rev 5:24–40
Menzel R, Manz G (2005) Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain. J Exp Biol 208:4317–4332
Menzel R, Shmida A (1993) The ecology of flower colours and the natural colour vision of insect pollinators: the Israeli flora as a study case. Biol Rev 68:81–120
Miller SM, Ngo TT, van Swinderen B (2012) Attentional switching in humans and flies: rivalry in large and miniature brains. Front Hum Neurosci 5:188. doi:10.3389/fnhum.2011.00188
Morawetz L, Spaethe J (2012) Visual attention in a complex search task differs between honeybees and bumblebees. J Exp Biol 215(14):2515–2523. doi:10.1242/jeb.066399
Müller H (1882) Versuche über die Farbenliebhaberei der Honigbiene. Kosmos 12:273–299
Niggebrugge C, Leboulle G, Menzel R, Komischke B, de Ibarra NH (2009) Fast learning but coarse discrimination of colours in restrained honeybees. J Exp Biol 212(9):1344–1350. doi:10.1242/jeb.021881
Núñez JA (1982) Honeybee foraging strategies at a food source in relation to its distance from the hive and the rate of sugar flow. J Apicult Res 21:139–150
O’Day PM, Lisman JE (1985) Octopamine enhances dark-adaptation in Limulus ventral photoreceptors. J Neurosci 5:1490–1496
Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. Oxford University Press, Oxford
Pophof B (2000) Octopamine modulates the sensitivity of silkmoth pheromone receptor neurons. J Comp Physiol A 186:307–313
Reser DH, Wijesekara Witharanage R, Rosa MGP, Dyer AG (2012) Honeybees (Apis mellifera) learn color discriminations via differential conditioning independent of long wavelength (green) photoreceptor modulation. PLoS One 7(11):e48577. doi:10.1371/journal.pone.0048577
Resnik J, Sobel N, Paz R (2011) Auditory aversive learning increases discrimination thresholds. Nat Neurosci 14(6):791-U157. doi:10.1038/nn.2802
Riveros AJ, Gronenberg W (2012) Decision-making and associative color learning in harnessed bumblebees (Bombus impatiens). Anim Cognit 15(6):1183–1193. doi:10.1007/s10071-012-0542-6
Rodríguez-Gironés MA, Trillo A, Corcobado G (2013) Long term effects of aversive reinforcement on colour discrimination learning in free-flying bumblebees. PLoS One 8(8):e71551. doi:10.1371/journal.pone.0071551
Sareen P, Wolf R, Heisenberg M (2011) Attracting the attention of a fly. Proc Natl Acad Sci USA 108(17):7230–7235. doi:10.1073/pnas.1102522108
Schäfer S, Bicker G (1986) Common projection areas of 5-HT- and GABA-like immunoreactive fibres in the visual system of the honeybee. Brain Res 380:368–370
Schäfer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honey bee. J Comp Neurol 280:43–58
Scheiner R, Baumann A, Blenau W (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4(4):259–276
Schiller PH, Logothetis NK, Charles ER (1990) Role of the color-opponent and broad-band channels in vision. Vis Neurosci 5:321–346
Schurmann FW, Klemm N (1984) Serotonin-immunoreactive neurons in the brain of the honeybee. J Comp Neurol 225(4):570–580. doi:10.1002/cne.902250407
Schurmann FW, Elekes K, Geffard M (1989) Dopamine-like immunoreactivity in the bee brain. Cell Tiss Res 256(2):399–410
Skinner BF (1938) The behavior of organisms. An experimental analysis. Appleton-Century-Crofts, New York
Skorupski P, Chittka L (2011) Is colour cognitive? Optics Laser Technol 43:251–260
Spaethe J, Tautz J, Chittka L (2006) Do honeybees detect colour targets using serial or parallel visual search? J Exp Biol 209:987–993
Spence KW (1937) The differential response in animal to stimuli varying within a single dimension. Psychol Rev 44:430–444
Takeda K (1961) Classical conditioned response in the honey bee. J Insect Physiol 6:168–179
Tang S, Juusola M (2010) Intrinsic activity in the fly brain gates visual information during behavioral choices. PLoS One 5(12):e14455. doi:10.1371/journal.pone.0014455
Tedjakumala SR, Aimable M, Giurfa M (2014) Pharmacological modulation of aversive responsiveness in honey bees. Front Behav Neurosci 7. doi:10.3389/fnbeh.2013.00221
Thamm M, Balfanz S, Scheiner R, Baumann A, Blenau W (2010) Characterization of the 5-HT1A receptor of the honeybee (Apis mellifera) and involvement of serotonin in phototactic behavior. Cell Mol Life Sci 67(14):2467–2479. doi:10.1007/s00018-010-0350-6
van Swinderen B (2007a) Attention-like processes in Drosophila require short-term memory genes. Science 315(5818):1590–1593. doi:10.1126/science.1137931
van Swinderen B (2007b) The attention span of a fly. Fly 1(3):187–189
van Swinderen B (2011) Attention in Drosophila. Int Rev Neurobiol 99:51–85
van Swinderen B, Andretic R (2011) Dopamine in Drosophila: setting arousal thresholds in a miniature brain. Proc Biol Sci 278(1707):906–913
van Swinderen B, Greenspan RJ (2003) Salience modulates 20–30 Hz brain activity in Drosophila. Nat Neurosci 6(6):579–586
von Dobkiewicz L (1912) Beitrag zur Biologie der Honigbiene. Biol Ztrbl 32:664–694
von Frisch K (1914) Der Farbensinn und Formensinn der Biene. Zool Jahrb Abt Allg Zool Physiol Tiere 37:1–238
von Hess C (1913) Experimentelle Untersuchungen ueber den angeblichen Farbensinn von Bienen. Zool Jahrb Abt Allg Zool Physiol 34:81–106
Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vis Res 41(5):639–653
Wyszecki G, Stiles WS (1982) Color science: concepts and methods, quantitative data and formulae, vol 2. Wiley, New York
Yang EC, Lin HC, Hung YS (2004) Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L. J Insect Physiol 50:913–925
Zheng L, de Polavieja GG, Wolfram V, Asyali MH, Hardie RC, Juusola M (2006) Feedback network controls photoreceptor output at the layer of first visual synapses in Drosophila. J Gen Physiol 127:495–510
Acknowledgments
We thank two anonymous reviewers for comments and corrections on a previous version of this work. This work was supported by the French National Research Agency (ANR; grant MINICOG to M.G.) and the Human Frontier Science Program (HFSP). Martin Giurfa thanks the Institut Universitaire de France, the French Research Council (CNRS) and the University Paul Sabatier of Toulouse for support.
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Avarguès-Weber, A., Giurfa, M. Cognitive components of color vision in honey bees: how conditioning variables modulate color learning and discrimination. J Comp Physiol A 200, 449–461 (2014). https://doi.org/10.1007/s00359-014-0909-z
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DOI: https://doi.org/10.1007/s00359-014-0909-z